Hindawi Publishing CorporationJournal of Parasitology ResearchVolume 2013 Article ID 420928 12 pageshttpdxdoiorg1011552013420928
Research ArticleFifteen Years of Annual Mass Treatment ofOnchocerciasis with Ivermectin Have Not InterruptedTransmission in the West Region of Cameroon
Moses N Katabarwa1 Albert Eyamba2 Philippe Nwane2 Peter Enyong3 Joseph Kamgno4
Thomas Kueteacute5 Souleymanou Yaya6 Rosalie Aboutou7 Leacuteonard Mukenge8
Claude Kafando8 Coulibaly Siaka8 Salifou Mkpouwoueiko7 Demanga Ngangue9
Benjamin Didier Biholong7 and Gervais Ondobo Andze7
1 The Carter Center Atlanta GA USA2The Carter Center Yaounde Cameroon3 Research Foundation for Tropical Diseases and Environment Buea Cameroon4 Filariasis Research Centre Yaounde Cameroon5 Faculty of Medicine and Pharmaceutical Sciences University of Douala Douala Cameroon6Ministry of Public Health North Region Garoua Cameroon7Ministry of Public Health Yaounde Cameroon8African Programme for Onchocerciasis Control Ouagadougou Burkina Faso9Ministry of Public Health West Region Bafoussam Cameroon
Correspondence should be addressed to Moses N Katabarwa mkatabaemoryedu
Received 17 December 2012 Revised 18 March 2013 Accepted 25 March 2013
Academic Editor Wej Choochote
Copyright copy 2013 Moses N Katabarwa et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited
We followed up the 1996 baseline parasitological and entomological studies on onchocerciasis transmission in eleven health districtsin West Region Cameroon Annual mass ivermectin treatment had been provided for 15 years Follow-up assessments which tookplace in 2005 2006 and 2011 consisted of skin snips for microfilariae (mf) and palpation examinations for nodules Follow-upSimulium vector dissections for larval infection rates were done from 2011 to 2012 mf prevalence in adults dropped from 687to 114 and nodule prevalence dropped from 659 to 121 The decrease of mf prevalence in children from 292 to 89 wasevidence that transmission was still continuing mf rates in the follow-up assessments among adults and in children levelled outafter a sharp reduction from baseline levels Only three health districts out of 11 were close to interruption of transmission Evidenceof continuing transmission was also observed in two out of three fly collection sites that had infective rates of 019 and 018 andATP of 70 (Foumbot) and 300 (Massangam) respectively Therefore halting of annual mass treatment with ivermectin cannot bedone after 15 years as it might escalate the risk of transmission recrudescence
1 Introduction
Onchocerciasis a leading cause of blindness is due to humaninfection with Onchocerca volvulus a parasitic worm thatforms nodules under the skin The female worms producemicrofilariae (mf) that live in the nodules inflame the skinand enter the eyes giving rise to inflammatory lesionsThemfwhich are picked up by Simulium flies during a blood meal
develop into L1 L2 and L3 larval stages The L3 (infective)larvae may be passed on to others on subsequent bites thuscompleting the life cycle Black flies breed in fast flowingrivers and streams lending the name ldquoriver blindnessrdquo to thecondition Ivermectin is a safe and effective microfilaricidaldrug that has been donated by Merck amp Co (Mectizan) since1987 for mass treatment of onchocerciasis This medicinekills the microfilaria and reduces the risk of developing eye
2 Journal of Parasitology Research
and skin diseases associated with the infection Ivermectinalso reduces the fecundity of adult worms and apparentlyshortens their life span [1] However treatment may be givenfor undetermined period of time in order to effect cure [2 3]
Onchocerciasis control in Africa has been very successfulover the last two decades In West Africa the OnchocerciasisControl Programme (OCP) eliminated onchocerciasis as apublic health problem from the savanna areas of 11 countriesthrough vector control and ivermectin treatment before itsclosure in 2002 However surveillance and mass treatmentwith ivermectin activities are still going on [4 5] OutsideOCP areas control of onchocerciasis in Africa is the respon-sibility of the African Programme forOnchocerciasis Control(APOC) a partnership of the World Bank World HealthOrganisation a coalition of Non-Governmental Develop-ment Organisations and affected African countries whichwas established in December 1995 Currently over 68 millionpeople are being treated with a single annual dose of iver-mectin every year in Africa [6 7]
The goal of APOC was to establish a mechanism forsustained delivery of an annual dose of ivermectin therebyachieving reduction of prevalence of onchocerciasis to apoint where the disease was no longer of public health orsocioeconomic concern However the APOC goal of elim-inating onchocerciasis as a public health problem (EPHP)was not quantitatively defined but logically taken to be whenprevalence is driven below the original baseline thresholdrequired to launch the mass ivermectin treatment programwhich is an onchocercal nodule rate ge20 or an mf ratege40 [8] Yet achieving EPHP as defined at these levels didnot necessarily indicate interruption of transmission In casetransmission is not interrupted halting mass treatment mayresult into disease recrudescence [8 9]
Onchocerciasis control in West Region began in 1996withCarterCenter andLionsClubs International Foundation(LCIF) assistance through a single annual dose of ivermectinas recommended by World Health Organisation Later in1998 the region began receiving additional funds fromAPOC for a period of five years for the implementationof community directed treatment with ivermectin (CDTI)for onchocerciasis control that was later to be sustained bythe government of Cameroon The five years of fundingwere followed by support for advocacy and replacement ofcapital equipment for three more years The government ofCameroon did not bridge the financial gap and take over theproject as expected [10] Therefore Carter Center continuedits technical and financial assistance to the CDTI activities tothe West Region APOC continued to provide limited fundsfor specific activities but onlywhen theywere deemed criticalfor sustainability of CDTI activities
The recent study in hyperendemic foci in Mali and Sene-gal showed that 15 to 17 years of annual ivermectin treatmenthad eliminated onchocerciasis transmission and that masstreatment could be safely stopped [11]This provided evidencethat in some areas an annual dose of ivermectin couldeliminate onchocerciasis The two criteria used by Diawaraet al to make this determination were entomological (lt05infected flies1000) and epidemiological (lt5 mf prevalencein all communities examined and lt1 in 90 communities
examined) However in the south of the Rio Falema focusthere were seven villages with mf prevalence between 1and 13 after 15ndash17 years of annual treatment that were notdiscussed in the paper This important report called for addi-tional studies in areas with similar durations of treatment todetermine if other successes could be documented across var-ious onchocerciasis ecological transmission zones in AfricaIn response to this report an impact study conducted inNorth Region of Cameroon showed substantial reductionin mf and nodule prevalences in three health districts thathad received up to 17 years of annual mass treatment withivermectin [8] Results of this study revealed that while theonchocerciasis foci in the health districts of Tchollire and ReyBouba appeared to fulfill the Diawara criteria of eliminationin theHealthDistrict of Touboro transmissionwas still goingon The objective of the present study was to determinewhether 15 years of annual treatment with ivermectin inWestRegion a different ecological setting had interrupted thetransmission of onchocerciasis as had been observed in Maliand Senegal [11]
2 Materials and Methods
21 Study Area West Region is close to 14000 km2 of terri-tory located in the central-western portion of the Republic ofCameroon (Figure 1) It borders the Northwest Region to thenorthwest the Adamawa Region to the northeast the CentreRegion to the east and southeast the Littoral Region to thesouthwest and the Southwest Region to the west The WestRegion is the smallest of Cameroonrsquos ten regions in area yetit has the highest population density with a total populationof about 1699000 people living in 20 health districts Themountainous terrain creates many perennial fast-runningrivers that support breeding of black flies which transmitonchocerciasis throughout the year The vegetation consistsof thick forest in the western and eastern parts of the regionwhile the middle part is a transition from forest to savannahwoodlandThemain vector of onchocerciasis inWest RegionofCameroon is Simulium squamosum amember of Simuliumdamnosum complex
22 History of Mass Treatment with Ivermectin Annualmass treatment with ivermectin commenced in 1996 andwas carried out annually through 2010 in all the 20 healthdistricts Validation of treatment coverage through house-hold face-to-face interviews was conducted every year from2003 to 2010 in order to ensure that what was reportedwas correct This also presented opportunities to identifyissues that could be improved upon in order to attain andsustain the desired treatment coverage of at least 90 ofthe ultimate treatment goal (UTG) UTG is the sum of alleligible persons for treatment (minus children lt5 years)among the total number of people at risk living in all at-risk communities in the onchocerciasis endemic area thatthe program ultimately has to treat [12] The individuals inthe samples selected for interviews were obtained throughmultistage random sampling in a homogenous populationat 95 confidence level where a plusmn5 sampling error was
Regional border Health district border Fly collection site 1996
Fly collection site 2011 Community assessed in 1996 Community assessed in 2011
West Region
North-West
Littoral
Far-North
North
CentreCameroonAdamaoua
Scale 1800 0000 5 10 20 30
N
E
S
W
(km)
South-WestRegion
LittoralRegion
Bangourain
FoumbanMatoupou-Chefferie
KouoptamoGalim
Mbouda
Batcham
Dschang
Massangam
Foumbot
Njon
Penka MichelBakassa
Bafoussam
Bamendjou Bandjoun
BahamBapi
Bangangte
Santchou Bandja
e
West
Figure 1 Map of West Region of Cameroon showing the study areas
accepted [13] The data was entered and analysed in (Epi InfoVersion 604 CDC Atlanta GA USA) Since every districtand community had equal chances of being selected everyyear the results obtained were considered representative ofthe annual treatment coverage [14ndash16] Annual validation oftreatment coverage reports showed achievement of at least90 of UTG every year (Table 1) Therefore the surveyedtreatment coverage validated the reported treatment coveragefrom 2003 to 2010
23 Baseline Assessments 1996 Before commencement ofmass treatment with ivermectin baseline entomological andparasitological surveys were conducted in this region in 1996with Carter Center support
231 Baseline Parasitological Assessments 1996 Microfilaria(mf) survey Baseline datawere secured from 12 communitiesbelonging to 7 health districts Bafang (3) Baham (1) Banja(1) Bangangte (2) Foumbot (2) Kekem (1) and Penka-Michel (1) After obtaining consent an individualrsquos nameage and gender were recorded on a registration form Adultsof 20 years and above who had lived in their respectivecommunities for at least 10 years were selected for skinsnipping A total of 931 adults from these communities were
assessed for mf Also 185 resident children (102 from onecommunity in Bafang and 83 from two in Foumbot) wereassessed It was not possible to skin snip children in otherbaseline communities Two skin snips were taken one fromthe posterior iliac crest and another from the buttock using acorneoscleral punchThe skin snips were placed immediatelyin wells of microtitration plates containing normal salinesolution and held at room temperature for 12 to 24 hours[16ndash18] The corresponding well numbers were reflected onthe patient form When the plate was full it was sealed witha transparent adhesive tape After 12ndash24 hours the snipswere removed and the fluid from each well was examinedseparately on a slide for microfilaria under high power(40x) magnification The results were expressed for eachindividual as ldquopositiverdquo or ldquonegativerdquo and were recorded inthe registration form Microfilaria prevalence was expressedas a percentage of the number examined [19] Consent wasobtained from individual adults assessed or from parents ofthe children assessed Individuals had the option to opt outwithout fear of repercussions
Nodule Survey A total of 332 adults of 20 years of ageand above who had lived in the area for at least 10 yearswere examined for nodules from the same communities that
4 Journal of Parasitology Research
Table 1 Comparing reported and validated (through surveys) UTG treatment coverage in West Region from 2003 to 2010
were assessed for mf Every participant was examined in awell-lit private room Trained health workers performed apalpation examination on the partially undressed participantpaying attention to bony prominences of the torso iliac crestsand upper trochanter of the femurs Onchocercal noduleswere identified clinically as being firm painless and mobile[19ndash21] Results were recorded on the form as ldquopositiverdquo orldquonegativerdquo Nodule prevalence was expressed as a percentageof the total number of persons examined
232 Entomological Survey Fly collection was carried out inBafang and Foumbot for a period of one month Potential flycollectors of at least 20 years of age were fully informed of thenature of work and the possibility of opting out of the studyif they wished so at any time without any repercussionsThecollectors worked 2 days in Bafang and 15 days in Foumbot inMay 1996 near the river banks where they exposed their legsin shifts from 0600 to 1200 and from 1200 to 1800 hours [19]As female Simulium flies seeking a blood meal settled on theexposed legs suction tubes were used to catch them beforethey bit Using a dissecting microscope (40x magnification)an experienced dissector opened the vector fliesrsquo abdomensthoraxes and heads Dissected flies were then examinedunder a light microscope in order to identify the presence ofinfection and to count the number of larval stages (L1 L2 andL3)when present Since fly collection lasted onemonth it wasnot possible to determine the annual transmission potential(ATP) Infective flies were defined as flies with L3s in the head[22 23]
Monthly biting rate (MBR) was calculated as per thestandard method as
MBR = (Number of flies collected
times number of days in the month)
times (Number of fly collection days)minus1
(1)
24 Follow-Up Assessments
241 Parasitological Assessments 2005 2006 and 2011 Base-line mf rates in the sentinel communities were followed up inonly 9 sentinel communities in 2005 threemonths aftermasstreatment with ivermectin in 2006 six months after andelevenmonths after treatment in 2011Three baseline sentinelcommunities (Foundjanti in Bafang Bapi in Baham andBakassa in Penka Michel) were not assessed in 2005 as theywere inaccessible as a result of heavy rains and the status quowasmaintained in 2006 A total of 878 and 780 resident adultswere assessed in 2005 for mf and nodules respectively Also403 resident children (le10 years old) were assessed for mf
In 2006 assessment for mf and nodules covered 782resident adults Skin snips were obtained from only 134children Skin snipping performed in 2005 and 2006 involvedtwo skin snips one taken from the posterior iliac crest andanother from the buttock with the help of a disposable steriledermal hook and a blade The hook and blade used for eachparticipant were safely discarded [16]
In 2011 2703 resident adults from 16 communitiesincluding 11 baseline communities were examined for mfand nodules Since the Ministry of Health wanted to knowthe situation inside and outside the sentinel communitiesfour additional high risk communities were considered in2011 assessments Also 626 resident children (le10 years)from 11 communities (including three baseline communities)were examined for mf mf prevalence was expressed as apercentage of the number examined Due to heavy rainsBakambe one of the original sentinel communities wasinaccessible and therefore was not assessed Nodule palpationwas not followed up in the present study as it had not beendone in children at baseline
The comparison of baselinewith follow-up results in 2005(three months after treatment) in 2006 (six months aftertreatment) and in 2011 (11 months after treatment) was donein order to shed light on the dynamics ofOnchocerca volvulusinfection with annual mass treatment The comparison ofbaseline results to follow-up assessments was possible as onlyqualitative (presence or absence of mf or nodules) data wasconsidered
242 Follow-Up Entomological Assessment Black fly collec-tion was carried out at three sites in Bafang Foumbot andMassangam health districts for 3 days during the third weekof eachmonth fromMarch 2011 to February 2012The criteriafor selection of potential fly collectors set during baselineentomological assessment were followed Bafang collectionsite is located in extreme west of the region Foumbot in themiddle and Makouopsap in the extreme east of the region
Landing female Simulium flies were collected and imme-diately dissected in order to determine the parous rate Theremains of the dissected parous flies were preserved in a tubecontaining 70 ethanol The tubes were labeled by collectionsite date and time Simulium flies were then grouped inbatches up to 50 and sent to the laboratory where theywere stained with Mayerrsquos hematoxylin and fully dissected insearch for onchocercal larval stages (L1 L2 and L3) in theabdomen the thorax and the head [24] Infective flies weredefined as flies with L3 in the head as in the baseline surveysmentioned previously [18] This information was used to cal-culate the monthly and annual transmission potentials whichare the indicators of transmission The annual transmission
Journal of Parasitology Research 5
potential (ATP) was calculated as the sum of the individualmonthly transmission potentials (MTPs) over the period of ayear [23]
Data Analysis Parasitological data from adults and childrenas well as entomological data were entered and analysedgraphically in Microsoft Excel and Epi Info CDC AtlantaGA USA for chi square test of independence The ento-mological data was analysed and graphically illustrated inMicrosoft Excel
Ethical Approval All the surveys from the baseline to thefollow-up studies were approved by the Ministry of PublicHealth of Cameroon and the National Ethical Committeein Yaounde In addition the Emory University InstitutionalReview Board (eIRB-11 438) approved and considered themas nonresearch but routine program evaluation The fol-lowup of 2011 was also conducted under the auspices ofWorldHealth Organisation All assessed individuals had the libertyof opting out of assessments if they wished so without anyrepercussions
3 Results
31 Microfilaria (mf) and Nodule Prevalences Among adultsthe mf rate reduced by about 91 from baseline level of667 (range 531 to 881) in 1996 to 60 (range 14 to183 119875 lt 00001) in 2005 three months after ivermectintreatment However mf rate increased in 2006 six monthsafter ivermectin treatment to 139 (range 21 to 336)although it was not statistically different from 2005 mf rate119875 lt 0053 The decrease of mf rate 139 in 2006 to114 (range 0 to 596) in 2011 was also not significant(119875 lt 0053) (Table 2 and Figure 2) Only one communityhad 0 mf rate while six communities had mf rates above10 and two above 40 after 15 years of annual masstreatment Persistent high mf rates were observed in com-munities of Babouantou (214) in Bandja health districtNjone (419) in Foumbot health district and Makouopsap(596) in Massangam health district However there werecommunities (Bakonti in Bafang Health District Folap inFoumban Mbafam in Kekem and Njisseng in Kouptamo)which registered mf rates below 5 in adults
In children overall baselinemf rate of 292 (range 127to 518) reduced to 42 (range 0 to 250) in 2005 withan 856 reduction 119875 lt 00001 (Table 3 and Figure 2)However there was no significant difference between mf rate42 in 2005 and 45 in 2006 three months and six monthsrespectively after mass treatmentThere results for 2006 werealso not significantly different from mf rate 89 obtainedin 2011 eleven months after treatment (Table 3 and Figure 2)There were children in 2 (133) communities with mf ratesabove 20 (Njone 252 and Makouopsap 656) EvenBabouantou with mf rate of 158 was considered high fora program with 15 years of annual treatment In Ndjipta III ofBangangte Health District Folap of Foumban and Mbafamof Kekem mf rates among children were 06 or less
The overall baseline nodule rate in adults of 663 (range40 to 897) declined to 95 (range 400ndash897) 119875 lt00001 in the 2005This represents a decline of 856Then itincreased to 185 (range 67ndash303) in 2006 and declinedto 121 (range 15ndash434) in 2011 (Table 4) There were9 communities out of 16 with nodule prevalence of at least10 Of particular interest are persistent high nodule ratesin Bakambe (232) and Fondjanti (232) communities ofBafang Health District Fossang-chefferie (173) and Njone(186) in Foumbot health district andMakouopsap (434)in Massangam Health District
32 Entomology Baseline monthly transmission potentialswere 15 in Bafang and 2104 in Foumbot (Table 5) In thefollow-up assessment the infection rates were 02 in BafangHealth District 088 in Foumbot and 067 in MassangamThe infective rates were 0 in Bafang Health District 019in Foumbot and 018 in Massangam Annual biting rateswere 52610 in Bafang 28560 in Foumbot and 125360 inMakouopsap while annual transmission potentials were 070 and 310 respectively Biting was generally throughout theyear although the main peak biting period in Makouopsapwas observed from January to May (Figure 3)
4 Discussion
Annual mass treatment with ivermectin for 15 years hadconsiderably reduced microfilaria and nodule prevalence inall the sentinel communities of West Region of CameroonElimination is considered attained when the microfilariaprevalence in skin snips is less than 5 in sampled communi-ties in less than 1 in 90of sampled communities andwhenentomological criteria of less than 05 infected flies1000 areattained [11] Among adults Foumban Health District wasclose to the epidemiological criterion while Bafang HealthDistrict was not very far from the entomological criterionwith the ATP of 0 mf rate among children in Foumbanand Kekem health districts was zero indicating no recentinfection an indication that interruption of transmissionmay be attained However the mf rates in Baham BanjaBangangte Foumbot andMassangam health districts amongadults and children were still uncomfortably high showingcontinuing transmission In adults nodule rates near orabove the threshold 20 for the mass treatment in somecommunities were of a major concern The infective rateof 018 to 019 and ATP of 70 to 300 confirmed continuingtransmission
One possible explanation for high mf rates in childrenand adults could have been low treatment coverage Howeverthe methodology for validating UTG treatment coveragefollowed standard statistical methods for selecting sampledcommunities and the interviewees This methodology hadbeen tested and used to validate performance of CDTI inCameroon and in other onchocerciasis endemic countries[14 15 25]TheUTG treatment coverage results were also cor-roborated by independent monitoring results in unpublishedreports supported by APOC Therefore there is no reason tobelieve that UTG treatment coverage was low and responsible
6 Journal of Parasitology Research
Table2Com
parin
gmfp
revalencea
mon
gadultsatbaselin
e(1996)a
ndfollo
wup
in2005200
6and2011three
mon
thssix
mon
thsandele
venmon
thsrespectiv
elyafte
rmasstreatment
inWestR
egion
Cameroo
n
Distric
tCom
mun
ityBa
selin
e1996
(119899=931)
Follo
wup
2005(119899=878)
Follo
wup
200
6(119899=782)
Follo
wup
2011(119899=2703)
No
exam
ined
No
positive
mf
positive
No
exam
ined
No
positive
mf
positive
No
exam
ined
No
positive
mf
positive
No
exam
ined
No
positive
mf
positive
Bakassa
6136
590
140
214lowast
972
21
251
1456
Bafang
Bakonti
5236
692
993
30lowast
753
40
338
1236
Fond
janti
124
8770
2125
864
Bakambe
122
65533
105
329lowast
916
66
ND
ND
ND
Baham
Bapi
145
77531
ND
ND
ND
ND
ND
ND
189
21111
Band
jaBa
bouantou
(Batou
la)
6849
721
537
132lowast
7614
184
8418
214
Bang
angte
Batchingou
8461
726
102
11108lowast
8014
175
247
45182
NdjiptaIII
(Fop
-Tchui)
8871
807
781
13lowast
576
105lowastlowast
929
98
Foum
bot
Fossang-
chefferielowast
3228
875
7113
183lowast
7219
264lowastlowast
150
19127lowastlowastlowast
Njone
5952
881
135
1181lowast
122
41336lowastlowast
167
70419lowastlowastlowast
Kekem
Mbafam
3927
692
952
21lowast
112
436
163
849
Penk
a-Michel
Bakassa
5732
561
ND
ND
ND
ND
ND
ND
195
736
Foum
ban
Folap
ND
ND
ND
ND
ND
ND
ND
ND
ND
265
000
Kouo
ptam
oNjisseng
ND
ND
ND
ND
ND
ND
ND
ND
ND
168
530
Malantouen
Matou
pou
ND
ND
ND
ND
ND
ND
ND
ND
ND
170
1376
Massang
amMakou
opsap
ND
ND
ND
ND
ND
ND
ND
ND
ND
9959
596
931
621
667
878
5360lowast
782
109
139
2703
308
114
NDnot
done
lowastSign
ificant
(119875lt005)mdash
follo
wup
2005
comparedwith
theb
aseline
lowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2006
comparedwith
2005
follo
wup
lowastlowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2011comparedwith
2006
follo
wup
Journal of Parasitology Research 7
667
6139 114
292
42 45 89
01020304050607080
m
f pre
vale
nce
AdultsChildren
1996119899 = 931 2005 (3 months after treatment)
119899 = 878
2006 (6 months
Baseline Followup
after treatment)119899 = 782
2011 (11 monthafter treatment)
119899 = 2703
Figure 2 Comparison of mf rates among adults and children atbaseline 1996 with followup surveys in 2005 2006 and 2011 inWestRegion of Cameroon
for failure to attain optimal parasitological and entomologicalimpacts
High vector density and mf rates suggest that the forceof transmission may have been very high and most likely thereason for the results obtained [26]The present study did notconsider the standardmeasure of intensity of infection whichis related to force of infection community mf load (CMFL)This requires a calculation that involves weighing the snipand counting the microfilaria which was not done [19] Werecommend that it should be done in future studies
In Massangam Health District it is possible that high mfand nodule rates in the follow-up assessments may be dueto the ldquoforce of infectionrdquo across the neighbouring CentralRegion where peer-reviewed studies indicate considerableonchocerciasis transmission [27 28] River Nja a tributary ofRiver Noun and River Kichi a tributary of River Mbam areknown black fly breeding sites responsible for cross-bordertransmission between West and Central regions Thereforewe recommend collaboration between the regions in order tounderstand the limits of cross-border onchocerciasis affectedarea and harmonize intervention if elimination becomes thegoal in Cameroon
Another possible explanation for high mf rates couldbe related to suboptimal response to ivermectin observedin some onchocerciasis endemic areas of Ghana The adultfemale O volvulus worms were resuming microfilaria repro-duction more rapidly after ivermectin treatment than wouldnormally be expected suggesting possible development ofresistance to ivermectin [29ndash31] We recommend that thepossibility of suboptimal response to ivermectin in WestRegion be investigated
The microfilaria rate in adults and children tended tofollow the expected trend where a single annual dose ofivermectin over a number of years significantly reduced thelow mf rates that tend to persist [3] The observed patternindicated a tendency for themf rate to raise a fewmonths aftermass treatment until another dose of ivermectin is providedconfirming that microfilarial production is not cumulativelyreduced by several annual ivermectin treatments [32] Themf rate trend at three six and eleven months after mass
treatment is usually not different from the infection ratewithin the flies over a period after mass treatment withivermectin [33] Ivermectin kills existing microfilariae andtends to exert an ldquoembryostatic effectrdquo by which microfilarialproduction is suppressed over a few weeks after treatmentbut then after the mf rate begins to increase [32] Underfavourable ecological conditions interruption of onchocer-ciasis transmission with annual mass treatment may requiremany more years before it is attained
As for twice yearly treatment with ivermectin or whenit is coupled with vector control infection rate continuedto fall implying that interruption of transmission could berapidly attained [1 33 34] We recommend that West Regionof Cameroon should consider twice yearly treatment or atleast annual treatment with targeted vector control
In the present study some communities (Folap andNjisseng) in Foumban and Kouoptamo health districts hadmf rates lower than 5 in adults and 0 in children Inthese communities the Diawara et al criteria are closeto being attained and yet with low levels of infectiontransmission is much more efficient than at high levels ofinfection [35ndash37] Thus if low levels of infection are notdetected and controlled they could result in fast diseaserecrudescence Skin snip (microscopy) has low sensitivity ofless than 20 at less than 20 nodule rate and the resultsobtained may not reflect correct mf endemicity levels [38]Therefore interventions in these health districts cannot behalted as disease recrudescence could occur [29 30] Whereinterruption of transmission of onchocerciasis is the objectivewe recommend a search for affordable less intrusive rapidsensitive and highly specific diagnostic tools for low levelinfections in order to validate interruption of onchocerciasistransmission
The APOC threshold for launching mass treatment isan onchocercal nodule rate of ge20 Fondjanti community(Bandja Health District) with nodule rate of 23 and mfrate of 64 would pass for mass treatment while Njonecommunity (Foumbot Health District) with nodule rate of186 and mf rate of 419 would fail [39] Nodule rate couldalso be confounded by the presence of ganglia and Taeniasolium [40 41] The entomological results showed that therisk of contracting onchocerciasis in FoumbotHealthDistrictwas higher than in Bafang Health District confirming thereliability of mf rates compared with nodule rates With theshift from control to elimination of onchocerciasis in Africawe recommend that nodule prevalence should not be usedto determine whether an endemic area should receive masstreatment or not
Annual biting rates with the range of 28560 to 125380are some of the highest observed globally Yet infective ratein Bafang from the western part of the region was zerojustifying low mf rates (06 in children and a mean of52 in adults) The question would be whether annual masstreatment could be withdrawn without resulting in diseaserecrudescence Existing low level transmission with the highannual biting rate of 52610 could still result in onchocerciasisrecrudescence It was also evident in this study that one-month baseline entomological data was likely to miss peakbiting transmission pattern of Simulium vectors and the
8 Journal of Parasitology Research
Table3Com
parin
gmfp
revalencea
mon
gchild
renatbaselin
e(1996)and
follo
wup
in2005200
6and2011three
mon
thssix
mon
thsandele
venmon
thsrespectiv
elyafterm
asstreatment
inWestR
egion
Cameroo
n
Distric
tCom
mun
ityBa
selin
e1996
(119899=185)
Follo
wup
2005(119899=403)
Follo
wup
200
6(119899=134)
Follo
wup
2011(119899=626)
No
Exam
ined
No
positive
mf
positive
No
Exam
ined
No
positive
mf
positive
No
Exam
ined
No
positive
mf
positive
Noexam
No
positive
mf
positive
Bafang
Bakonti-B
akassa
102
13127
740
0lowast43
000
167
106
Bafang
Batchieu
704
57
40
00
Baham
Bapi
ND
ND
ND
292
69
Band
jaBa
bouantou
(Batou
la)lowast
ND
ND
ND
647
109
143
214
193
158
Bang
angte
Batchingoulowast
ND
ND
ND
241
42
152
133
211
48
Bang
angte
NdjiptaIII(Fo
p-Tchu
i)lowastND
ND
ND
632
32
50
00
250
00
FossangCh
efferie
ND
ND
ND
380
00
40
00
252
80
Foum
bot
Njone
2019
950
123
25lowast
161
63
8224
293lowastlowastlowast
Foum
bot
Kousang-Malanden
6322
349
ND
ND
ND
ND
ND
ND
ND
ND
ND
Kekem
Mbafamlowast
ND
ND
ND
580
00
330
00
200
00
Penk
a-Michel
Bakassa
ND
ND
ND
ND
ND
ND
ND
ND
ND
741
14Fo
umban
Folap
ND
ND
ND
ND
ND
ND
ND
ND
ND
108
000
Kouo
ptam
oNjisseng
ND
ND
ND
ND
ND
ND
ND
ND
ND
241
42
Massang
amMakou
opsap
ND
ND
ND
ND
ND
ND
ND
ND
ND
3221
656
12185
5429
240
317
42lowast
134
645
626
5689
NDnot
done
lowastSign
ificant
(119875lt005)mdash
follo
wup
2005
comparedwith
theb
aseline
lowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2006
comparedwith
2005
follo
wup
lowastlowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2011comparedwith
2006
follo
wup
Journal of Parasitology Research 9
Table4
Com
parin
gnod
ulep
revalencea
mon
gadu
ltsatbaselin
e(1996)and
follo
wup
in2005200
6and2011three
mon
thssix
mon
thsandele
venmon
thsrespectiv
elyafterm
asstreatment
inWestR
egion
Cameroo
n
Distric
tCom
mun
ityBa
selin
e1996
(119899=305)
Follo
wup
2005(119899=780)
Follo
wup
200
6(119899=782)
Follo
wup
2011(119899=2703)
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
Bafang
Bakassa
2716
593
139
110
79lowast
9711
113
251
2184
Bakonti
2711
407
9850
51lowast
755
67
338
36107
Fond
janti
2719
704
125
29232
Bakambe
2719
704
105
110
105lowast
9113
143
125
29232
Baham
Bapi
2915
517
ND
ND
ND
ND
ND
ND
189
1579
Band
jaBa
bouantou
(Batou
la)
2616
615
6150
82lowast
7618
237lowastlowast
8412
143
Bang
angte
Batchingou
2922
759
101
160
158lowast
8023
288lowastlowast
247
29117lowastlowastlowast
NdjiptaIII(Fo
p-Tchu
i)29
23793
7850
64lowast
578
140lowastlowast
929
98
Foum
bot
Fossang-chefferie
2824
857
7170
99lowast
7218
250lowastlowast
150
26173lowastlowastlowast
Njone
2926
897
3490
265lowast
122
37303
167
31186lowastlowastlowast
Kekem
Mbafam
2417
708
9350
54lowast
112
12107lowastlowast
163
27166
Penk
a-Michel
Bakassa
3012
400
ND
ND
ND
ND
ND
ND
195
1577
Foum
ban
Folap
ND
ND
ND
ND
ND
ND
ND
ND
ND
265
415
Kouo
ptam
oNjisseng
ND
ND
ND
ND
ND
ND
ND
ND
ND
168
636
Malantouen
Matou
pou
ND
ND
ND
ND
ND
ND
ND
ND
ND
170
953
Massang
amMakou
opsap
ND
ND
ND
ND
ND
ND
ND
ND
ND
9943
434
332
220
663
780
7495lowast
782
145
185lowastlowast
2828
341
121lowastlowastlowast
NDnot
done
lowastSign
ificant
(119875lt005)mdash
follo
wup
2005
comparedwith
theb
aseline
lowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2006
comparedwith
2005
follo
wup
lowastlowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2011comparedwith
2006
follo
wup
10 Journal of Parasitology Research
Table 5 Comparing baseline entomological data of 1996 at two fly collection sites and three during 2011
Monthyear of black fly collection Baseline May 1996 Followup 2011Black fly collection sites Bafang (Basseu) Foumbot (Maka) Bafang Foumbot MassangamNumber of Simulium caught 5 166 5261 2856 12538Number of Simulium dissected 5 142 5261 2856 12138Number of parous flies 1 97 1502 1028 2845Parous rate () 20 683 285 36 234Number of Simulium flies infected (L1 L2 L3] 1 12 3 9 19Infection rate () 2000 845 020 088 067Number of Simulium flies infective L3 larval stage in the head 20 2 0 2 5Infective rate () 200 211 000 019 018Monthly biting rate per person 750 166000 na na naMonthly transmission potentiallowast 150 21040 na na naAnnual biting rate per person Na na 52610 28560 125380Annual transmission potential Na na 0 70 310
0
500
1000
1500
2000
2500
3000
3500
4000
No
of fl
ies c
olle
cted
BafangFoumbotMakouopsap
MarApr2011 2012
May Jun Jul AugSeptOctNovDec Jan Feb
Figure 3 Monthly seasonal biting of Simulium flies at 3 fly catchingsites in West Region
calculation ofATPTherefore collection of entomological dataover several months is required as reflected in the follow-up study The information on peak biting and transmissionpatterns could effectively be utilized for ivermectin treatmentfor maximum impact on transmission especially where theforce of transmission is considerably high if elimination ofonchocerciasis is the goal In the follow-up survey it is onlyat Bafang fly collection site that the entomological criterionfor interruption of transmission was met with an ATP of zero[42]
The present study however did not perform moleculartesting in order to determine if the L3 larvae wereO volvulusor another (animal) Onchocerca species Based on humanmf prevalence in skin and infections in children we thinkthat there is likelihood that some of the larvae observedin vectors were O volvulus However a study conducted inNorth Region of Cameroon during the 1990s showed that
33 of infective larvae in S damnosum were O volvuluswhereas 65 were O ochengi and 2 were O ramachandrini[43] It is until such a study is conducted in West Region ofCameroon that we will know the extent to which O ochengiis responsible for a significant proportion of infected flies thatcould confound the infection rate there
Our findings reflecting an observation period of 15 yearsshowed that annual mass treatment with ivermectin may notinterrupt the transmission of onchocerciasis in all differentecological zones of West Region Therefore the intensive useof ivermectin is recommended if interruption of transmissionof onchocerciasis is to be attained [1]
5 Conclusion
Annual mass treatment with ivermectin through commu-nity-directed treatment was preferred as a good and lessexpensive method for controlling onchocerciasis in endemicAfrican countries with assistance from the African Pro-gramme for Onchocerciasis Control The studies in MaliSenegal and Nigeria have shown that an annual dose ofivermectin had interrupted transmission of the disease andall interventions could be halted without the risk of diseaserecrudescence However an annual dose of ivermectin hasnot interrupted transmission after 15 years of mass treatmentin some areas in West Region of Cameroon just like inNorth region [8] It has also been less effective in someonchocerciasis endemic areas in Ghana The present paperagain highlights the fact that for interruption of onchocer-ciasis transmission feasible and different but complementarystrategic options should be adopted as elimination becomesthe goal in Africa
Acknowledgments
The investigators would like to acknowledge the staff ofMinistry of Health at the national regional and healthdistrict levels in West Region along with Carter CenterCameroon Office for mobilizing and educating selected
Journal of Parasitology Research 11
communities and providing policy and administrative sup-port The involvement of community members in selectedcommunities in mf and nodule assessments and Simulium flycollection is highly appreciated The Carter Center the LionsClubs International Foundation (LCIF) and the African Pro-gramme for onchocerciasis Control (APOC) which fundedthe CDTI activities and the surveys are also highly appreci-ated
References
[1] E W Cupp and M S Cupp ldquoShort report impact of iver-mectin community-level treatments on elimination of adultOnchocerca volvulus when individuals receive multiple treat-ments per yearrdquoThe American Journal of Tropical Medicine andHygiene vol 73 no 6 pp 1159ndash1161 2005
[2] H R Taylor M Pacque B Munoz and B M Greene ldquoImpactof mass treatment of onchocerciasis with ivermectin on thetransmission of infectionrdquo Science vol 250 no 4977 pp 116ndash118 1990
[3] G J J M Borsboom B A Boatin N J D Nagelkerkeet al ldquoImpact of ivermectin on onchocerciasis transmissionassessing the empirical evidence that repeated ivermectin masstreatmentsmay lead to eliminationeradication inWest-AfricardquoFilaria Journal vol 2 article 8 2003
[4] A D Hopkins ldquoIvermectin and onchocerciasis is it all solvedrdquoEye vol 19 no 10 pp 1057ndash1066 2005
[5] L Yameogo ldquoSpecial intervention zonesrdquo Annals of TropicalMedicine and Parasitology vol 102 supplement 1 pp 23ndash242008
[6] D H Molyneux and M N Malecela ldquoNeglected tropicaldiseases and themillennium development goals why the ldquootherdiseasesrdquo matter reality versus rhetoricrdquo Parasites amp Vectorsvol 4 2011
[7] WHOReportAcceleratingWorkToOvercome theGlobal Impactof Neglected Tropical Disease A Roadmap For Implementationvol 1211WorldHealthOrganization 20AvenueAppia GenevaSwitzerland 2012
[8] M N Katabarwa A Eyamba P Nwane et al ldquoSeventeenyears of annual distribution of ivermectin has not interruptedonchocerciasis transmission in North Region Cameroonrdquo TheAmerican Journal of Tropical Medicine and Hygiene vol 85 no6 pp 1041ndash1049 2011
[9] B A Boatin and F O Richards ldquoControl of onchocerciasisrdquoAdvances in Parasitology vol 61 pp 349ndash394 2006
[10] D R Hopkins F O Richards and M Katabarwa ldquoWhitheronchocerciasis control in Africardquo American Journal of TropicalMedicine and Hygiene vol 72 no 1 pp 1ndash2 2005
[11] L Diawara M O Traore A Badji et al ldquoFeasibilityof onchocerciasis elimination with ivermectin treatment inendemic foci in Africa first evidence from studies in Mali andSenegalrdquo PLoS Neglected Tropical Diseases vol 3 no 7 articlee497 2009
[12] F O Richards E S Miri M Katabarwa et al ldquoThe carter cen-terrsquos assistance to river blindness control programs establish-ing treatment objectives and goals for monitoring ivermectindelivery systems on two continentsrdquo The American Journal ofTropical Medicine and Hygiene vol 65 no 2 pp 108ndash114 2001
[13] P Salant and D A Dilman How to Conduct Your Own SurveyJohn Wiley amp Sons 1994
[14] M N Katabarwa P Habomugisha and F O Richards ldquoImple-menting community-directed treatmentwith ivermectin for the
control of onchocerciasis in Uganda (1997-2000) an evalua-tionrdquo Annals of Tropical Medicine and Parasitology vol 96 no1 pp 61ndash73 2002
[15] E C Emukah U Enyinnaya N S Olaniran et al ldquoFactorsaffecting the attrition of community-directed distributors ofivermectin in an onchocerciasis-control programme in the Imoand Abia states of south-eastern Nigeriardquo Annals of TropicalMedicine and Parasitology vol 102 no 1 pp 45ndash51 2008
[16] A Prost and J Prodrsquohon ldquoLe diagnostique parasitologique delrsquoonchocercose revue critique des methods en usagerdquoMedicineTropicale vol 38 pp 519ndash532 1978
[17] H Schulz Key ldquoA simple technique to assess the total number ofOnchocerca volvulusmicrofilariae in skin snipsrdquo Tropenmedizinund Parasitologie vol 29 no 1 pp 51ndash54 1978
[18] WHO Report ldquoOnchocerciasis and its control Report of aWHO Expert Committee on Onchocerciasis Controlrdquo TechRep 852 Geneva Switzerland 1995
[19] WHO Report Strategies For Ivermectin Distribution ThroughPrimaryHealth Care SystemWHOPHL91 24WHOGenevaSwitzerland 1991
[20] E J Albiez D W Buttner and B O L Duke ldquoDiagnosisand extirpation of nodules in human onchocerciasisrdquo TropicalMedicine and Parasitology vol 39 no 4 pp 331ndash346 1988
[21] P Ngoumou J F Walsh and J M Mace ldquoA rapid mappingtechnique for the prevalence and distribution of onchocerciasisa Cameroon case studyrdquo Annals of Tropical Medicine andParasitology vol 88 no 5 pp 463ndash474 1994
[22] M Katabarwa A W Onapa and B Nakileza ldquoRapid epidemi-ological mapping of onchocerciasis in areas of uganda whereSimulium neavei SL is the vectorrdquo East African Medical Journalvol 76 no 8 pp 440ndash446 1999
[23] J F Walsh J B Davies R Le Berre and R Garms ldquoStandard-ization of criteria for assessing the effect of Simulium control inonchocerciasis control programmesrdquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 72 no 6 pp 675ndash676 1978
[24] J B Davies ldquoA rapid staining and clearing technique for detect-ing filarial larvae in alcohol-preserved vectorsrdquo Transactions ofthe Royal Society of Tropical Medicine and Hygiene vol 89 no3 p 280 1995
[25] M Katabarwa P Habomugisha A Eyamba S Agunyo andC Mentou ldquoMonitoring ivermectin distributors involved inintegrated health care services through community-directedinterventionsmdasha comparison of Cameroon and Uganda expe-riences over a period of three years (2004ndash2006)rdquo TropicalMedicine and International Health vol 15 no 2 pp 216ndash2232010
[26] J Remme O Ba K Y Dadzie and M Karam ldquoA force-of-infection model for onchocerciasis and its applications inthe epidemiological evaluation of the onchocerciasis controlprogramme in the volta river basin areardquo Bulletin of the WorldHealth Organization vol 64 no 5 pp 667ndash681 1986
[27] P Barbazan H Escaffre R Mbentengam and M BoussinesqldquoEntomologic study on the transmission of onchocerciasis ina forest-savanna transition area of Cameroonrdquo Bulletin de laSociete de Pathologie Exotique vol 91 no 2 pp 178ndash182 1998
[28] E Cadot P Barbazan andM Boussinesq ldquoGeographical deter-minants of onchocerciasis transmission in a forestsavannahtransition zone two villages of the mbam focusrdquo Sante vol 8no 6 pp 429ndash435 1998
[29] K Awadzi S K Attah E T Addy et al ldquoThirty-monthfollow-up of sub-optimal responders to multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in Ghanardquo
12 Journal of Parasitology Research
Annals of Tropical Medicine and Parasitology vol 98 no 4 pp359ndash370 2004
[30] K Awadzi D A Boakye G Edwards et al ldquoAn investigationof persistent microfilaridermias despite multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in GhanardquoAnnals of Tropical Medicine and Parasitology vol 98 no 3 pp231ndash249 2004
[31] M Y Osei-Atweneboana J K Eng D A Boakye J OGyapong and R K Prichard ldquoPrevalence and intensity ofOnchocerca volvulus infection and efficacy of ivermectin inendemic communities in Ghana a two-phase epidemiologicalstudyrdquoThe Lancet vol 369 no 9578 pp 2021ndash2029 2007
[32] C Bottomley V Isham R C Collins and M G BasanezldquoRates of microfilarial production by Onchocerca volvulus arenot cumulatively reduced by multiple ivermectin treatmentsrdquoParasitology vol 135 no 13 pp 1571ndash1581 2008
[33] R Garms T L Lakwo R Ndyomugyenyi et al ldquoThe elimina-tion of the vector Simulium neavei from the Itwara onchocerci-asis focus in Uganda by ground larvicidingrdquo Acta Tropica vol111 no 3 pp 203ndash210 2009
[34] R Ndyomugyenyi E Tukesiga D W Buttner and R GarmsldquoThe impact of ivermectin treatment alone and when inparallel with Simulium neavei elimination on onchocerciasis inUgandardquo Tropical Medicine and International Health vol 9 no8 pp 882ndash886 2004
[35] H P Duerr and M Eichner ldquoEpidemiology and control ofonchocerciasis the threshold biting rate of savannah onchocer-ciasis in Africardquo International Journal for Parasitology vol 40no 6 pp 641ndash650 2010
[36] K Dietz ldquoDensity-dependence in parasite transmissiondynamicsrdquo Parasitology Today vol 4 no 4 pp 91ndash97 1988
[37] M G Basanez J H F Remme E S Alley et al ldquoDensity-dependent processes in the transmission of human onchocerci-asis relationship between the numbers ofmicrofilariae ingestedand successful larval development in the simuliid vectorrdquoParasitology vol 110 no 4 pp 409ndash427 1995
[38] B A Boatin L Toe E S Alley N J D Nagelkerke GBorsboom and J D F Habbema ldquoDetection of Onchocercavolvulus infection in lowprevalence areas a comparison of threediagnostic methodsrdquo Parasitology vol 125 no 6 pp 545ndash5522002
[39] M Noma B E B Nwoke I Nutall et al ldquoRapid epidemio-logical mapping of onchocerciasis (REMO) its application bythe African programme for onchocerciasis control (APOC)rdquoAnnals of Tropical Medicine and Parasitology vol 96 supple-ment 1 pp S29ndashS39 2002
[40] G Fobi J R M Mbina G Ozoh et al ldquoOnchocerciasis inthe area of Lastourville Gabon Clinical and entomologicalaspectsrdquo Bulletin de la Societe de Pathologie Exotique vol 99no 4 pp 269ndash271 2006
[41] M N Katabarwa A Eyamba M Chouaibou et al ldquoDoesonchocerciasis transmission take place in hypoendemic areasa study from theNorth Region of CameroonrdquoTropicalMedicineand International Health vol 15 no 5 pp 645ndash652 2010
[42] WHO Report Certification of Elimination of Human Onchocer-ciasis Criteria and Procedures Criteria For Certification of Inter-ruption of TransmissionElimination of Human OnchocerciasisWorld Health Organization Geneva Switzerland 2001
[43] R Seidenfaden A Fischer I Bonow D Ekale V Tanya andA Renz ldquoCombined benefits of annual mass treatment withivermectin and cattle zooprophylaxis on the severity of humanonchocerciasis in northern Cameroonrdquo Tropical Medicine andInternational Health vol 6 no 9 pp 715ndash725 2001
and skin diseases associated with the infection Ivermectinalso reduces the fecundity of adult worms and apparentlyshortens their life span [1] However treatment may be givenfor undetermined period of time in order to effect cure [2 3]
Onchocerciasis control in Africa has been very successfulover the last two decades In West Africa the OnchocerciasisControl Programme (OCP) eliminated onchocerciasis as apublic health problem from the savanna areas of 11 countriesthrough vector control and ivermectin treatment before itsclosure in 2002 However surveillance and mass treatmentwith ivermectin activities are still going on [4 5] OutsideOCP areas control of onchocerciasis in Africa is the respon-sibility of the African Programme forOnchocerciasis Control(APOC) a partnership of the World Bank World HealthOrganisation a coalition of Non-Governmental Develop-ment Organisations and affected African countries whichwas established in December 1995 Currently over 68 millionpeople are being treated with a single annual dose of iver-mectin every year in Africa [6 7]
The goal of APOC was to establish a mechanism forsustained delivery of an annual dose of ivermectin therebyachieving reduction of prevalence of onchocerciasis to apoint where the disease was no longer of public health orsocioeconomic concern However the APOC goal of elim-inating onchocerciasis as a public health problem (EPHP)was not quantitatively defined but logically taken to be whenprevalence is driven below the original baseline thresholdrequired to launch the mass ivermectin treatment programwhich is an onchocercal nodule rate ge20 or an mf ratege40 [8] Yet achieving EPHP as defined at these levels didnot necessarily indicate interruption of transmission In casetransmission is not interrupted halting mass treatment mayresult into disease recrudescence [8 9]
Onchocerciasis control in West Region began in 1996withCarterCenter andLionsClubs International Foundation(LCIF) assistance through a single annual dose of ivermectinas recommended by World Health Organisation Later in1998 the region began receiving additional funds fromAPOC for a period of five years for the implementationof community directed treatment with ivermectin (CDTI)for onchocerciasis control that was later to be sustained bythe government of Cameroon The five years of fundingwere followed by support for advocacy and replacement ofcapital equipment for three more years The government ofCameroon did not bridge the financial gap and take over theproject as expected [10] Therefore Carter Center continuedits technical and financial assistance to the CDTI activities tothe West Region APOC continued to provide limited fundsfor specific activities but onlywhen theywere deemed criticalfor sustainability of CDTI activities
The recent study in hyperendemic foci in Mali and Sene-gal showed that 15 to 17 years of annual ivermectin treatmenthad eliminated onchocerciasis transmission and that masstreatment could be safely stopped [11]This provided evidencethat in some areas an annual dose of ivermectin couldeliminate onchocerciasis The two criteria used by Diawaraet al to make this determination were entomological (lt05infected flies1000) and epidemiological (lt5 mf prevalencein all communities examined and lt1 in 90 communities
examined) However in the south of the Rio Falema focusthere were seven villages with mf prevalence between 1and 13 after 15ndash17 years of annual treatment that were notdiscussed in the paper This important report called for addi-tional studies in areas with similar durations of treatment todetermine if other successes could be documented across var-ious onchocerciasis ecological transmission zones in AfricaIn response to this report an impact study conducted inNorth Region of Cameroon showed substantial reductionin mf and nodule prevalences in three health districts thathad received up to 17 years of annual mass treatment withivermectin [8] Results of this study revealed that while theonchocerciasis foci in the health districts of Tchollire and ReyBouba appeared to fulfill the Diawara criteria of eliminationin theHealthDistrict of Touboro transmissionwas still goingon The objective of the present study was to determinewhether 15 years of annual treatment with ivermectin inWestRegion a different ecological setting had interrupted thetransmission of onchocerciasis as had been observed in Maliand Senegal [11]
2 Materials and Methods
21 Study Area West Region is close to 14000 km2 of terri-tory located in the central-western portion of the Republic ofCameroon (Figure 1) It borders the Northwest Region to thenorthwest the Adamawa Region to the northeast the CentreRegion to the east and southeast the Littoral Region to thesouthwest and the Southwest Region to the west The WestRegion is the smallest of Cameroonrsquos ten regions in area yetit has the highest population density with a total populationof about 1699000 people living in 20 health districts Themountainous terrain creates many perennial fast-runningrivers that support breeding of black flies which transmitonchocerciasis throughout the year The vegetation consistsof thick forest in the western and eastern parts of the regionwhile the middle part is a transition from forest to savannahwoodlandThemain vector of onchocerciasis inWest RegionofCameroon is Simulium squamosum amember of Simuliumdamnosum complex
22 History of Mass Treatment with Ivermectin Annualmass treatment with ivermectin commenced in 1996 andwas carried out annually through 2010 in all the 20 healthdistricts Validation of treatment coverage through house-hold face-to-face interviews was conducted every year from2003 to 2010 in order to ensure that what was reportedwas correct This also presented opportunities to identifyissues that could be improved upon in order to attain andsustain the desired treatment coverage of at least 90 ofthe ultimate treatment goal (UTG) UTG is the sum of alleligible persons for treatment (minus children lt5 years)among the total number of people at risk living in all at-risk communities in the onchocerciasis endemic area thatthe program ultimately has to treat [12] The individuals inthe samples selected for interviews were obtained throughmultistage random sampling in a homogenous populationat 95 confidence level where a plusmn5 sampling error was
Regional border Health district border Fly collection site 1996
Fly collection site 2011 Community assessed in 1996 Community assessed in 2011
West Region
North-West
Littoral
Far-North
North
CentreCameroonAdamaoua
Scale 1800 0000 5 10 20 30
N
E
S
W
(km)
South-WestRegion
LittoralRegion
Bangourain
FoumbanMatoupou-Chefferie
KouoptamoGalim
Mbouda
Batcham
Dschang
Massangam
Foumbot
Njon
Penka MichelBakassa
Bafoussam
Bamendjou Bandjoun
BahamBapi
Bangangte
Santchou Bandja
e
West
Figure 1 Map of West Region of Cameroon showing the study areas
accepted [13] The data was entered and analysed in (Epi InfoVersion 604 CDC Atlanta GA USA) Since every districtand community had equal chances of being selected everyyear the results obtained were considered representative ofthe annual treatment coverage [14ndash16] Annual validation oftreatment coverage reports showed achievement of at least90 of UTG every year (Table 1) Therefore the surveyedtreatment coverage validated the reported treatment coveragefrom 2003 to 2010
23 Baseline Assessments 1996 Before commencement ofmass treatment with ivermectin baseline entomological andparasitological surveys were conducted in this region in 1996with Carter Center support
231 Baseline Parasitological Assessments 1996 Microfilaria(mf) survey Baseline datawere secured from 12 communitiesbelonging to 7 health districts Bafang (3) Baham (1) Banja(1) Bangangte (2) Foumbot (2) Kekem (1) and Penka-Michel (1) After obtaining consent an individualrsquos nameage and gender were recorded on a registration form Adultsof 20 years and above who had lived in their respectivecommunities for at least 10 years were selected for skinsnipping A total of 931 adults from these communities were
assessed for mf Also 185 resident children (102 from onecommunity in Bafang and 83 from two in Foumbot) wereassessed It was not possible to skin snip children in otherbaseline communities Two skin snips were taken one fromthe posterior iliac crest and another from the buttock using acorneoscleral punchThe skin snips were placed immediatelyin wells of microtitration plates containing normal salinesolution and held at room temperature for 12 to 24 hours[16ndash18] The corresponding well numbers were reflected onthe patient form When the plate was full it was sealed witha transparent adhesive tape After 12ndash24 hours the snipswere removed and the fluid from each well was examinedseparately on a slide for microfilaria under high power(40x) magnification The results were expressed for eachindividual as ldquopositiverdquo or ldquonegativerdquo and were recorded inthe registration form Microfilaria prevalence was expressedas a percentage of the number examined [19] Consent wasobtained from individual adults assessed or from parents ofthe children assessed Individuals had the option to opt outwithout fear of repercussions
Nodule Survey A total of 332 adults of 20 years of ageand above who had lived in the area for at least 10 yearswere examined for nodules from the same communities that
4 Journal of Parasitology Research
Table 1 Comparing reported and validated (through surveys) UTG treatment coverage in West Region from 2003 to 2010
were assessed for mf Every participant was examined in awell-lit private room Trained health workers performed apalpation examination on the partially undressed participantpaying attention to bony prominences of the torso iliac crestsand upper trochanter of the femurs Onchocercal noduleswere identified clinically as being firm painless and mobile[19ndash21] Results were recorded on the form as ldquopositiverdquo orldquonegativerdquo Nodule prevalence was expressed as a percentageof the total number of persons examined
232 Entomological Survey Fly collection was carried out inBafang and Foumbot for a period of one month Potential flycollectors of at least 20 years of age were fully informed of thenature of work and the possibility of opting out of the studyif they wished so at any time without any repercussionsThecollectors worked 2 days in Bafang and 15 days in Foumbot inMay 1996 near the river banks where they exposed their legsin shifts from 0600 to 1200 and from 1200 to 1800 hours [19]As female Simulium flies seeking a blood meal settled on theexposed legs suction tubes were used to catch them beforethey bit Using a dissecting microscope (40x magnification)an experienced dissector opened the vector fliesrsquo abdomensthoraxes and heads Dissected flies were then examinedunder a light microscope in order to identify the presence ofinfection and to count the number of larval stages (L1 L2 andL3)when present Since fly collection lasted onemonth it wasnot possible to determine the annual transmission potential(ATP) Infective flies were defined as flies with L3s in the head[22 23]
Monthly biting rate (MBR) was calculated as per thestandard method as
MBR = (Number of flies collected
times number of days in the month)
times (Number of fly collection days)minus1
(1)
24 Follow-Up Assessments
241 Parasitological Assessments 2005 2006 and 2011 Base-line mf rates in the sentinel communities were followed up inonly 9 sentinel communities in 2005 threemonths aftermasstreatment with ivermectin in 2006 six months after andelevenmonths after treatment in 2011Three baseline sentinelcommunities (Foundjanti in Bafang Bapi in Baham andBakassa in Penka Michel) were not assessed in 2005 as theywere inaccessible as a result of heavy rains and the status quowasmaintained in 2006 A total of 878 and 780 resident adultswere assessed in 2005 for mf and nodules respectively Also403 resident children (le10 years old) were assessed for mf
In 2006 assessment for mf and nodules covered 782resident adults Skin snips were obtained from only 134children Skin snipping performed in 2005 and 2006 involvedtwo skin snips one taken from the posterior iliac crest andanother from the buttock with the help of a disposable steriledermal hook and a blade The hook and blade used for eachparticipant were safely discarded [16]
In 2011 2703 resident adults from 16 communitiesincluding 11 baseline communities were examined for mfand nodules Since the Ministry of Health wanted to knowthe situation inside and outside the sentinel communitiesfour additional high risk communities were considered in2011 assessments Also 626 resident children (le10 years)from 11 communities (including three baseline communities)were examined for mf mf prevalence was expressed as apercentage of the number examined Due to heavy rainsBakambe one of the original sentinel communities wasinaccessible and therefore was not assessed Nodule palpationwas not followed up in the present study as it had not beendone in children at baseline
The comparison of baselinewith follow-up results in 2005(three months after treatment) in 2006 (six months aftertreatment) and in 2011 (11 months after treatment) was donein order to shed light on the dynamics ofOnchocerca volvulusinfection with annual mass treatment The comparison ofbaseline results to follow-up assessments was possible as onlyqualitative (presence or absence of mf or nodules) data wasconsidered
242 Follow-Up Entomological Assessment Black fly collec-tion was carried out at three sites in Bafang Foumbot andMassangam health districts for 3 days during the third weekof eachmonth fromMarch 2011 to February 2012The criteriafor selection of potential fly collectors set during baselineentomological assessment were followed Bafang collectionsite is located in extreme west of the region Foumbot in themiddle and Makouopsap in the extreme east of the region
Landing female Simulium flies were collected and imme-diately dissected in order to determine the parous rate Theremains of the dissected parous flies were preserved in a tubecontaining 70 ethanol The tubes were labeled by collectionsite date and time Simulium flies were then grouped inbatches up to 50 and sent to the laboratory where theywere stained with Mayerrsquos hematoxylin and fully dissected insearch for onchocercal larval stages (L1 L2 and L3) in theabdomen the thorax and the head [24] Infective flies weredefined as flies with L3 in the head as in the baseline surveysmentioned previously [18] This information was used to cal-culate the monthly and annual transmission potentials whichare the indicators of transmission The annual transmission
Journal of Parasitology Research 5
potential (ATP) was calculated as the sum of the individualmonthly transmission potentials (MTPs) over the period of ayear [23]
Data Analysis Parasitological data from adults and childrenas well as entomological data were entered and analysedgraphically in Microsoft Excel and Epi Info CDC AtlantaGA USA for chi square test of independence The ento-mological data was analysed and graphically illustrated inMicrosoft Excel
Ethical Approval All the surveys from the baseline to thefollow-up studies were approved by the Ministry of PublicHealth of Cameroon and the National Ethical Committeein Yaounde In addition the Emory University InstitutionalReview Board (eIRB-11 438) approved and considered themas nonresearch but routine program evaluation The fol-lowup of 2011 was also conducted under the auspices ofWorldHealth Organisation All assessed individuals had the libertyof opting out of assessments if they wished so without anyrepercussions
3 Results
31 Microfilaria (mf) and Nodule Prevalences Among adultsthe mf rate reduced by about 91 from baseline level of667 (range 531 to 881) in 1996 to 60 (range 14 to183 119875 lt 00001) in 2005 three months after ivermectintreatment However mf rate increased in 2006 six monthsafter ivermectin treatment to 139 (range 21 to 336)although it was not statistically different from 2005 mf rate119875 lt 0053 The decrease of mf rate 139 in 2006 to114 (range 0 to 596) in 2011 was also not significant(119875 lt 0053) (Table 2 and Figure 2) Only one communityhad 0 mf rate while six communities had mf rates above10 and two above 40 after 15 years of annual masstreatment Persistent high mf rates were observed in com-munities of Babouantou (214) in Bandja health districtNjone (419) in Foumbot health district and Makouopsap(596) in Massangam health district However there werecommunities (Bakonti in Bafang Health District Folap inFoumban Mbafam in Kekem and Njisseng in Kouptamo)which registered mf rates below 5 in adults
In children overall baselinemf rate of 292 (range 127to 518) reduced to 42 (range 0 to 250) in 2005 withan 856 reduction 119875 lt 00001 (Table 3 and Figure 2)However there was no significant difference between mf rate42 in 2005 and 45 in 2006 three months and six monthsrespectively after mass treatmentThere results for 2006 werealso not significantly different from mf rate 89 obtainedin 2011 eleven months after treatment (Table 3 and Figure 2)There were children in 2 (133) communities with mf ratesabove 20 (Njone 252 and Makouopsap 656) EvenBabouantou with mf rate of 158 was considered high fora program with 15 years of annual treatment In Ndjipta III ofBangangte Health District Folap of Foumban and Mbafamof Kekem mf rates among children were 06 or less
The overall baseline nodule rate in adults of 663 (range40 to 897) declined to 95 (range 400ndash897) 119875 lt00001 in the 2005This represents a decline of 856Then itincreased to 185 (range 67ndash303) in 2006 and declinedto 121 (range 15ndash434) in 2011 (Table 4) There were9 communities out of 16 with nodule prevalence of at least10 Of particular interest are persistent high nodule ratesin Bakambe (232) and Fondjanti (232) communities ofBafang Health District Fossang-chefferie (173) and Njone(186) in Foumbot health district andMakouopsap (434)in Massangam Health District
32 Entomology Baseline monthly transmission potentialswere 15 in Bafang and 2104 in Foumbot (Table 5) In thefollow-up assessment the infection rates were 02 in BafangHealth District 088 in Foumbot and 067 in MassangamThe infective rates were 0 in Bafang Health District 019in Foumbot and 018 in Massangam Annual biting rateswere 52610 in Bafang 28560 in Foumbot and 125360 inMakouopsap while annual transmission potentials were 070 and 310 respectively Biting was generally throughout theyear although the main peak biting period in Makouopsapwas observed from January to May (Figure 3)
4 Discussion
Annual mass treatment with ivermectin for 15 years hadconsiderably reduced microfilaria and nodule prevalence inall the sentinel communities of West Region of CameroonElimination is considered attained when the microfilariaprevalence in skin snips is less than 5 in sampled communi-ties in less than 1 in 90of sampled communities andwhenentomological criteria of less than 05 infected flies1000 areattained [11] Among adults Foumban Health District wasclose to the epidemiological criterion while Bafang HealthDistrict was not very far from the entomological criterionwith the ATP of 0 mf rate among children in Foumbanand Kekem health districts was zero indicating no recentinfection an indication that interruption of transmissionmay be attained However the mf rates in Baham BanjaBangangte Foumbot andMassangam health districts amongadults and children were still uncomfortably high showingcontinuing transmission In adults nodule rates near orabove the threshold 20 for the mass treatment in somecommunities were of a major concern The infective rateof 018 to 019 and ATP of 70 to 300 confirmed continuingtransmission
One possible explanation for high mf rates in childrenand adults could have been low treatment coverage Howeverthe methodology for validating UTG treatment coveragefollowed standard statistical methods for selecting sampledcommunities and the interviewees This methodology hadbeen tested and used to validate performance of CDTI inCameroon and in other onchocerciasis endemic countries[14 15 25]TheUTG treatment coverage results were also cor-roborated by independent monitoring results in unpublishedreports supported by APOC Therefore there is no reason tobelieve that UTG treatment coverage was low and responsible
6 Journal of Parasitology Research
Table2Com
parin
gmfp
revalencea
mon
gadultsatbaselin
e(1996)a
ndfollo
wup
in2005200
6and2011three
mon
thssix
mon
thsandele
venmon
thsrespectiv
elyafte
rmasstreatment
inWestR
egion
Cameroo
n
Distric
tCom
mun
ityBa
selin
e1996
(119899=931)
Follo
wup
2005(119899=878)
Follo
wup
200
6(119899=782)
Follo
wup
2011(119899=2703)
No
exam
ined
No
positive
mf
positive
No
exam
ined
No
positive
mf
positive
No
exam
ined
No
positive
mf
positive
No
exam
ined
No
positive
mf
positive
Bakassa
6136
590
140
214lowast
972
21
251
1456
Bafang
Bakonti
5236
692
993
30lowast
753
40
338
1236
Fond
janti
124
8770
2125
864
Bakambe
122
65533
105
329lowast
916
66
ND
ND
ND
Baham
Bapi
145
77531
ND
ND
ND
ND
ND
ND
189
21111
Band
jaBa
bouantou
(Batou
la)
6849
721
537
132lowast
7614
184
8418
214
Bang
angte
Batchingou
8461
726
102
11108lowast
8014
175
247
45182
NdjiptaIII
(Fop
-Tchui)
8871
807
781
13lowast
576
105lowastlowast
929
98
Foum
bot
Fossang-
chefferielowast
3228
875
7113
183lowast
7219
264lowastlowast
150
19127lowastlowastlowast
Njone
5952
881
135
1181lowast
122
41336lowastlowast
167
70419lowastlowastlowast
Kekem
Mbafam
3927
692
952
21lowast
112
436
163
849
Penk
a-Michel
Bakassa
5732
561
ND
ND
ND
ND
ND
ND
195
736
Foum
ban
Folap
ND
ND
ND
ND
ND
ND
ND
ND
ND
265
000
Kouo
ptam
oNjisseng
ND
ND
ND
ND
ND
ND
ND
ND
ND
168
530
Malantouen
Matou
pou
ND
ND
ND
ND
ND
ND
ND
ND
ND
170
1376
Massang
amMakou
opsap
ND
ND
ND
ND
ND
ND
ND
ND
ND
9959
596
931
621
667
878
5360lowast
782
109
139
2703
308
114
NDnot
done
lowastSign
ificant
(119875lt005)mdash
follo
wup
2005
comparedwith
theb
aseline
lowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2006
comparedwith
2005
follo
wup
lowastlowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2011comparedwith
2006
follo
wup
Journal of Parasitology Research 7
667
6139 114
292
42 45 89
01020304050607080
m
f pre
vale
nce
AdultsChildren
1996119899 = 931 2005 (3 months after treatment)
119899 = 878
2006 (6 months
Baseline Followup
after treatment)119899 = 782
2011 (11 monthafter treatment)
119899 = 2703
Figure 2 Comparison of mf rates among adults and children atbaseline 1996 with followup surveys in 2005 2006 and 2011 inWestRegion of Cameroon
for failure to attain optimal parasitological and entomologicalimpacts
High vector density and mf rates suggest that the forceof transmission may have been very high and most likely thereason for the results obtained [26]The present study did notconsider the standardmeasure of intensity of infection whichis related to force of infection community mf load (CMFL)This requires a calculation that involves weighing the snipand counting the microfilaria which was not done [19] Werecommend that it should be done in future studies
In Massangam Health District it is possible that high mfand nodule rates in the follow-up assessments may be dueto the ldquoforce of infectionrdquo across the neighbouring CentralRegion where peer-reviewed studies indicate considerableonchocerciasis transmission [27 28] River Nja a tributary ofRiver Noun and River Kichi a tributary of River Mbam areknown black fly breeding sites responsible for cross-bordertransmission between West and Central regions Thereforewe recommend collaboration between the regions in order tounderstand the limits of cross-border onchocerciasis affectedarea and harmonize intervention if elimination becomes thegoal in Cameroon
Another possible explanation for high mf rates couldbe related to suboptimal response to ivermectin observedin some onchocerciasis endemic areas of Ghana The adultfemale O volvulus worms were resuming microfilaria repro-duction more rapidly after ivermectin treatment than wouldnormally be expected suggesting possible development ofresistance to ivermectin [29ndash31] We recommend that thepossibility of suboptimal response to ivermectin in WestRegion be investigated
The microfilaria rate in adults and children tended tofollow the expected trend where a single annual dose ofivermectin over a number of years significantly reduced thelow mf rates that tend to persist [3] The observed patternindicated a tendency for themf rate to raise a fewmonths aftermass treatment until another dose of ivermectin is providedconfirming that microfilarial production is not cumulativelyreduced by several annual ivermectin treatments [32] Themf rate trend at three six and eleven months after mass
treatment is usually not different from the infection ratewithin the flies over a period after mass treatment withivermectin [33] Ivermectin kills existing microfilariae andtends to exert an ldquoembryostatic effectrdquo by which microfilarialproduction is suppressed over a few weeks after treatmentbut then after the mf rate begins to increase [32] Underfavourable ecological conditions interruption of onchocer-ciasis transmission with annual mass treatment may requiremany more years before it is attained
As for twice yearly treatment with ivermectin or whenit is coupled with vector control infection rate continuedto fall implying that interruption of transmission could berapidly attained [1 33 34] We recommend that West Regionof Cameroon should consider twice yearly treatment or atleast annual treatment with targeted vector control
In the present study some communities (Folap andNjisseng) in Foumban and Kouoptamo health districts hadmf rates lower than 5 in adults and 0 in children Inthese communities the Diawara et al criteria are closeto being attained and yet with low levels of infectiontransmission is much more efficient than at high levels ofinfection [35ndash37] Thus if low levels of infection are notdetected and controlled they could result in fast diseaserecrudescence Skin snip (microscopy) has low sensitivity ofless than 20 at less than 20 nodule rate and the resultsobtained may not reflect correct mf endemicity levels [38]Therefore interventions in these health districts cannot behalted as disease recrudescence could occur [29 30] Whereinterruption of transmission of onchocerciasis is the objectivewe recommend a search for affordable less intrusive rapidsensitive and highly specific diagnostic tools for low levelinfections in order to validate interruption of onchocerciasistransmission
The APOC threshold for launching mass treatment isan onchocercal nodule rate of ge20 Fondjanti community(Bandja Health District) with nodule rate of 23 and mfrate of 64 would pass for mass treatment while Njonecommunity (Foumbot Health District) with nodule rate of186 and mf rate of 419 would fail [39] Nodule rate couldalso be confounded by the presence of ganglia and Taeniasolium [40 41] The entomological results showed that therisk of contracting onchocerciasis in FoumbotHealthDistrictwas higher than in Bafang Health District confirming thereliability of mf rates compared with nodule rates With theshift from control to elimination of onchocerciasis in Africawe recommend that nodule prevalence should not be usedto determine whether an endemic area should receive masstreatment or not
Annual biting rates with the range of 28560 to 125380are some of the highest observed globally Yet infective ratein Bafang from the western part of the region was zerojustifying low mf rates (06 in children and a mean of52 in adults) The question would be whether annual masstreatment could be withdrawn without resulting in diseaserecrudescence Existing low level transmission with the highannual biting rate of 52610 could still result in onchocerciasisrecrudescence It was also evident in this study that one-month baseline entomological data was likely to miss peakbiting transmission pattern of Simulium vectors and the
8 Journal of Parasitology Research
Table3Com
parin
gmfp
revalencea
mon
gchild
renatbaselin
e(1996)and
follo
wup
in2005200
6and2011three
mon
thssix
mon
thsandele
venmon
thsrespectiv
elyafterm
asstreatment
inWestR
egion
Cameroo
n
Distric
tCom
mun
ityBa
selin
e1996
(119899=185)
Follo
wup
2005(119899=403)
Follo
wup
200
6(119899=134)
Follo
wup
2011(119899=626)
No
Exam
ined
No
positive
mf
positive
No
Exam
ined
No
positive
mf
positive
No
Exam
ined
No
positive
mf
positive
Noexam
No
positive
mf
positive
Bafang
Bakonti-B
akassa
102
13127
740
0lowast43
000
167
106
Bafang
Batchieu
704
57
40
00
Baham
Bapi
ND
ND
ND
292
69
Band
jaBa
bouantou
(Batou
la)lowast
ND
ND
ND
647
109
143
214
193
158
Bang
angte
Batchingoulowast
ND
ND
ND
241
42
152
133
211
48
Bang
angte
NdjiptaIII(Fo
p-Tchu
i)lowastND
ND
ND
632
32
50
00
250
00
FossangCh
efferie
ND
ND
ND
380
00
40
00
252
80
Foum
bot
Njone
2019
950
123
25lowast
161
63
8224
293lowastlowastlowast
Foum
bot
Kousang-Malanden
6322
349
ND
ND
ND
ND
ND
ND
ND
ND
ND
Kekem
Mbafamlowast
ND
ND
ND
580
00
330
00
200
00
Penk
a-Michel
Bakassa
ND
ND
ND
ND
ND
ND
ND
ND
ND
741
14Fo
umban
Folap
ND
ND
ND
ND
ND
ND
ND
ND
ND
108
000
Kouo
ptam
oNjisseng
ND
ND
ND
ND
ND
ND
ND
ND
ND
241
42
Massang
amMakou
opsap
ND
ND
ND
ND
ND
ND
ND
ND
ND
3221
656
12185
5429
240
317
42lowast
134
645
626
5689
NDnot
done
lowastSign
ificant
(119875lt005)mdash
follo
wup
2005
comparedwith
theb
aseline
lowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2006
comparedwith
2005
follo
wup
lowastlowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2011comparedwith
2006
follo
wup
Journal of Parasitology Research 9
Table4
Com
parin
gnod
ulep
revalencea
mon
gadu
ltsatbaselin
e(1996)and
follo
wup
in2005200
6and2011three
mon
thssix
mon
thsandele
venmon
thsrespectiv
elyafterm
asstreatment
inWestR
egion
Cameroo
n
Distric
tCom
mun
ityBa
selin
e1996
(119899=305)
Follo
wup
2005(119899=780)
Follo
wup
200
6(119899=782)
Follo
wup
2011(119899=2703)
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
Bafang
Bakassa
2716
593
139
110
79lowast
9711
113
251
2184
Bakonti
2711
407
9850
51lowast
755
67
338
36107
Fond
janti
2719
704
125
29232
Bakambe
2719
704
105
110
105lowast
9113
143
125
29232
Baham
Bapi
2915
517
ND
ND
ND
ND
ND
ND
189
1579
Band
jaBa
bouantou
(Batou
la)
2616
615
6150
82lowast
7618
237lowastlowast
8412
143
Bang
angte
Batchingou
2922
759
101
160
158lowast
8023
288lowastlowast
247
29117lowastlowastlowast
NdjiptaIII(Fo
p-Tchu
i)29
23793
7850
64lowast
578
140lowastlowast
929
98
Foum
bot
Fossang-chefferie
2824
857
7170
99lowast
7218
250lowastlowast
150
26173lowastlowastlowast
Njone
2926
897
3490
265lowast
122
37303
167
31186lowastlowastlowast
Kekem
Mbafam
2417
708
9350
54lowast
112
12107lowastlowast
163
27166
Penk
a-Michel
Bakassa
3012
400
ND
ND
ND
ND
ND
ND
195
1577
Foum
ban
Folap
ND
ND
ND
ND
ND
ND
ND
ND
ND
265
415
Kouo
ptam
oNjisseng
ND
ND
ND
ND
ND
ND
ND
ND
ND
168
636
Malantouen
Matou
pou
ND
ND
ND
ND
ND
ND
ND
ND
ND
170
953
Massang
amMakou
opsap
ND
ND
ND
ND
ND
ND
ND
ND
ND
9943
434
332
220
663
780
7495lowast
782
145
185lowastlowast
2828
341
121lowastlowastlowast
NDnot
done
lowastSign
ificant
(119875lt005)mdash
follo
wup
2005
comparedwith
theb
aseline
lowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2006
comparedwith
2005
follo
wup
lowastlowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2011comparedwith
2006
follo
wup
10 Journal of Parasitology Research
Table 5 Comparing baseline entomological data of 1996 at two fly collection sites and three during 2011
Monthyear of black fly collection Baseline May 1996 Followup 2011Black fly collection sites Bafang (Basseu) Foumbot (Maka) Bafang Foumbot MassangamNumber of Simulium caught 5 166 5261 2856 12538Number of Simulium dissected 5 142 5261 2856 12138Number of parous flies 1 97 1502 1028 2845Parous rate () 20 683 285 36 234Number of Simulium flies infected (L1 L2 L3] 1 12 3 9 19Infection rate () 2000 845 020 088 067Number of Simulium flies infective L3 larval stage in the head 20 2 0 2 5Infective rate () 200 211 000 019 018Monthly biting rate per person 750 166000 na na naMonthly transmission potentiallowast 150 21040 na na naAnnual biting rate per person Na na 52610 28560 125380Annual transmission potential Na na 0 70 310
0
500
1000
1500
2000
2500
3000
3500
4000
No
of fl
ies c
olle
cted
BafangFoumbotMakouopsap
MarApr2011 2012
May Jun Jul AugSeptOctNovDec Jan Feb
Figure 3 Monthly seasonal biting of Simulium flies at 3 fly catchingsites in West Region
calculation ofATPTherefore collection of entomological dataover several months is required as reflected in the follow-up study The information on peak biting and transmissionpatterns could effectively be utilized for ivermectin treatmentfor maximum impact on transmission especially where theforce of transmission is considerably high if elimination ofonchocerciasis is the goal In the follow-up survey it is onlyat Bafang fly collection site that the entomological criterionfor interruption of transmission was met with an ATP of zero[42]
The present study however did not perform moleculartesting in order to determine if the L3 larvae wereO volvulusor another (animal) Onchocerca species Based on humanmf prevalence in skin and infections in children we thinkthat there is likelihood that some of the larvae observedin vectors were O volvulus However a study conducted inNorth Region of Cameroon during the 1990s showed that
33 of infective larvae in S damnosum were O volvuluswhereas 65 were O ochengi and 2 were O ramachandrini[43] It is until such a study is conducted in West Region ofCameroon that we will know the extent to which O ochengiis responsible for a significant proportion of infected flies thatcould confound the infection rate there
Our findings reflecting an observation period of 15 yearsshowed that annual mass treatment with ivermectin may notinterrupt the transmission of onchocerciasis in all differentecological zones of West Region Therefore the intensive useof ivermectin is recommended if interruption of transmissionof onchocerciasis is to be attained [1]
5 Conclusion
Annual mass treatment with ivermectin through commu-nity-directed treatment was preferred as a good and lessexpensive method for controlling onchocerciasis in endemicAfrican countries with assistance from the African Pro-gramme for Onchocerciasis Control The studies in MaliSenegal and Nigeria have shown that an annual dose ofivermectin had interrupted transmission of the disease andall interventions could be halted without the risk of diseaserecrudescence However an annual dose of ivermectin hasnot interrupted transmission after 15 years of mass treatmentin some areas in West Region of Cameroon just like inNorth region [8] It has also been less effective in someonchocerciasis endemic areas in Ghana The present paperagain highlights the fact that for interruption of onchocer-ciasis transmission feasible and different but complementarystrategic options should be adopted as elimination becomesthe goal in Africa
Acknowledgments
The investigators would like to acknowledge the staff ofMinistry of Health at the national regional and healthdistrict levels in West Region along with Carter CenterCameroon Office for mobilizing and educating selected
Journal of Parasitology Research 11
communities and providing policy and administrative sup-port The involvement of community members in selectedcommunities in mf and nodule assessments and Simulium flycollection is highly appreciated The Carter Center the LionsClubs International Foundation (LCIF) and the African Pro-gramme for onchocerciasis Control (APOC) which fundedthe CDTI activities and the surveys are also highly appreci-ated
References
[1] E W Cupp and M S Cupp ldquoShort report impact of iver-mectin community-level treatments on elimination of adultOnchocerca volvulus when individuals receive multiple treat-ments per yearrdquoThe American Journal of Tropical Medicine andHygiene vol 73 no 6 pp 1159ndash1161 2005
[2] H R Taylor M Pacque B Munoz and B M Greene ldquoImpactof mass treatment of onchocerciasis with ivermectin on thetransmission of infectionrdquo Science vol 250 no 4977 pp 116ndash118 1990
[3] G J J M Borsboom B A Boatin N J D Nagelkerkeet al ldquoImpact of ivermectin on onchocerciasis transmissionassessing the empirical evidence that repeated ivermectin masstreatmentsmay lead to eliminationeradication inWest-AfricardquoFilaria Journal vol 2 article 8 2003
[4] A D Hopkins ldquoIvermectin and onchocerciasis is it all solvedrdquoEye vol 19 no 10 pp 1057ndash1066 2005
[5] L Yameogo ldquoSpecial intervention zonesrdquo Annals of TropicalMedicine and Parasitology vol 102 supplement 1 pp 23ndash242008
[6] D H Molyneux and M N Malecela ldquoNeglected tropicaldiseases and themillennium development goals why the ldquootherdiseasesrdquo matter reality versus rhetoricrdquo Parasites amp Vectorsvol 4 2011
[7] WHOReportAcceleratingWorkToOvercome theGlobal Impactof Neglected Tropical Disease A Roadmap For Implementationvol 1211WorldHealthOrganization 20AvenueAppia GenevaSwitzerland 2012
[8] M N Katabarwa A Eyamba P Nwane et al ldquoSeventeenyears of annual distribution of ivermectin has not interruptedonchocerciasis transmission in North Region Cameroonrdquo TheAmerican Journal of Tropical Medicine and Hygiene vol 85 no6 pp 1041ndash1049 2011
[9] B A Boatin and F O Richards ldquoControl of onchocerciasisrdquoAdvances in Parasitology vol 61 pp 349ndash394 2006
[10] D R Hopkins F O Richards and M Katabarwa ldquoWhitheronchocerciasis control in Africardquo American Journal of TropicalMedicine and Hygiene vol 72 no 1 pp 1ndash2 2005
[11] L Diawara M O Traore A Badji et al ldquoFeasibilityof onchocerciasis elimination with ivermectin treatment inendemic foci in Africa first evidence from studies in Mali andSenegalrdquo PLoS Neglected Tropical Diseases vol 3 no 7 articlee497 2009
[12] F O Richards E S Miri M Katabarwa et al ldquoThe carter cen-terrsquos assistance to river blindness control programs establish-ing treatment objectives and goals for monitoring ivermectindelivery systems on two continentsrdquo The American Journal ofTropical Medicine and Hygiene vol 65 no 2 pp 108ndash114 2001
[13] P Salant and D A Dilman How to Conduct Your Own SurveyJohn Wiley amp Sons 1994
[14] M N Katabarwa P Habomugisha and F O Richards ldquoImple-menting community-directed treatmentwith ivermectin for the
control of onchocerciasis in Uganda (1997-2000) an evalua-tionrdquo Annals of Tropical Medicine and Parasitology vol 96 no1 pp 61ndash73 2002
[15] E C Emukah U Enyinnaya N S Olaniran et al ldquoFactorsaffecting the attrition of community-directed distributors ofivermectin in an onchocerciasis-control programme in the Imoand Abia states of south-eastern Nigeriardquo Annals of TropicalMedicine and Parasitology vol 102 no 1 pp 45ndash51 2008
[16] A Prost and J Prodrsquohon ldquoLe diagnostique parasitologique delrsquoonchocercose revue critique des methods en usagerdquoMedicineTropicale vol 38 pp 519ndash532 1978
[17] H Schulz Key ldquoA simple technique to assess the total number ofOnchocerca volvulusmicrofilariae in skin snipsrdquo Tropenmedizinund Parasitologie vol 29 no 1 pp 51ndash54 1978
[18] WHO Report ldquoOnchocerciasis and its control Report of aWHO Expert Committee on Onchocerciasis Controlrdquo TechRep 852 Geneva Switzerland 1995
[19] WHO Report Strategies For Ivermectin Distribution ThroughPrimaryHealth Care SystemWHOPHL91 24WHOGenevaSwitzerland 1991
[20] E J Albiez D W Buttner and B O L Duke ldquoDiagnosisand extirpation of nodules in human onchocerciasisrdquo TropicalMedicine and Parasitology vol 39 no 4 pp 331ndash346 1988
[21] P Ngoumou J F Walsh and J M Mace ldquoA rapid mappingtechnique for the prevalence and distribution of onchocerciasisa Cameroon case studyrdquo Annals of Tropical Medicine andParasitology vol 88 no 5 pp 463ndash474 1994
[22] M Katabarwa A W Onapa and B Nakileza ldquoRapid epidemi-ological mapping of onchocerciasis in areas of uganda whereSimulium neavei SL is the vectorrdquo East African Medical Journalvol 76 no 8 pp 440ndash446 1999
[23] J F Walsh J B Davies R Le Berre and R Garms ldquoStandard-ization of criteria for assessing the effect of Simulium control inonchocerciasis control programmesrdquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 72 no 6 pp 675ndash676 1978
[24] J B Davies ldquoA rapid staining and clearing technique for detect-ing filarial larvae in alcohol-preserved vectorsrdquo Transactions ofthe Royal Society of Tropical Medicine and Hygiene vol 89 no3 p 280 1995
[25] M Katabarwa P Habomugisha A Eyamba S Agunyo andC Mentou ldquoMonitoring ivermectin distributors involved inintegrated health care services through community-directedinterventionsmdasha comparison of Cameroon and Uganda expe-riences over a period of three years (2004ndash2006)rdquo TropicalMedicine and International Health vol 15 no 2 pp 216ndash2232010
[26] J Remme O Ba K Y Dadzie and M Karam ldquoA force-of-infection model for onchocerciasis and its applications inthe epidemiological evaluation of the onchocerciasis controlprogramme in the volta river basin areardquo Bulletin of the WorldHealth Organization vol 64 no 5 pp 667ndash681 1986
[27] P Barbazan H Escaffre R Mbentengam and M BoussinesqldquoEntomologic study on the transmission of onchocerciasis ina forest-savanna transition area of Cameroonrdquo Bulletin de laSociete de Pathologie Exotique vol 91 no 2 pp 178ndash182 1998
[28] E Cadot P Barbazan andM Boussinesq ldquoGeographical deter-minants of onchocerciasis transmission in a forestsavannahtransition zone two villages of the mbam focusrdquo Sante vol 8no 6 pp 429ndash435 1998
[29] K Awadzi S K Attah E T Addy et al ldquoThirty-monthfollow-up of sub-optimal responders to multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in Ghanardquo
12 Journal of Parasitology Research
Annals of Tropical Medicine and Parasitology vol 98 no 4 pp359ndash370 2004
[30] K Awadzi D A Boakye G Edwards et al ldquoAn investigationof persistent microfilaridermias despite multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in GhanardquoAnnals of Tropical Medicine and Parasitology vol 98 no 3 pp231ndash249 2004
[31] M Y Osei-Atweneboana J K Eng D A Boakye J OGyapong and R K Prichard ldquoPrevalence and intensity ofOnchocerca volvulus infection and efficacy of ivermectin inendemic communities in Ghana a two-phase epidemiologicalstudyrdquoThe Lancet vol 369 no 9578 pp 2021ndash2029 2007
[32] C Bottomley V Isham R C Collins and M G BasanezldquoRates of microfilarial production by Onchocerca volvulus arenot cumulatively reduced by multiple ivermectin treatmentsrdquoParasitology vol 135 no 13 pp 1571ndash1581 2008
[33] R Garms T L Lakwo R Ndyomugyenyi et al ldquoThe elimina-tion of the vector Simulium neavei from the Itwara onchocerci-asis focus in Uganda by ground larvicidingrdquo Acta Tropica vol111 no 3 pp 203ndash210 2009
[34] R Ndyomugyenyi E Tukesiga D W Buttner and R GarmsldquoThe impact of ivermectin treatment alone and when inparallel with Simulium neavei elimination on onchocerciasis inUgandardquo Tropical Medicine and International Health vol 9 no8 pp 882ndash886 2004
[35] H P Duerr and M Eichner ldquoEpidemiology and control ofonchocerciasis the threshold biting rate of savannah onchocer-ciasis in Africardquo International Journal for Parasitology vol 40no 6 pp 641ndash650 2010
[36] K Dietz ldquoDensity-dependence in parasite transmissiondynamicsrdquo Parasitology Today vol 4 no 4 pp 91ndash97 1988
[37] M G Basanez J H F Remme E S Alley et al ldquoDensity-dependent processes in the transmission of human onchocerci-asis relationship between the numbers ofmicrofilariae ingestedand successful larval development in the simuliid vectorrdquoParasitology vol 110 no 4 pp 409ndash427 1995
[38] B A Boatin L Toe E S Alley N J D Nagelkerke GBorsboom and J D F Habbema ldquoDetection of Onchocercavolvulus infection in lowprevalence areas a comparison of threediagnostic methodsrdquo Parasitology vol 125 no 6 pp 545ndash5522002
[39] M Noma B E B Nwoke I Nutall et al ldquoRapid epidemio-logical mapping of onchocerciasis (REMO) its application bythe African programme for onchocerciasis control (APOC)rdquoAnnals of Tropical Medicine and Parasitology vol 96 supple-ment 1 pp S29ndashS39 2002
[40] G Fobi J R M Mbina G Ozoh et al ldquoOnchocerciasis inthe area of Lastourville Gabon Clinical and entomologicalaspectsrdquo Bulletin de la Societe de Pathologie Exotique vol 99no 4 pp 269ndash271 2006
[41] M N Katabarwa A Eyamba M Chouaibou et al ldquoDoesonchocerciasis transmission take place in hypoendemic areasa study from theNorth Region of CameroonrdquoTropicalMedicineand International Health vol 15 no 5 pp 645ndash652 2010
[42] WHO Report Certification of Elimination of Human Onchocer-ciasis Criteria and Procedures Criteria For Certification of Inter-ruption of TransmissionElimination of Human OnchocerciasisWorld Health Organization Geneva Switzerland 2001
[43] R Seidenfaden A Fischer I Bonow D Ekale V Tanya andA Renz ldquoCombined benefits of annual mass treatment withivermectin and cattle zooprophylaxis on the severity of humanonchocerciasis in northern Cameroonrdquo Tropical Medicine andInternational Health vol 6 no 9 pp 715ndash725 2001
Regional border Health district border Fly collection site 1996
Fly collection site 2011 Community assessed in 1996 Community assessed in 2011
West Region
North-West
Littoral
Far-North
North
CentreCameroonAdamaoua
Scale 1800 0000 5 10 20 30
N
E
S
W
(km)
South-WestRegion
LittoralRegion
Bangourain
FoumbanMatoupou-Chefferie
KouoptamoGalim
Mbouda
Batcham
Dschang
Massangam
Foumbot
Njon
Penka MichelBakassa
Bafoussam
Bamendjou Bandjoun
BahamBapi
Bangangte
Santchou Bandja
e
West
Figure 1 Map of West Region of Cameroon showing the study areas
accepted [13] The data was entered and analysed in (Epi InfoVersion 604 CDC Atlanta GA USA) Since every districtand community had equal chances of being selected everyyear the results obtained were considered representative ofthe annual treatment coverage [14ndash16] Annual validation oftreatment coverage reports showed achievement of at least90 of UTG every year (Table 1) Therefore the surveyedtreatment coverage validated the reported treatment coveragefrom 2003 to 2010
23 Baseline Assessments 1996 Before commencement ofmass treatment with ivermectin baseline entomological andparasitological surveys were conducted in this region in 1996with Carter Center support
231 Baseline Parasitological Assessments 1996 Microfilaria(mf) survey Baseline datawere secured from 12 communitiesbelonging to 7 health districts Bafang (3) Baham (1) Banja(1) Bangangte (2) Foumbot (2) Kekem (1) and Penka-Michel (1) After obtaining consent an individualrsquos nameage and gender were recorded on a registration form Adultsof 20 years and above who had lived in their respectivecommunities for at least 10 years were selected for skinsnipping A total of 931 adults from these communities were
assessed for mf Also 185 resident children (102 from onecommunity in Bafang and 83 from two in Foumbot) wereassessed It was not possible to skin snip children in otherbaseline communities Two skin snips were taken one fromthe posterior iliac crest and another from the buttock using acorneoscleral punchThe skin snips were placed immediatelyin wells of microtitration plates containing normal salinesolution and held at room temperature for 12 to 24 hours[16ndash18] The corresponding well numbers were reflected onthe patient form When the plate was full it was sealed witha transparent adhesive tape After 12ndash24 hours the snipswere removed and the fluid from each well was examinedseparately on a slide for microfilaria under high power(40x) magnification The results were expressed for eachindividual as ldquopositiverdquo or ldquonegativerdquo and were recorded inthe registration form Microfilaria prevalence was expressedas a percentage of the number examined [19] Consent wasobtained from individual adults assessed or from parents ofthe children assessed Individuals had the option to opt outwithout fear of repercussions
Nodule Survey A total of 332 adults of 20 years of ageand above who had lived in the area for at least 10 yearswere examined for nodules from the same communities that
4 Journal of Parasitology Research
Table 1 Comparing reported and validated (through surveys) UTG treatment coverage in West Region from 2003 to 2010
were assessed for mf Every participant was examined in awell-lit private room Trained health workers performed apalpation examination on the partially undressed participantpaying attention to bony prominences of the torso iliac crestsand upper trochanter of the femurs Onchocercal noduleswere identified clinically as being firm painless and mobile[19ndash21] Results were recorded on the form as ldquopositiverdquo orldquonegativerdquo Nodule prevalence was expressed as a percentageof the total number of persons examined
232 Entomological Survey Fly collection was carried out inBafang and Foumbot for a period of one month Potential flycollectors of at least 20 years of age were fully informed of thenature of work and the possibility of opting out of the studyif they wished so at any time without any repercussionsThecollectors worked 2 days in Bafang and 15 days in Foumbot inMay 1996 near the river banks where they exposed their legsin shifts from 0600 to 1200 and from 1200 to 1800 hours [19]As female Simulium flies seeking a blood meal settled on theexposed legs suction tubes were used to catch them beforethey bit Using a dissecting microscope (40x magnification)an experienced dissector opened the vector fliesrsquo abdomensthoraxes and heads Dissected flies were then examinedunder a light microscope in order to identify the presence ofinfection and to count the number of larval stages (L1 L2 andL3)when present Since fly collection lasted onemonth it wasnot possible to determine the annual transmission potential(ATP) Infective flies were defined as flies with L3s in the head[22 23]
Monthly biting rate (MBR) was calculated as per thestandard method as
MBR = (Number of flies collected
times number of days in the month)
times (Number of fly collection days)minus1
(1)
24 Follow-Up Assessments
241 Parasitological Assessments 2005 2006 and 2011 Base-line mf rates in the sentinel communities were followed up inonly 9 sentinel communities in 2005 threemonths aftermasstreatment with ivermectin in 2006 six months after andelevenmonths after treatment in 2011Three baseline sentinelcommunities (Foundjanti in Bafang Bapi in Baham andBakassa in Penka Michel) were not assessed in 2005 as theywere inaccessible as a result of heavy rains and the status quowasmaintained in 2006 A total of 878 and 780 resident adultswere assessed in 2005 for mf and nodules respectively Also403 resident children (le10 years old) were assessed for mf
In 2006 assessment for mf and nodules covered 782resident adults Skin snips were obtained from only 134children Skin snipping performed in 2005 and 2006 involvedtwo skin snips one taken from the posterior iliac crest andanother from the buttock with the help of a disposable steriledermal hook and a blade The hook and blade used for eachparticipant were safely discarded [16]
In 2011 2703 resident adults from 16 communitiesincluding 11 baseline communities were examined for mfand nodules Since the Ministry of Health wanted to knowthe situation inside and outside the sentinel communitiesfour additional high risk communities were considered in2011 assessments Also 626 resident children (le10 years)from 11 communities (including three baseline communities)were examined for mf mf prevalence was expressed as apercentage of the number examined Due to heavy rainsBakambe one of the original sentinel communities wasinaccessible and therefore was not assessed Nodule palpationwas not followed up in the present study as it had not beendone in children at baseline
The comparison of baselinewith follow-up results in 2005(three months after treatment) in 2006 (six months aftertreatment) and in 2011 (11 months after treatment) was donein order to shed light on the dynamics ofOnchocerca volvulusinfection with annual mass treatment The comparison ofbaseline results to follow-up assessments was possible as onlyqualitative (presence or absence of mf or nodules) data wasconsidered
242 Follow-Up Entomological Assessment Black fly collec-tion was carried out at three sites in Bafang Foumbot andMassangam health districts for 3 days during the third weekof eachmonth fromMarch 2011 to February 2012The criteriafor selection of potential fly collectors set during baselineentomological assessment were followed Bafang collectionsite is located in extreme west of the region Foumbot in themiddle and Makouopsap in the extreme east of the region
Landing female Simulium flies were collected and imme-diately dissected in order to determine the parous rate Theremains of the dissected parous flies were preserved in a tubecontaining 70 ethanol The tubes were labeled by collectionsite date and time Simulium flies were then grouped inbatches up to 50 and sent to the laboratory where theywere stained with Mayerrsquos hematoxylin and fully dissected insearch for onchocercal larval stages (L1 L2 and L3) in theabdomen the thorax and the head [24] Infective flies weredefined as flies with L3 in the head as in the baseline surveysmentioned previously [18] This information was used to cal-culate the monthly and annual transmission potentials whichare the indicators of transmission The annual transmission
Journal of Parasitology Research 5
potential (ATP) was calculated as the sum of the individualmonthly transmission potentials (MTPs) over the period of ayear [23]
Data Analysis Parasitological data from adults and childrenas well as entomological data were entered and analysedgraphically in Microsoft Excel and Epi Info CDC AtlantaGA USA for chi square test of independence The ento-mological data was analysed and graphically illustrated inMicrosoft Excel
Ethical Approval All the surveys from the baseline to thefollow-up studies were approved by the Ministry of PublicHealth of Cameroon and the National Ethical Committeein Yaounde In addition the Emory University InstitutionalReview Board (eIRB-11 438) approved and considered themas nonresearch but routine program evaluation The fol-lowup of 2011 was also conducted under the auspices ofWorldHealth Organisation All assessed individuals had the libertyof opting out of assessments if they wished so without anyrepercussions
3 Results
31 Microfilaria (mf) and Nodule Prevalences Among adultsthe mf rate reduced by about 91 from baseline level of667 (range 531 to 881) in 1996 to 60 (range 14 to183 119875 lt 00001) in 2005 three months after ivermectintreatment However mf rate increased in 2006 six monthsafter ivermectin treatment to 139 (range 21 to 336)although it was not statistically different from 2005 mf rate119875 lt 0053 The decrease of mf rate 139 in 2006 to114 (range 0 to 596) in 2011 was also not significant(119875 lt 0053) (Table 2 and Figure 2) Only one communityhad 0 mf rate while six communities had mf rates above10 and two above 40 after 15 years of annual masstreatment Persistent high mf rates were observed in com-munities of Babouantou (214) in Bandja health districtNjone (419) in Foumbot health district and Makouopsap(596) in Massangam health district However there werecommunities (Bakonti in Bafang Health District Folap inFoumban Mbafam in Kekem and Njisseng in Kouptamo)which registered mf rates below 5 in adults
In children overall baselinemf rate of 292 (range 127to 518) reduced to 42 (range 0 to 250) in 2005 withan 856 reduction 119875 lt 00001 (Table 3 and Figure 2)However there was no significant difference between mf rate42 in 2005 and 45 in 2006 three months and six monthsrespectively after mass treatmentThere results for 2006 werealso not significantly different from mf rate 89 obtainedin 2011 eleven months after treatment (Table 3 and Figure 2)There were children in 2 (133) communities with mf ratesabove 20 (Njone 252 and Makouopsap 656) EvenBabouantou with mf rate of 158 was considered high fora program with 15 years of annual treatment In Ndjipta III ofBangangte Health District Folap of Foumban and Mbafamof Kekem mf rates among children were 06 or less
The overall baseline nodule rate in adults of 663 (range40 to 897) declined to 95 (range 400ndash897) 119875 lt00001 in the 2005This represents a decline of 856Then itincreased to 185 (range 67ndash303) in 2006 and declinedto 121 (range 15ndash434) in 2011 (Table 4) There were9 communities out of 16 with nodule prevalence of at least10 Of particular interest are persistent high nodule ratesin Bakambe (232) and Fondjanti (232) communities ofBafang Health District Fossang-chefferie (173) and Njone(186) in Foumbot health district andMakouopsap (434)in Massangam Health District
32 Entomology Baseline monthly transmission potentialswere 15 in Bafang and 2104 in Foumbot (Table 5) In thefollow-up assessment the infection rates were 02 in BafangHealth District 088 in Foumbot and 067 in MassangamThe infective rates were 0 in Bafang Health District 019in Foumbot and 018 in Massangam Annual biting rateswere 52610 in Bafang 28560 in Foumbot and 125360 inMakouopsap while annual transmission potentials were 070 and 310 respectively Biting was generally throughout theyear although the main peak biting period in Makouopsapwas observed from January to May (Figure 3)
4 Discussion
Annual mass treatment with ivermectin for 15 years hadconsiderably reduced microfilaria and nodule prevalence inall the sentinel communities of West Region of CameroonElimination is considered attained when the microfilariaprevalence in skin snips is less than 5 in sampled communi-ties in less than 1 in 90of sampled communities andwhenentomological criteria of less than 05 infected flies1000 areattained [11] Among adults Foumban Health District wasclose to the epidemiological criterion while Bafang HealthDistrict was not very far from the entomological criterionwith the ATP of 0 mf rate among children in Foumbanand Kekem health districts was zero indicating no recentinfection an indication that interruption of transmissionmay be attained However the mf rates in Baham BanjaBangangte Foumbot andMassangam health districts amongadults and children were still uncomfortably high showingcontinuing transmission In adults nodule rates near orabove the threshold 20 for the mass treatment in somecommunities were of a major concern The infective rateof 018 to 019 and ATP of 70 to 300 confirmed continuingtransmission
One possible explanation for high mf rates in childrenand adults could have been low treatment coverage Howeverthe methodology for validating UTG treatment coveragefollowed standard statistical methods for selecting sampledcommunities and the interviewees This methodology hadbeen tested and used to validate performance of CDTI inCameroon and in other onchocerciasis endemic countries[14 15 25]TheUTG treatment coverage results were also cor-roborated by independent monitoring results in unpublishedreports supported by APOC Therefore there is no reason tobelieve that UTG treatment coverage was low and responsible
6 Journal of Parasitology Research
Table2Com
parin
gmfp
revalencea
mon
gadultsatbaselin
e(1996)a
ndfollo
wup
in2005200
6and2011three
mon
thssix
mon
thsandele
venmon
thsrespectiv
elyafte
rmasstreatment
inWestR
egion
Cameroo
n
Distric
tCom
mun
ityBa
selin
e1996
(119899=931)
Follo
wup
2005(119899=878)
Follo
wup
200
6(119899=782)
Follo
wup
2011(119899=2703)
No
exam
ined
No
positive
mf
positive
No
exam
ined
No
positive
mf
positive
No
exam
ined
No
positive
mf
positive
No
exam
ined
No
positive
mf
positive
Bakassa
6136
590
140
214lowast
972
21
251
1456
Bafang
Bakonti
5236
692
993
30lowast
753
40
338
1236
Fond
janti
124
8770
2125
864
Bakambe
122
65533
105
329lowast
916
66
ND
ND
ND
Baham
Bapi
145
77531
ND
ND
ND
ND
ND
ND
189
21111
Band
jaBa
bouantou
(Batou
la)
6849
721
537
132lowast
7614
184
8418
214
Bang
angte
Batchingou
8461
726
102
11108lowast
8014
175
247
45182
NdjiptaIII
(Fop
-Tchui)
8871
807
781
13lowast
576
105lowastlowast
929
98
Foum
bot
Fossang-
chefferielowast
3228
875
7113
183lowast
7219
264lowastlowast
150
19127lowastlowastlowast
Njone
5952
881
135
1181lowast
122
41336lowastlowast
167
70419lowastlowastlowast
Kekem
Mbafam
3927
692
952
21lowast
112
436
163
849
Penk
a-Michel
Bakassa
5732
561
ND
ND
ND
ND
ND
ND
195
736
Foum
ban
Folap
ND
ND
ND
ND
ND
ND
ND
ND
ND
265
000
Kouo
ptam
oNjisseng
ND
ND
ND
ND
ND
ND
ND
ND
ND
168
530
Malantouen
Matou
pou
ND
ND
ND
ND
ND
ND
ND
ND
ND
170
1376
Massang
amMakou
opsap
ND
ND
ND
ND
ND
ND
ND
ND
ND
9959
596
931
621
667
878
5360lowast
782
109
139
2703
308
114
NDnot
done
lowastSign
ificant
(119875lt005)mdash
follo
wup
2005
comparedwith
theb
aseline
lowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2006
comparedwith
2005
follo
wup
lowastlowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2011comparedwith
2006
follo
wup
Journal of Parasitology Research 7
667
6139 114
292
42 45 89
01020304050607080
m
f pre
vale
nce
AdultsChildren
1996119899 = 931 2005 (3 months after treatment)
119899 = 878
2006 (6 months
Baseline Followup
after treatment)119899 = 782
2011 (11 monthafter treatment)
119899 = 2703
Figure 2 Comparison of mf rates among adults and children atbaseline 1996 with followup surveys in 2005 2006 and 2011 inWestRegion of Cameroon
for failure to attain optimal parasitological and entomologicalimpacts
High vector density and mf rates suggest that the forceof transmission may have been very high and most likely thereason for the results obtained [26]The present study did notconsider the standardmeasure of intensity of infection whichis related to force of infection community mf load (CMFL)This requires a calculation that involves weighing the snipand counting the microfilaria which was not done [19] Werecommend that it should be done in future studies
In Massangam Health District it is possible that high mfand nodule rates in the follow-up assessments may be dueto the ldquoforce of infectionrdquo across the neighbouring CentralRegion where peer-reviewed studies indicate considerableonchocerciasis transmission [27 28] River Nja a tributary ofRiver Noun and River Kichi a tributary of River Mbam areknown black fly breeding sites responsible for cross-bordertransmission between West and Central regions Thereforewe recommend collaboration between the regions in order tounderstand the limits of cross-border onchocerciasis affectedarea and harmonize intervention if elimination becomes thegoal in Cameroon
Another possible explanation for high mf rates couldbe related to suboptimal response to ivermectin observedin some onchocerciasis endemic areas of Ghana The adultfemale O volvulus worms were resuming microfilaria repro-duction more rapidly after ivermectin treatment than wouldnormally be expected suggesting possible development ofresistance to ivermectin [29ndash31] We recommend that thepossibility of suboptimal response to ivermectin in WestRegion be investigated
The microfilaria rate in adults and children tended tofollow the expected trend where a single annual dose ofivermectin over a number of years significantly reduced thelow mf rates that tend to persist [3] The observed patternindicated a tendency for themf rate to raise a fewmonths aftermass treatment until another dose of ivermectin is providedconfirming that microfilarial production is not cumulativelyreduced by several annual ivermectin treatments [32] Themf rate trend at three six and eleven months after mass
treatment is usually not different from the infection ratewithin the flies over a period after mass treatment withivermectin [33] Ivermectin kills existing microfilariae andtends to exert an ldquoembryostatic effectrdquo by which microfilarialproduction is suppressed over a few weeks after treatmentbut then after the mf rate begins to increase [32] Underfavourable ecological conditions interruption of onchocer-ciasis transmission with annual mass treatment may requiremany more years before it is attained
As for twice yearly treatment with ivermectin or whenit is coupled with vector control infection rate continuedto fall implying that interruption of transmission could berapidly attained [1 33 34] We recommend that West Regionof Cameroon should consider twice yearly treatment or atleast annual treatment with targeted vector control
In the present study some communities (Folap andNjisseng) in Foumban and Kouoptamo health districts hadmf rates lower than 5 in adults and 0 in children Inthese communities the Diawara et al criteria are closeto being attained and yet with low levels of infectiontransmission is much more efficient than at high levels ofinfection [35ndash37] Thus if low levels of infection are notdetected and controlled they could result in fast diseaserecrudescence Skin snip (microscopy) has low sensitivity ofless than 20 at less than 20 nodule rate and the resultsobtained may not reflect correct mf endemicity levels [38]Therefore interventions in these health districts cannot behalted as disease recrudescence could occur [29 30] Whereinterruption of transmission of onchocerciasis is the objectivewe recommend a search for affordable less intrusive rapidsensitive and highly specific diagnostic tools for low levelinfections in order to validate interruption of onchocerciasistransmission
The APOC threshold for launching mass treatment isan onchocercal nodule rate of ge20 Fondjanti community(Bandja Health District) with nodule rate of 23 and mfrate of 64 would pass for mass treatment while Njonecommunity (Foumbot Health District) with nodule rate of186 and mf rate of 419 would fail [39] Nodule rate couldalso be confounded by the presence of ganglia and Taeniasolium [40 41] The entomological results showed that therisk of contracting onchocerciasis in FoumbotHealthDistrictwas higher than in Bafang Health District confirming thereliability of mf rates compared with nodule rates With theshift from control to elimination of onchocerciasis in Africawe recommend that nodule prevalence should not be usedto determine whether an endemic area should receive masstreatment or not
Annual biting rates with the range of 28560 to 125380are some of the highest observed globally Yet infective ratein Bafang from the western part of the region was zerojustifying low mf rates (06 in children and a mean of52 in adults) The question would be whether annual masstreatment could be withdrawn without resulting in diseaserecrudescence Existing low level transmission with the highannual biting rate of 52610 could still result in onchocerciasisrecrudescence It was also evident in this study that one-month baseline entomological data was likely to miss peakbiting transmission pattern of Simulium vectors and the
8 Journal of Parasitology Research
Table3Com
parin
gmfp
revalencea
mon
gchild
renatbaselin
e(1996)and
follo
wup
in2005200
6and2011three
mon
thssix
mon
thsandele
venmon
thsrespectiv
elyafterm
asstreatment
inWestR
egion
Cameroo
n
Distric
tCom
mun
ityBa
selin
e1996
(119899=185)
Follo
wup
2005(119899=403)
Follo
wup
200
6(119899=134)
Follo
wup
2011(119899=626)
No
Exam
ined
No
positive
mf
positive
No
Exam
ined
No
positive
mf
positive
No
Exam
ined
No
positive
mf
positive
Noexam
No
positive
mf
positive
Bafang
Bakonti-B
akassa
102
13127
740
0lowast43
000
167
106
Bafang
Batchieu
704
57
40
00
Baham
Bapi
ND
ND
ND
292
69
Band
jaBa
bouantou
(Batou
la)lowast
ND
ND
ND
647
109
143
214
193
158
Bang
angte
Batchingoulowast
ND
ND
ND
241
42
152
133
211
48
Bang
angte
NdjiptaIII(Fo
p-Tchu
i)lowastND
ND
ND
632
32
50
00
250
00
FossangCh
efferie
ND
ND
ND
380
00
40
00
252
80
Foum
bot
Njone
2019
950
123
25lowast
161
63
8224
293lowastlowastlowast
Foum
bot
Kousang-Malanden
6322
349
ND
ND
ND
ND
ND
ND
ND
ND
ND
Kekem
Mbafamlowast
ND
ND
ND
580
00
330
00
200
00
Penk
a-Michel
Bakassa
ND
ND
ND
ND
ND
ND
ND
ND
ND
741
14Fo
umban
Folap
ND
ND
ND
ND
ND
ND
ND
ND
ND
108
000
Kouo
ptam
oNjisseng
ND
ND
ND
ND
ND
ND
ND
ND
ND
241
42
Massang
amMakou
opsap
ND
ND
ND
ND
ND
ND
ND
ND
ND
3221
656
12185
5429
240
317
42lowast
134
645
626
5689
NDnot
done
lowastSign
ificant
(119875lt005)mdash
follo
wup
2005
comparedwith
theb
aseline
lowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2006
comparedwith
2005
follo
wup
lowastlowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2011comparedwith
2006
follo
wup
Journal of Parasitology Research 9
Table4
Com
parin
gnod
ulep
revalencea
mon
gadu
ltsatbaselin
e(1996)and
follo
wup
in2005200
6and2011three
mon
thssix
mon
thsandele
venmon
thsrespectiv
elyafterm
asstreatment
inWestR
egion
Cameroo
n
Distric
tCom
mun
ityBa
selin
e1996
(119899=305)
Follo
wup
2005(119899=780)
Follo
wup
200
6(119899=782)
Follo
wup
2011(119899=2703)
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
Bafang
Bakassa
2716
593
139
110
79lowast
9711
113
251
2184
Bakonti
2711
407
9850
51lowast
755
67
338
36107
Fond
janti
2719
704
125
29232
Bakambe
2719
704
105
110
105lowast
9113
143
125
29232
Baham
Bapi
2915
517
ND
ND
ND
ND
ND
ND
189
1579
Band
jaBa
bouantou
(Batou
la)
2616
615
6150
82lowast
7618
237lowastlowast
8412
143
Bang
angte
Batchingou
2922
759
101
160
158lowast
8023
288lowastlowast
247
29117lowastlowastlowast
NdjiptaIII(Fo
p-Tchu
i)29
23793
7850
64lowast
578
140lowastlowast
929
98
Foum
bot
Fossang-chefferie
2824
857
7170
99lowast
7218
250lowastlowast
150
26173lowastlowastlowast
Njone
2926
897
3490
265lowast
122
37303
167
31186lowastlowastlowast
Kekem
Mbafam
2417
708
9350
54lowast
112
12107lowastlowast
163
27166
Penk
a-Michel
Bakassa
3012
400
ND
ND
ND
ND
ND
ND
195
1577
Foum
ban
Folap
ND
ND
ND
ND
ND
ND
ND
ND
ND
265
415
Kouo
ptam
oNjisseng
ND
ND
ND
ND
ND
ND
ND
ND
ND
168
636
Malantouen
Matou
pou
ND
ND
ND
ND
ND
ND
ND
ND
ND
170
953
Massang
amMakou
opsap
ND
ND
ND
ND
ND
ND
ND
ND
ND
9943
434
332
220
663
780
7495lowast
782
145
185lowastlowast
2828
341
121lowastlowastlowast
NDnot
done
lowastSign
ificant
(119875lt005)mdash
follo
wup
2005
comparedwith
theb
aseline
lowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2006
comparedwith
2005
follo
wup
lowastlowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2011comparedwith
2006
follo
wup
10 Journal of Parasitology Research
Table 5 Comparing baseline entomological data of 1996 at two fly collection sites and three during 2011
Monthyear of black fly collection Baseline May 1996 Followup 2011Black fly collection sites Bafang (Basseu) Foumbot (Maka) Bafang Foumbot MassangamNumber of Simulium caught 5 166 5261 2856 12538Number of Simulium dissected 5 142 5261 2856 12138Number of parous flies 1 97 1502 1028 2845Parous rate () 20 683 285 36 234Number of Simulium flies infected (L1 L2 L3] 1 12 3 9 19Infection rate () 2000 845 020 088 067Number of Simulium flies infective L3 larval stage in the head 20 2 0 2 5Infective rate () 200 211 000 019 018Monthly biting rate per person 750 166000 na na naMonthly transmission potentiallowast 150 21040 na na naAnnual biting rate per person Na na 52610 28560 125380Annual transmission potential Na na 0 70 310
0
500
1000
1500
2000
2500
3000
3500
4000
No
of fl
ies c
olle
cted
BafangFoumbotMakouopsap
MarApr2011 2012
May Jun Jul AugSeptOctNovDec Jan Feb
Figure 3 Monthly seasonal biting of Simulium flies at 3 fly catchingsites in West Region
calculation ofATPTherefore collection of entomological dataover several months is required as reflected in the follow-up study The information on peak biting and transmissionpatterns could effectively be utilized for ivermectin treatmentfor maximum impact on transmission especially where theforce of transmission is considerably high if elimination ofonchocerciasis is the goal In the follow-up survey it is onlyat Bafang fly collection site that the entomological criterionfor interruption of transmission was met with an ATP of zero[42]
The present study however did not perform moleculartesting in order to determine if the L3 larvae wereO volvulusor another (animal) Onchocerca species Based on humanmf prevalence in skin and infections in children we thinkthat there is likelihood that some of the larvae observedin vectors were O volvulus However a study conducted inNorth Region of Cameroon during the 1990s showed that
33 of infective larvae in S damnosum were O volvuluswhereas 65 were O ochengi and 2 were O ramachandrini[43] It is until such a study is conducted in West Region ofCameroon that we will know the extent to which O ochengiis responsible for a significant proportion of infected flies thatcould confound the infection rate there
Our findings reflecting an observation period of 15 yearsshowed that annual mass treatment with ivermectin may notinterrupt the transmission of onchocerciasis in all differentecological zones of West Region Therefore the intensive useof ivermectin is recommended if interruption of transmissionof onchocerciasis is to be attained [1]
5 Conclusion
Annual mass treatment with ivermectin through commu-nity-directed treatment was preferred as a good and lessexpensive method for controlling onchocerciasis in endemicAfrican countries with assistance from the African Pro-gramme for Onchocerciasis Control The studies in MaliSenegal and Nigeria have shown that an annual dose ofivermectin had interrupted transmission of the disease andall interventions could be halted without the risk of diseaserecrudescence However an annual dose of ivermectin hasnot interrupted transmission after 15 years of mass treatmentin some areas in West Region of Cameroon just like inNorth region [8] It has also been less effective in someonchocerciasis endemic areas in Ghana The present paperagain highlights the fact that for interruption of onchocer-ciasis transmission feasible and different but complementarystrategic options should be adopted as elimination becomesthe goal in Africa
Acknowledgments
The investigators would like to acknowledge the staff ofMinistry of Health at the national regional and healthdistrict levels in West Region along with Carter CenterCameroon Office for mobilizing and educating selected
Journal of Parasitology Research 11
communities and providing policy and administrative sup-port The involvement of community members in selectedcommunities in mf and nodule assessments and Simulium flycollection is highly appreciated The Carter Center the LionsClubs International Foundation (LCIF) and the African Pro-gramme for onchocerciasis Control (APOC) which fundedthe CDTI activities and the surveys are also highly appreci-ated
References
[1] E W Cupp and M S Cupp ldquoShort report impact of iver-mectin community-level treatments on elimination of adultOnchocerca volvulus when individuals receive multiple treat-ments per yearrdquoThe American Journal of Tropical Medicine andHygiene vol 73 no 6 pp 1159ndash1161 2005
[2] H R Taylor M Pacque B Munoz and B M Greene ldquoImpactof mass treatment of onchocerciasis with ivermectin on thetransmission of infectionrdquo Science vol 250 no 4977 pp 116ndash118 1990
[3] G J J M Borsboom B A Boatin N J D Nagelkerkeet al ldquoImpact of ivermectin on onchocerciasis transmissionassessing the empirical evidence that repeated ivermectin masstreatmentsmay lead to eliminationeradication inWest-AfricardquoFilaria Journal vol 2 article 8 2003
[4] A D Hopkins ldquoIvermectin and onchocerciasis is it all solvedrdquoEye vol 19 no 10 pp 1057ndash1066 2005
[5] L Yameogo ldquoSpecial intervention zonesrdquo Annals of TropicalMedicine and Parasitology vol 102 supplement 1 pp 23ndash242008
[6] D H Molyneux and M N Malecela ldquoNeglected tropicaldiseases and themillennium development goals why the ldquootherdiseasesrdquo matter reality versus rhetoricrdquo Parasites amp Vectorsvol 4 2011
[7] WHOReportAcceleratingWorkToOvercome theGlobal Impactof Neglected Tropical Disease A Roadmap For Implementationvol 1211WorldHealthOrganization 20AvenueAppia GenevaSwitzerland 2012
[8] M N Katabarwa A Eyamba P Nwane et al ldquoSeventeenyears of annual distribution of ivermectin has not interruptedonchocerciasis transmission in North Region Cameroonrdquo TheAmerican Journal of Tropical Medicine and Hygiene vol 85 no6 pp 1041ndash1049 2011
[9] B A Boatin and F O Richards ldquoControl of onchocerciasisrdquoAdvances in Parasitology vol 61 pp 349ndash394 2006
[10] D R Hopkins F O Richards and M Katabarwa ldquoWhitheronchocerciasis control in Africardquo American Journal of TropicalMedicine and Hygiene vol 72 no 1 pp 1ndash2 2005
[11] L Diawara M O Traore A Badji et al ldquoFeasibilityof onchocerciasis elimination with ivermectin treatment inendemic foci in Africa first evidence from studies in Mali andSenegalrdquo PLoS Neglected Tropical Diseases vol 3 no 7 articlee497 2009
[12] F O Richards E S Miri M Katabarwa et al ldquoThe carter cen-terrsquos assistance to river blindness control programs establish-ing treatment objectives and goals for monitoring ivermectindelivery systems on two continentsrdquo The American Journal ofTropical Medicine and Hygiene vol 65 no 2 pp 108ndash114 2001
[13] P Salant and D A Dilman How to Conduct Your Own SurveyJohn Wiley amp Sons 1994
[14] M N Katabarwa P Habomugisha and F O Richards ldquoImple-menting community-directed treatmentwith ivermectin for the
control of onchocerciasis in Uganda (1997-2000) an evalua-tionrdquo Annals of Tropical Medicine and Parasitology vol 96 no1 pp 61ndash73 2002
[15] E C Emukah U Enyinnaya N S Olaniran et al ldquoFactorsaffecting the attrition of community-directed distributors ofivermectin in an onchocerciasis-control programme in the Imoand Abia states of south-eastern Nigeriardquo Annals of TropicalMedicine and Parasitology vol 102 no 1 pp 45ndash51 2008
[16] A Prost and J Prodrsquohon ldquoLe diagnostique parasitologique delrsquoonchocercose revue critique des methods en usagerdquoMedicineTropicale vol 38 pp 519ndash532 1978
[17] H Schulz Key ldquoA simple technique to assess the total number ofOnchocerca volvulusmicrofilariae in skin snipsrdquo Tropenmedizinund Parasitologie vol 29 no 1 pp 51ndash54 1978
[18] WHO Report ldquoOnchocerciasis and its control Report of aWHO Expert Committee on Onchocerciasis Controlrdquo TechRep 852 Geneva Switzerland 1995
[19] WHO Report Strategies For Ivermectin Distribution ThroughPrimaryHealth Care SystemWHOPHL91 24WHOGenevaSwitzerland 1991
[20] E J Albiez D W Buttner and B O L Duke ldquoDiagnosisand extirpation of nodules in human onchocerciasisrdquo TropicalMedicine and Parasitology vol 39 no 4 pp 331ndash346 1988
[21] P Ngoumou J F Walsh and J M Mace ldquoA rapid mappingtechnique for the prevalence and distribution of onchocerciasisa Cameroon case studyrdquo Annals of Tropical Medicine andParasitology vol 88 no 5 pp 463ndash474 1994
[22] M Katabarwa A W Onapa and B Nakileza ldquoRapid epidemi-ological mapping of onchocerciasis in areas of uganda whereSimulium neavei SL is the vectorrdquo East African Medical Journalvol 76 no 8 pp 440ndash446 1999
[23] J F Walsh J B Davies R Le Berre and R Garms ldquoStandard-ization of criteria for assessing the effect of Simulium control inonchocerciasis control programmesrdquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 72 no 6 pp 675ndash676 1978
[24] J B Davies ldquoA rapid staining and clearing technique for detect-ing filarial larvae in alcohol-preserved vectorsrdquo Transactions ofthe Royal Society of Tropical Medicine and Hygiene vol 89 no3 p 280 1995
[25] M Katabarwa P Habomugisha A Eyamba S Agunyo andC Mentou ldquoMonitoring ivermectin distributors involved inintegrated health care services through community-directedinterventionsmdasha comparison of Cameroon and Uganda expe-riences over a period of three years (2004ndash2006)rdquo TropicalMedicine and International Health vol 15 no 2 pp 216ndash2232010
[26] J Remme O Ba K Y Dadzie and M Karam ldquoA force-of-infection model for onchocerciasis and its applications inthe epidemiological evaluation of the onchocerciasis controlprogramme in the volta river basin areardquo Bulletin of the WorldHealth Organization vol 64 no 5 pp 667ndash681 1986
[27] P Barbazan H Escaffre R Mbentengam and M BoussinesqldquoEntomologic study on the transmission of onchocerciasis ina forest-savanna transition area of Cameroonrdquo Bulletin de laSociete de Pathologie Exotique vol 91 no 2 pp 178ndash182 1998
[28] E Cadot P Barbazan andM Boussinesq ldquoGeographical deter-minants of onchocerciasis transmission in a forestsavannahtransition zone two villages of the mbam focusrdquo Sante vol 8no 6 pp 429ndash435 1998
[29] K Awadzi S K Attah E T Addy et al ldquoThirty-monthfollow-up of sub-optimal responders to multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in Ghanardquo
12 Journal of Parasitology Research
Annals of Tropical Medicine and Parasitology vol 98 no 4 pp359ndash370 2004
[30] K Awadzi D A Boakye G Edwards et al ldquoAn investigationof persistent microfilaridermias despite multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in GhanardquoAnnals of Tropical Medicine and Parasitology vol 98 no 3 pp231ndash249 2004
[31] M Y Osei-Atweneboana J K Eng D A Boakye J OGyapong and R K Prichard ldquoPrevalence and intensity ofOnchocerca volvulus infection and efficacy of ivermectin inendemic communities in Ghana a two-phase epidemiologicalstudyrdquoThe Lancet vol 369 no 9578 pp 2021ndash2029 2007
[32] C Bottomley V Isham R C Collins and M G BasanezldquoRates of microfilarial production by Onchocerca volvulus arenot cumulatively reduced by multiple ivermectin treatmentsrdquoParasitology vol 135 no 13 pp 1571ndash1581 2008
[33] R Garms T L Lakwo R Ndyomugyenyi et al ldquoThe elimina-tion of the vector Simulium neavei from the Itwara onchocerci-asis focus in Uganda by ground larvicidingrdquo Acta Tropica vol111 no 3 pp 203ndash210 2009
[34] R Ndyomugyenyi E Tukesiga D W Buttner and R GarmsldquoThe impact of ivermectin treatment alone and when inparallel with Simulium neavei elimination on onchocerciasis inUgandardquo Tropical Medicine and International Health vol 9 no8 pp 882ndash886 2004
[35] H P Duerr and M Eichner ldquoEpidemiology and control ofonchocerciasis the threshold biting rate of savannah onchocer-ciasis in Africardquo International Journal for Parasitology vol 40no 6 pp 641ndash650 2010
[36] K Dietz ldquoDensity-dependence in parasite transmissiondynamicsrdquo Parasitology Today vol 4 no 4 pp 91ndash97 1988
[37] M G Basanez J H F Remme E S Alley et al ldquoDensity-dependent processes in the transmission of human onchocerci-asis relationship between the numbers ofmicrofilariae ingestedand successful larval development in the simuliid vectorrdquoParasitology vol 110 no 4 pp 409ndash427 1995
[38] B A Boatin L Toe E S Alley N J D Nagelkerke GBorsboom and J D F Habbema ldquoDetection of Onchocercavolvulus infection in lowprevalence areas a comparison of threediagnostic methodsrdquo Parasitology vol 125 no 6 pp 545ndash5522002
[39] M Noma B E B Nwoke I Nutall et al ldquoRapid epidemio-logical mapping of onchocerciasis (REMO) its application bythe African programme for onchocerciasis control (APOC)rdquoAnnals of Tropical Medicine and Parasitology vol 96 supple-ment 1 pp S29ndashS39 2002
[40] G Fobi J R M Mbina G Ozoh et al ldquoOnchocerciasis inthe area of Lastourville Gabon Clinical and entomologicalaspectsrdquo Bulletin de la Societe de Pathologie Exotique vol 99no 4 pp 269ndash271 2006
[41] M N Katabarwa A Eyamba M Chouaibou et al ldquoDoesonchocerciasis transmission take place in hypoendemic areasa study from theNorth Region of CameroonrdquoTropicalMedicineand International Health vol 15 no 5 pp 645ndash652 2010
[42] WHO Report Certification of Elimination of Human Onchocer-ciasis Criteria and Procedures Criteria For Certification of Inter-ruption of TransmissionElimination of Human OnchocerciasisWorld Health Organization Geneva Switzerland 2001
[43] R Seidenfaden A Fischer I Bonow D Ekale V Tanya andA Renz ldquoCombined benefits of annual mass treatment withivermectin and cattle zooprophylaxis on the severity of humanonchocerciasis in northern Cameroonrdquo Tropical Medicine andInternational Health vol 6 no 9 pp 715ndash725 2001
were assessed for mf Every participant was examined in awell-lit private room Trained health workers performed apalpation examination on the partially undressed participantpaying attention to bony prominences of the torso iliac crestsand upper trochanter of the femurs Onchocercal noduleswere identified clinically as being firm painless and mobile[19ndash21] Results were recorded on the form as ldquopositiverdquo orldquonegativerdquo Nodule prevalence was expressed as a percentageof the total number of persons examined
232 Entomological Survey Fly collection was carried out inBafang and Foumbot for a period of one month Potential flycollectors of at least 20 years of age were fully informed of thenature of work and the possibility of opting out of the studyif they wished so at any time without any repercussionsThecollectors worked 2 days in Bafang and 15 days in Foumbot inMay 1996 near the river banks where they exposed their legsin shifts from 0600 to 1200 and from 1200 to 1800 hours [19]As female Simulium flies seeking a blood meal settled on theexposed legs suction tubes were used to catch them beforethey bit Using a dissecting microscope (40x magnification)an experienced dissector opened the vector fliesrsquo abdomensthoraxes and heads Dissected flies were then examinedunder a light microscope in order to identify the presence ofinfection and to count the number of larval stages (L1 L2 andL3)when present Since fly collection lasted onemonth it wasnot possible to determine the annual transmission potential(ATP) Infective flies were defined as flies with L3s in the head[22 23]
Monthly biting rate (MBR) was calculated as per thestandard method as
MBR = (Number of flies collected
times number of days in the month)
times (Number of fly collection days)minus1
(1)
24 Follow-Up Assessments
241 Parasitological Assessments 2005 2006 and 2011 Base-line mf rates in the sentinel communities were followed up inonly 9 sentinel communities in 2005 threemonths aftermasstreatment with ivermectin in 2006 six months after andelevenmonths after treatment in 2011Three baseline sentinelcommunities (Foundjanti in Bafang Bapi in Baham andBakassa in Penka Michel) were not assessed in 2005 as theywere inaccessible as a result of heavy rains and the status quowasmaintained in 2006 A total of 878 and 780 resident adultswere assessed in 2005 for mf and nodules respectively Also403 resident children (le10 years old) were assessed for mf
In 2006 assessment for mf and nodules covered 782resident adults Skin snips were obtained from only 134children Skin snipping performed in 2005 and 2006 involvedtwo skin snips one taken from the posterior iliac crest andanother from the buttock with the help of a disposable steriledermal hook and a blade The hook and blade used for eachparticipant were safely discarded [16]
In 2011 2703 resident adults from 16 communitiesincluding 11 baseline communities were examined for mfand nodules Since the Ministry of Health wanted to knowthe situation inside and outside the sentinel communitiesfour additional high risk communities were considered in2011 assessments Also 626 resident children (le10 years)from 11 communities (including three baseline communities)were examined for mf mf prevalence was expressed as apercentage of the number examined Due to heavy rainsBakambe one of the original sentinel communities wasinaccessible and therefore was not assessed Nodule palpationwas not followed up in the present study as it had not beendone in children at baseline
The comparison of baselinewith follow-up results in 2005(three months after treatment) in 2006 (six months aftertreatment) and in 2011 (11 months after treatment) was donein order to shed light on the dynamics ofOnchocerca volvulusinfection with annual mass treatment The comparison ofbaseline results to follow-up assessments was possible as onlyqualitative (presence or absence of mf or nodules) data wasconsidered
242 Follow-Up Entomological Assessment Black fly collec-tion was carried out at three sites in Bafang Foumbot andMassangam health districts for 3 days during the third weekof eachmonth fromMarch 2011 to February 2012The criteriafor selection of potential fly collectors set during baselineentomological assessment were followed Bafang collectionsite is located in extreme west of the region Foumbot in themiddle and Makouopsap in the extreme east of the region
Landing female Simulium flies were collected and imme-diately dissected in order to determine the parous rate Theremains of the dissected parous flies were preserved in a tubecontaining 70 ethanol The tubes were labeled by collectionsite date and time Simulium flies were then grouped inbatches up to 50 and sent to the laboratory where theywere stained with Mayerrsquos hematoxylin and fully dissected insearch for onchocercal larval stages (L1 L2 and L3) in theabdomen the thorax and the head [24] Infective flies weredefined as flies with L3 in the head as in the baseline surveysmentioned previously [18] This information was used to cal-culate the monthly and annual transmission potentials whichare the indicators of transmission The annual transmission
Journal of Parasitology Research 5
potential (ATP) was calculated as the sum of the individualmonthly transmission potentials (MTPs) over the period of ayear [23]
Data Analysis Parasitological data from adults and childrenas well as entomological data were entered and analysedgraphically in Microsoft Excel and Epi Info CDC AtlantaGA USA for chi square test of independence The ento-mological data was analysed and graphically illustrated inMicrosoft Excel
Ethical Approval All the surveys from the baseline to thefollow-up studies were approved by the Ministry of PublicHealth of Cameroon and the National Ethical Committeein Yaounde In addition the Emory University InstitutionalReview Board (eIRB-11 438) approved and considered themas nonresearch but routine program evaluation The fol-lowup of 2011 was also conducted under the auspices ofWorldHealth Organisation All assessed individuals had the libertyof opting out of assessments if they wished so without anyrepercussions
3 Results
31 Microfilaria (mf) and Nodule Prevalences Among adultsthe mf rate reduced by about 91 from baseline level of667 (range 531 to 881) in 1996 to 60 (range 14 to183 119875 lt 00001) in 2005 three months after ivermectintreatment However mf rate increased in 2006 six monthsafter ivermectin treatment to 139 (range 21 to 336)although it was not statistically different from 2005 mf rate119875 lt 0053 The decrease of mf rate 139 in 2006 to114 (range 0 to 596) in 2011 was also not significant(119875 lt 0053) (Table 2 and Figure 2) Only one communityhad 0 mf rate while six communities had mf rates above10 and two above 40 after 15 years of annual masstreatment Persistent high mf rates were observed in com-munities of Babouantou (214) in Bandja health districtNjone (419) in Foumbot health district and Makouopsap(596) in Massangam health district However there werecommunities (Bakonti in Bafang Health District Folap inFoumban Mbafam in Kekem and Njisseng in Kouptamo)which registered mf rates below 5 in adults
In children overall baselinemf rate of 292 (range 127to 518) reduced to 42 (range 0 to 250) in 2005 withan 856 reduction 119875 lt 00001 (Table 3 and Figure 2)However there was no significant difference between mf rate42 in 2005 and 45 in 2006 three months and six monthsrespectively after mass treatmentThere results for 2006 werealso not significantly different from mf rate 89 obtainedin 2011 eleven months after treatment (Table 3 and Figure 2)There were children in 2 (133) communities with mf ratesabove 20 (Njone 252 and Makouopsap 656) EvenBabouantou with mf rate of 158 was considered high fora program with 15 years of annual treatment In Ndjipta III ofBangangte Health District Folap of Foumban and Mbafamof Kekem mf rates among children were 06 or less
The overall baseline nodule rate in adults of 663 (range40 to 897) declined to 95 (range 400ndash897) 119875 lt00001 in the 2005This represents a decline of 856Then itincreased to 185 (range 67ndash303) in 2006 and declinedto 121 (range 15ndash434) in 2011 (Table 4) There were9 communities out of 16 with nodule prevalence of at least10 Of particular interest are persistent high nodule ratesin Bakambe (232) and Fondjanti (232) communities ofBafang Health District Fossang-chefferie (173) and Njone(186) in Foumbot health district andMakouopsap (434)in Massangam Health District
32 Entomology Baseline monthly transmission potentialswere 15 in Bafang and 2104 in Foumbot (Table 5) In thefollow-up assessment the infection rates were 02 in BafangHealth District 088 in Foumbot and 067 in MassangamThe infective rates were 0 in Bafang Health District 019in Foumbot and 018 in Massangam Annual biting rateswere 52610 in Bafang 28560 in Foumbot and 125360 inMakouopsap while annual transmission potentials were 070 and 310 respectively Biting was generally throughout theyear although the main peak biting period in Makouopsapwas observed from January to May (Figure 3)
4 Discussion
Annual mass treatment with ivermectin for 15 years hadconsiderably reduced microfilaria and nodule prevalence inall the sentinel communities of West Region of CameroonElimination is considered attained when the microfilariaprevalence in skin snips is less than 5 in sampled communi-ties in less than 1 in 90of sampled communities andwhenentomological criteria of less than 05 infected flies1000 areattained [11] Among adults Foumban Health District wasclose to the epidemiological criterion while Bafang HealthDistrict was not very far from the entomological criterionwith the ATP of 0 mf rate among children in Foumbanand Kekem health districts was zero indicating no recentinfection an indication that interruption of transmissionmay be attained However the mf rates in Baham BanjaBangangte Foumbot andMassangam health districts amongadults and children were still uncomfortably high showingcontinuing transmission In adults nodule rates near orabove the threshold 20 for the mass treatment in somecommunities were of a major concern The infective rateof 018 to 019 and ATP of 70 to 300 confirmed continuingtransmission
One possible explanation for high mf rates in childrenand adults could have been low treatment coverage Howeverthe methodology for validating UTG treatment coveragefollowed standard statistical methods for selecting sampledcommunities and the interviewees This methodology hadbeen tested and used to validate performance of CDTI inCameroon and in other onchocerciasis endemic countries[14 15 25]TheUTG treatment coverage results were also cor-roborated by independent monitoring results in unpublishedreports supported by APOC Therefore there is no reason tobelieve that UTG treatment coverage was low and responsible
6 Journal of Parasitology Research
Table2Com
parin
gmfp
revalencea
mon
gadultsatbaselin
e(1996)a
ndfollo
wup
in2005200
6and2011three
mon
thssix
mon
thsandele
venmon
thsrespectiv
elyafte
rmasstreatment
inWestR
egion
Cameroo
n
Distric
tCom
mun
ityBa
selin
e1996
(119899=931)
Follo
wup
2005(119899=878)
Follo
wup
200
6(119899=782)
Follo
wup
2011(119899=2703)
No
exam
ined
No
positive
mf
positive
No
exam
ined
No
positive
mf
positive
No
exam
ined
No
positive
mf
positive
No
exam
ined
No
positive
mf
positive
Bakassa
6136
590
140
214lowast
972
21
251
1456
Bafang
Bakonti
5236
692
993
30lowast
753
40
338
1236
Fond
janti
124
8770
2125
864
Bakambe
122
65533
105
329lowast
916
66
ND
ND
ND
Baham
Bapi
145
77531
ND
ND
ND
ND
ND
ND
189
21111
Band
jaBa
bouantou
(Batou
la)
6849
721
537
132lowast
7614
184
8418
214
Bang
angte
Batchingou
8461
726
102
11108lowast
8014
175
247
45182
NdjiptaIII
(Fop
-Tchui)
8871
807
781
13lowast
576
105lowastlowast
929
98
Foum
bot
Fossang-
chefferielowast
3228
875
7113
183lowast
7219
264lowastlowast
150
19127lowastlowastlowast
Njone
5952
881
135
1181lowast
122
41336lowastlowast
167
70419lowastlowastlowast
Kekem
Mbafam
3927
692
952
21lowast
112
436
163
849
Penk
a-Michel
Bakassa
5732
561
ND
ND
ND
ND
ND
ND
195
736
Foum
ban
Folap
ND
ND
ND
ND
ND
ND
ND
ND
ND
265
000
Kouo
ptam
oNjisseng
ND
ND
ND
ND
ND
ND
ND
ND
ND
168
530
Malantouen
Matou
pou
ND
ND
ND
ND
ND
ND
ND
ND
ND
170
1376
Massang
amMakou
opsap
ND
ND
ND
ND
ND
ND
ND
ND
ND
9959
596
931
621
667
878
5360lowast
782
109
139
2703
308
114
NDnot
done
lowastSign
ificant
(119875lt005)mdash
follo
wup
2005
comparedwith
theb
aseline
lowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2006
comparedwith
2005
follo
wup
lowastlowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2011comparedwith
2006
follo
wup
Journal of Parasitology Research 7
667
6139 114
292
42 45 89
01020304050607080
m
f pre
vale
nce
AdultsChildren
1996119899 = 931 2005 (3 months after treatment)
119899 = 878
2006 (6 months
Baseline Followup
after treatment)119899 = 782
2011 (11 monthafter treatment)
119899 = 2703
Figure 2 Comparison of mf rates among adults and children atbaseline 1996 with followup surveys in 2005 2006 and 2011 inWestRegion of Cameroon
for failure to attain optimal parasitological and entomologicalimpacts
High vector density and mf rates suggest that the forceof transmission may have been very high and most likely thereason for the results obtained [26]The present study did notconsider the standardmeasure of intensity of infection whichis related to force of infection community mf load (CMFL)This requires a calculation that involves weighing the snipand counting the microfilaria which was not done [19] Werecommend that it should be done in future studies
In Massangam Health District it is possible that high mfand nodule rates in the follow-up assessments may be dueto the ldquoforce of infectionrdquo across the neighbouring CentralRegion where peer-reviewed studies indicate considerableonchocerciasis transmission [27 28] River Nja a tributary ofRiver Noun and River Kichi a tributary of River Mbam areknown black fly breeding sites responsible for cross-bordertransmission between West and Central regions Thereforewe recommend collaboration between the regions in order tounderstand the limits of cross-border onchocerciasis affectedarea and harmonize intervention if elimination becomes thegoal in Cameroon
Another possible explanation for high mf rates couldbe related to suboptimal response to ivermectin observedin some onchocerciasis endemic areas of Ghana The adultfemale O volvulus worms were resuming microfilaria repro-duction more rapidly after ivermectin treatment than wouldnormally be expected suggesting possible development ofresistance to ivermectin [29ndash31] We recommend that thepossibility of suboptimal response to ivermectin in WestRegion be investigated
The microfilaria rate in adults and children tended tofollow the expected trend where a single annual dose ofivermectin over a number of years significantly reduced thelow mf rates that tend to persist [3] The observed patternindicated a tendency for themf rate to raise a fewmonths aftermass treatment until another dose of ivermectin is providedconfirming that microfilarial production is not cumulativelyreduced by several annual ivermectin treatments [32] Themf rate trend at three six and eleven months after mass
treatment is usually not different from the infection ratewithin the flies over a period after mass treatment withivermectin [33] Ivermectin kills existing microfilariae andtends to exert an ldquoembryostatic effectrdquo by which microfilarialproduction is suppressed over a few weeks after treatmentbut then after the mf rate begins to increase [32] Underfavourable ecological conditions interruption of onchocer-ciasis transmission with annual mass treatment may requiremany more years before it is attained
As for twice yearly treatment with ivermectin or whenit is coupled with vector control infection rate continuedto fall implying that interruption of transmission could berapidly attained [1 33 34] We recommend that West Regionof Cameroon should consider twice yearly treatment or atleast annual treatment with targeted vector control
In the present study some communities (Folap andNjisseng) in Foumban and Kouoptamo health districts hadmf rates lower than 5 in adults and 0 in children Inthese communities the Diawara et al criteria are closeto being attained and yet with low levels of infectiontransmission is much more efficient than at high levels ofinfection [35ndash37] Thus if low levels of infection are notdetected and controlled they could result in fast diseaserecrudescence Skin snip (microscopy) has low sensitivity ofless than 20 at less than 20 nodule rate and the resultsobtained may not reflect correct mf endemicity levels [38]Therefore interventions in these health districts cannot behalted as disease recrudescence could occur [29 30] Whereinterruption of transmission of onchocerciasis is the objectivewe recommend a search for affordable less intrusive rapidsensitive and highly specific diagnostic tools for low levelinfections in order to validate interruption of onchocerciasistransmission
The APOC threshold for launching mass treatment isan onchocercal nodule rate of ge20 Fondjanti community(Bandja Health District) with nodule rate of 23 and mfrate of 64 would pass for mass treatment while Njonecommunity (Foumbot Health District) with nodule rate of186 and mf rate of 419 would fail [39] Nodule rate couldalso be confounded by the presence of ganglia and Taeniasolium [40 41] The entomological results showed that therisk of contracting onchocerciasis in FoumbotHealthDistrictwas higher than in Bafang Health District confirming thereliability of mf rates compared with nodule rates With theshift from control to elimination of onchocerciasis in Africawe recommend that nodule prevalence should not be usedto determine whether an endemic area should receive masstreatment or not
Annual biting rates with the range of 28560 to 125380are some of the highest observed globally Yet infective ratein Bafang from the western part of the region was zerojustifying low mf rates (06 in children and a mean of52 in adults) The question would be whether annual masstreatment could be withdrawn without resulting in diseaserecrudescence Existing low level transmission with the highannual biting rate of 52610 could still result in onchocerciasisrecrudescence It was also evident in this study that one-month baseline entomological data was likely to miss peakbiting transmission pattern of Simulium vectors and the
8 Journal of Parasitology Research
Table3Com
parin
gmfp
revalencea
mon
gchild
renatbaselin
e(1996)and
follo
wup
in2005200
6and2011three
mon
thssix
mon
thsandele
venmon
thsrespectiv
elyafterm
asstreatment
inWestR
egion
Cameroo
n
Distric
tCom
mun
ityBa
selin
e1996
(119899=185)
Follo
wup
2005(119899=403)
Follo
wup
200
6(119899=134)
Follo
wup
2011(119899=626)
No
Exam
ined
No
positive
mf
positive
No
Exam
ined
No
positive
mf
positive
No
Exam
ined
No
positive
mf
positive
Noexam
No
positive
mf
positive
Bafang
Bakonti-B
akassa
102
13127
740
0lowast43
000
167
106
Bafang
Batchieu
704
57
40
00
Baham
Bapi
ND
ND
ND
292
69
Band
jaBa
bouantou
(Batou
la)lowast
ND
ND
ND
647
109
143
214
193
158
Bang
angte
Batchingoulowast
ND
ND
ND
241
42
152
133
211
48
Bang
angte
NdjiptaIII(Fo
p-Tchu
i)lowastND
ND
ND
632
32
50
00
250
00
FossangCh
efferie
ND
ND
ND
380
00
40
00
252
80
Foum
bot
Njone
2019
950
123
25lowast
161
63
8224
293lowastlowastlowast
Foum
bot
Kousang-Malanden
6322
349
ND
ND
ND
ND
ND
ND
ND
ND
ND
Kekem
Mbafamlowast
ND
ND
ND
580
00
330
00
200
00
Penk
a-Michel
Bakassa
ND
ND
ND
ND
ND
ND
ND
ND
ND
741
14Fo
umban
Folap
ND
ND
ND
ND
ND
ND
ND
ND
ND
108
000
Kouo
ptam
oNjisseng
ND
ND
ND
ND
ND
ND
ND
ND
ND
241
42
Massang
amMakou
opsap
ND
ND
ND
ND
ND
ND
ND
ND
ND
3221
656
12185
5429
240
317
42lowast
134
645
626
5689
NDnot
done
lowastSign
ificant
(119875lt005)mdash
follo
wup
2005
comparedwith
theb
aseline
lowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2006
comparedwith
2005
follo
wup
lowastlowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2011comparedwith
2006
follo
wup
Journal of Parasitology Research 9
Table4
Com
parin
gnod
ulep
revalencea
mon
gadu
ltsatbaselin
e(1996)and
follo
wup
in2005200
6and2011three
mon
thssix
mon
thsandele
venmon
thsrespectiv
elyafterm
asstreatment
inWestR
egion
Cameroo
n
Distric
tCom
mun
ityBa
selin
e1996
(119899=305)
Follo
wup
2005(119899=780)
Follo
wup
200
6(119899=782)
Follo
wup
2011(119899=2703)
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
Bafang
Bakassa
2716
593
139
110
79lowast
9711
113
251
2184
Bakonti
2711
407
9850
51lowast
755
67
338
36107
Fond
janti
2719
704
125
29232
Bakambe
2719
704
105
110
105lowast
9113
143
125
29232
Baham
Bapi
2915
517
ND
ND
ND
ND
ND
ND
189
1579
Band
jaBa
bouantou
(Batou
la)
2616
615
6150
82lowast
7618
237lowastlowast
8412
143
Bang
angte
Batchingou
2922
759
101
160
158lowast
8023
288lowastlowast
247
29117lowastlowastlowast
NdjiptaIII(Fo
p-Tchu
i)29
23793
7850
64lowast
578
140lowastlowast
929
98
Foum
bot
Fossang-chefferie
2824
857
7170
99lowast
7218
250lowastlowast
150
26173lowastlowastlowast
Njone
2926
897
3490
265lowast
122
37303
167
31186lowastlowastlowast
Kekem
Mbafam
2417
708
9350
54lowast
112
12107lowastlowast
163
27166
Penk
a-Michel
Bakassa
3012
400
ND
ND
ND
ND
ND
ND
195
1577
Foum
ban
Folap
ND
ND
ND
ND
ND
ND
ND
ND
ND
265
415
Kouo
ptam
oNjisseng
ND
ND
ND
ND
ND
ND
ND
ND
ND
168
636
Malantouen
Matou
pou
ND
ND
ND
ND
ND
ND
ND
ND
ND
170
953
Massang
amMakou
opsap
ND
ND
ND
ND
ND
ND
ND
ND
ND
9943
434
332
220
663
780
7495lowast
782
145
185lowastlowast
2828
341
121lowastlowastlowast
NDnot
done
lowastSign
ificant
(119875lt005)mdash
follo
wup
2005
comparedwith
theb
aseline
lowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2006
comparedwith
2005
follo
wup
lowastlowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2011comparedwith
2006
follo
wup
10 Journal of Parasitology Research
Table 5 Comparing baseline entomological data of 1996 at two fly collection sites and three during 2011
Monthyear of black fly collection Baseline May 1996 Followup 2011Black fly collection sites Bafang (Basseu) Foumbot (Maka) Bafang Foumbot MassangamNumber of Simulium caught 5 166 5261 2856 12538Number of Simulium dissected 5 142 5261 2856 12138Number of parous flies 1 97 1502 1028 2845Parous rate () 20 683 285 36 234Number of Simulium flies infected (L1 L2 L3] 1 12 3 9 19Infection rate () 2000 845 020 088 067Number of Simulium flies infective L3 larval stage in the head 20 2 0 2 5Infective rate () 200 211 000 019 018Monthly biting rate per person 750 166000 na na naMonthly transmission potentiallowast 150 21040 na na naAnnual biting rate per person Na na 52610 28560 125380Annual transmission potential Na na 0 70 310
0
500
1000
1500
2000
2500
3000
3500
4000
No
of fl
ies c
olle
cted
BafangFoumbotMakouopsap
MarApr2011 2012
May Jun Jul AugSeptOctNovDec Jan Feb
Figure 3 Monthly seasonal biting of Simulium flies at 3 fly catchingsites in West Region
calculation ofATPTherefore collection of entomological dataover several months is required as reflected in the follow-up study The information on peak biting and transmissionpatterns could effectively be utilized for ivermectin treatmentfor maximum impact on transmission especially where theforce of transmission is considerably high if elimination ofonchocerciasis is the goal In the follow-up survey it is onlyat Bafang fly collection site that the entomological criterionfor interruption of transmission was met with an ATP of zero[42]
The present study however did not perform moleculartesting in order to determine if the L3 larvae wereO volvulusor another (animal) Onchocerca species Based on humanmf prevalence in skin and infections in children we thinkthat there is likelihood that some of the larvae observedin vectors were O volvulus However a study conducted inNorth Region of Cameroon during the 1990s showed that
33 of infective larvae in S damnosum were O volvuluswhereas 65 were O ochengi and 2 were O ramachandrini[43] It is until such a study is conducted in West Region ofCameroon that we will know the extent to which O ochengiis responsible for a significant proportion of infected flies thatcould confound the infection rate there
Our findings reflecting an observation period of 15 yearsshowed that annual mass treatment with ivermectin may notinterrupt the transmission of onchocerciasis in all differentecological zones of West Region Therefore the intensive useof ivermectin is recommended if interruption of transmissionof onchocerciasis is to be attained [1]
5 Conclusion
Annual mass treatment with ivermectin through commu-nity-directed treatment was preferred as a good and lessexpensive method for controlling onchocerciasis in endemicAfrican countries with assistance from the African Pro-gramme for Onchocerciasis Control The studies in MaliSenegal and Nigeria have shown that an annual dose ofivermectin had interrupted transmission of the disease andall interventions could be halted without the risk of diseaserecrudescence However an annual dose of ivermectin hasnot interrupted transmission after 15 years of mass treatmentin some areas in West Region of Cameroon just like inNorth region [8] It has also been less effective in someonchocerciasis endemic areas in Ghana The present paperagain highlights the fact that for interruption of onchocer-ciasis transmission feasible and different but complementarystrategic options should be adopted as elimination becomesthe goal in Africa
Acknowledgments
The investigators would like to acknowledge the staff ofMinistry of Health at the national regional and healthdistrict levels in West Region along with Carter CenterCameroon Office for mobilizing and educating selected
Journal of Parasitology Research 11
communities and providing policy and administrative sup-port The involvement of community members in selectedcommunities in mf and nodule assessments and Simulium flycollection is highly appreciated The Carter Center the LionsClubs International Foundation (LCIF) and the African Pro-gramme for onchocerciasis Control (APOC) which fundedthe CDTI activities and the surveys are also highly appreci-ated
References
[1] E W Cupp and M S Cupp ldquoShort report impact of iver-mectin community-level treatments on elimination of adultOnchocerca volvulus when individuals receive multiple treat-ments per yearrdquoThe American Journal of Tropical Medicine andHygiene vol 73 no 6 pp 1159ndash1161 2005
[2] H R Taylor M Pacque B Munoz and B M Greene ldquoImpactof mass treatment of onchocerciasis with ivermectin on thetransmission of infectionrdquo Science vol 250 no 4977 pp 116ndash118 1990
[3] G J J M Borsboom B A Boatin N J D Nagelkerkeet al ldquoImpact of ivermectin on onchocerciasis transmissionassessing the empirical evidence that repeated ivermectin masstreatmentsmay lead to eliminationeradication inWest-AfricardquoFilaria Journal vol 2 article 8 2003
[4] A D Hopkins ldquoIvermectin and onchocerciasis is it all solvedrdquoEye vol 19 no 10 pp 1057ndash1066 2005
[5] L Yameogo ldquoSpecial intervention zonesrdquo Annals of TropicalMedicine and Parasitology vol 102 supplement 1 pp 23ndash242008
[6] D H Molyneux and M N Malecela ldquoNeglected tropicaldiseases and themillennium development goals why the ldquootherdiseasesrdquo matter reality versus rhetoricrdquo Parasites amp Vectorsvol 4 2011
[7] WHOReportAcceleratingWorkToOvercome theGlobal Impactof Neglected Tropical Disease A Roadmap For Implementationvol 1211WorldHealthOrganization 20AvenueAppia GenevaSwitzerland 2012
[8] M N Katabarwa A Eyamba P Nwane et al ldquoSeventeenyears of annual distribution of ivermectin has not interruptedonchocerciasis transmission in North Region Cameroonrdquo TheAmerican Journal of Tropical Medicine and Hygiene vol 85 no6 pp 1041ndash1049 2011
[9] B A Boatin and F O Richards ldquoControl of onchocerciasisrdquoAdvances in Parasitology vol 61 pp 349ndash394 2006
[10] D R Hopkins F O Richards and M Katabarwa ldquoWhitheronchocerciasis control in Africardquo American Journal of TropicalMedicine and Hygiene vol 72 no 1 pp 1ndash2 2005
[11] L Diawara M O Traore A Badji et al ldquoFeasibilityof onchocerciasis elimination with ivermectin treatment inendemic foci in Africa first evidence from studies in Mali andSenegalrdquo PLoS Neglected Tropical Diseases vol 3 no 7 articlee497 2009
[12] F O Richards E S Miri M Katabarwa et al ldquoThe carter cen-terrsquos assistance to river blindness control programs establish-ing treatment objectives and goals for monitoring ivermectindelivery systems on two continentsrdquo The American Journal ofTropical Medicine and Hygiene vol 65 no 2 pp 108ndash114 2001
[13] P Salant and D A Dilman How to Conduct Your Own SurveyJohn Wiley amp Sons 1994
[14] M N Katabarwa P Habomugisha and F O Richards ldquoImple-menting community-directed treatmentwith ivermectin for the
control of onchocerciasis in Uganda (1997-2000) an evalua-tionrdquo Annals of Tropical Medicine and Parasitology vol 96 no1 pp 61ndash73 2002
[15] E C Emukah U Enyinnaya N S Olaniran et al ldquoFactorsaffecting the attrition of community-directed distributors ofivermectin in an onchocerciasis-control programme in the Imoand Abia states of south-eastern Nigeriardquo Annals of TropicalMedicine and Parasitology vol 102 no 1 pp 45ndash51 2008
[16] A Prost and J Prodrsquohon ldquoLe diagnostique parasitologique delrsquoonchocercose revue critique des methods en usagerdquoMedicineTropicale vol 38 pp 519ndash532 1978
[17] H Schulz Key ldquoA simple technique to assess the total number ofOnchocerca volvulusmicrofilariae in skin snipsrdquo Tropenmedizinund Parasitologie vol 29 no 1 pp 51ndash54 1978
[18] WHO Report ldquoOnchocerciasis and its control Report of aWHO Expert Committee on Onchocerciasis Controlrdquo TechRep 852 Geneva Switzerland 1995
[19] WHO Report Strategies For Ivermectin Distribution ThroughPrimaryHealth Care SystemWHOPHL91 24WHOGenevaSwitzerland 1991
[20] E J Albiez D W Buttner and B O L Duke ldquoDiagnosisand extirpation of nodules in human onchocerciasisrdquo TropicalMedicine and Parasitology vol 39 no 4 pp 331ndash346 1988
[21] P Ngoumou J F Walsh and J M Mace ldquoA rapid mappingtechnique for the prevalence and distribution of onchocerciasisa Cameroon case studyrdquo Annals of Tropical Medicine andParasitology vol 88 no 5 pp 463ndash474 1994
[22] M Katabarwa A W Onapa and B Nakileza ldquoRapid epidemi-ological mapping of onchocerciasis in areas of uganda whereSimulium neavei SL is the vectorrdquo East African Medical Journalvol 76 no 8 pp 440ndash446 1999
[23] J F Walsh J B Davies R Le Berre and R Garms ldquoStandard-ization of criteria for assessing the effect of Simulium control inonchocerciasis control programmesrdquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 72 no 6 pp 675ndash676 1978
[24] J B Davies ldquoA rapid staining and clearing technique for detect-ing filarial larvae in alcohol-preserved vectorsrdquo Transactions ofthe Royal Society of Tropical Medicine and Hygiene vol 89 no3 p 280 1995
[25] M Katabarwa P Habomugisha A Eyamba S Agunyo andC Mentou ldquoMonitoring ivermectin distributors involved inintegrated health care services through community-directedinterventionsmdasha comparison of Cameroon and Uganda expe-riences over a period of three years (2004ndash2006)rdquo TropicalMedicine and International Health vol 15 no 2 pp 216ndash2232010
[26] J Remme O Ba K Y Dadzie and M Karam ldquoA force-of-infection model for onchocerciasis and its applications inthe epidemiological evaluation of the onchocerciasis controlprogramme in the volta river basin areardquo Bulletin of the WorldHealth Organization vol 64 no 5 pp 667ndash681 1986
[27] P Barbazan H Escaffre R Mbentengam and M BoussinesqldquoEntomologic study on the transmission of onchocerciasis ina forest-savanna transition area of Cameroonrdquo Bulletin de laSociete de Pathologie Exotique vol 91 no 2 pp 178ndash182 1998
[28] E Cadot P Barbazan andM Boussinesq ldquoGeographical deter-minants of onchocerciasis transmission in a forestsavannahtransition zone two villages of the mbam focusrdquo Sante vol 8no 6 pp 429ndash435 1998
[29] K Awadzi S K Attah E T Addy et al ldquoThirty-monthfollow-up of sub-optimal responders to multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in Ghanardquo
12 Journal of Parasitology Research
Annals of Tropical Medicine and Parasitology vol 98 no 4 pp359ndash370 2004
[30] K Awadzi D A Boakye G Edwards et al ldquoAn investigationof persistent microfilaridermias despite multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in GhanardquoAnnals of Tropical Medicine and Parasitology vol 98 no 3 pp231ndash249 2004
[31] M Y Osei-Atweneboana J K Eng D A Boakye J OGyapong and R K Prichard ldquoPrevalence and intensity ofOnchocerca volvulus infection and efficacy of ivermectin inendemic communities in Ghana a two-phase epidemiologicalstudyrdquoThe Lancet vol 369 no 9578 pp 2021ndash2029 2007
[32] C Bottomley V Isham R C Collins and M G BasanezldquoRates of microfilarial production by Onchocerca volvulus arenot cumulatively reduced by multiple ivermectin treatmentsrdquoParasitology vol 135 no 13 pp 1571ndash1581 2008
[33] R Garms T L Lakwo R Ndyomugyenyi et al ldquoThe elimina-tion of the vector Simulium neavei from the Itwara onchocerci-asis focus in Uganda by ground larvicidingrdquo Acta Tropica vol111 no 3 pp 203ndash210 2009
[34] R Ndyomugyenyi E Tukesiga D W Buttner and R GarmsldquoThe impact of ivermectin treatment alone and when inparallel with Simulium neavei elimination on onchocerciasis inUgandardquo Tropical Medicine and International Health vol 9 no8 pp 882ndash886 2004
[35] H P Duerr and M Eichner ldquoEpidemiology and control ofonchocerciasis the threshold biting rate of savannah onchocer-ciasis in Africardquo International Journal for Parasitology vol 40no 6 pp 641ndash650 2010
[36] K Dietz ldquoDensity-dependence in parasite transmissiondynamicsrdquo Parasitology Today vol 4 no 4 pp 91ndash97 1988
[37] M G Basanez J H F Remme E S Alley et al ldquoDensity-dependent processes in the transmission of human onchocerci-asis relationship between the numbers ofmicrofilariae ingestedand successful larval development in the simuliid vectorrdquoParasitology vol 110 no 4 pp 409ndash427 1995
[38] B A Boatin L Toe E S Alley N J D Nagelkerke GBorsboom and J D F Habbema ldquoDetection of Onchocercavolvulus infection in lowprevalence areas a comparison of threediagnostic methodsrdquo Parasitology vol 125 no 6 pp 545ndash5522002
[39] M Noma B E B Nwoke I Nutall et al ldquoRapid epidemio-logical mapping of onchocerciasis (REMO) its application bythe African programme for onchocerciasis control (APOC)rdquoAnnals of Tropical Medicine and Parasitology vol 96 supple-ment 1 pp S29ndashS39 2002
[40] G Fobi J R M Mbina G Ozoh et al ldquoOnchocerciasis inthe area of Lastourville Gabon Clinical and entomologicalaspectsrdquo Bulletin de la Societe de Pathologie Exotique vol 99no 4 pp 269ndash271 2006
[41] M N Katabarwa A Eyamba M Chouaibou et al ldquoDoesonchocerciasis transmission take place in hypoendemic areasa study from theNorth Region of CameroonrdquoTropicalMedicineand International Health vol 15 no 5 pp 645ndash652 2010
[42] WHO Report Certification of Elimination of Human Onchocer-ciasis Criteria and Procedures Criteria For Certification of Inter-ruption of TransmissionElimination of Human OnchocerciasisWorld Health Organization Geneva Switzerland 2001
[43] R Seidenfaden A Fischer I Bonow D Ekale V Tanya andA Renz ldquoCombined benefits of annual mass treatment withivermectin and cattle zooprophylaxis on the severity of humanonchocerciasis in northern Cameroonrdquo Tropical Medicine andInternational Health vol 6 no 9 pp 715ndash725 2001
potential (ATP) was calculated as the sum of the individualmonthly transmission potentials (MTPs) over the period of ayear [23]
Data Analysis Parasitological data from adults and childrenas well as entomological data were entered and analysedgraphically in Microsoft Excel and Epi Info CDC AtlantaGA USA for chi square test of independence The ento-mological data was analysed and graphically illustrated inMicrosoft Excel
Ethical Approval All the surveys from the baseline to thefollow-up studies were approved by the Ministry of PublicHealth of Cameroon and the National Ethical Committeein Yaounde In addition the Emory University InstitutionalReview Board (eIRB-11 438) approved and considered themas nonresearch but routine program evaluation The fol-lowup of 2011 was also conducted under the auspices ofWorldHealth Organisation All assessed individuals had the libertyof opting out of assessments if they wished so without anyrepercussions
3 Results
31 Microfilaria (mf) and Nodule Prevalences Among adultsthe mf rate reduced by about 91 from baseline level of667 (range 531 to 881) in 1996 to 60 (range 14 to183 119875 lt 00001) in 2005 three months after ivermectintreatment However mf rate increased in 2006 six monthsafter ivermectin treatment to 139 (range 21 to 336)although it was not statistically different from 2005 mf rate119875 lt 0053 The decrease of mf rate 139 in 2006 to114 (range 0 to 596) in 2011 was also not significant(119875 lt 0053) (Table 2 and Figure 2) Only one communityhad 0 mf rate while six communities had mf rates above10 and two above 40 after 15 years of annual masstreatment Persistent high mf rates were observed in com-munities of Babouantou (214) in Bandja health districtNjone (419) in Foumbot health district and Makouopsap(596) in Massangam health district However there werecommunities (Bakonti in Bafang Health District Folap inFoumban Mbafam in Kekem and Njisseng in Kouptamo)which registered mf rates below 5 in adults
In children overall baselinemf rate of 292 (range 127to 518) reduced to 42 (range 0 to 250) in 2005 withan 856 reduction 119875 lt 00001 (Table 3 and Figure 2)However there was no significant difference between mf rate42 in 2005 and 45 in 2006 three months and six monthsrespectively after mass treatmentThere results for 2006 werealso not significantly different from mf rate 89 obtainedin 2011 eleven months after treatment (Table 3 and Figure 2)There were children in 2 (133) communities with mf ratesabove 20 (Njone 252 and Makouopsap 656) EvenBabouantou with mf rate of 158 was considered high fora program with 15 years of annual treatment In Ndjipta III ofBangangte Health District Folap of Foumban and Mbafamof Kekem mf rates among children were 06 or less
The overall baseline nodule rate in adults of 663 (range40 to 897) declined to 95 (range 400ndash897) 119875 lt00001 in the 2005This represents a decline of 856Then itincreased to 185 (range 67ndash303) in 2006 and declinedto 121 (range 15ndash434) in 2011 (Table 4) There were9 communities out of 16 with nodule prevalence of at least10 Of particular interest are persistent high nodule ratesin Bakambe (232) and Fondjanti (232) communities ofBafang Health District Fossang-chefferie (173) and Njone(186) in Foumbot health district andMakouopsap (434)in Massangam Health District
32 Entomology Baseline monthly transmission potentialswere 15 in Bafang and 2104 in Foumbot (Table 5) In thefollow-up assessment the infection rates were 02 in BafangHealth District 088 in Foumbot and 067 in MassangamThe infective rates were 0 in Bafang Health District 019in Foumbot and 018 in Massangam Annual biting rateswere 52610 in Bafang 28560 in Foumbot and 125360 inMakouopsap while annual transmission potentials were 070 and 310 respectively Biting was generally throughout theyear although the main peak biting period in Makouopsapwas observed from January to May (Figure 3)
4 Discussion
Annual mass treatment with ivermectin for 15 years hadconsiderably reduced microfilaria and nodule prevalence inall the sentinel communities of West Region of CameroonElimination is considered attained when the microfilariaprevalence in skin snips is less than 5 in sampled communi-ties in less than 1 in 90of sampled communities andwhenentomological criteria of less than 05 infected flies1000 areattained [11] Among adults Foumban Health District wasclose to the epidemiological criterion while Bafang HealthDistrict was not very far from the entomological criterionwith the ATP of 0 mf rate among children in Foumbanand Kekem health districts was zero indicating no recentinfection an indication that interruption of transmissionmay be attained However the mf rates in Baham BanjaBangangte Foumbot andMassangam health districts amongadults and children were still uncomfortably high showingcontinuing transmission In adults nodule rates near orabove the threshold 20 for the mass treatment in somecommunities were of a major concern The infective rateof 018 to 019 and ATP of 70 to 300 confirmed continuingtransmission
One possible explanation for high mf rates in childrenand adults could have been low treatment coverage Howeverthe methodology for validating UTG treatment coveragefollowed standard statistical methods for selecting sampledcommunities and the interviewees This methodology hadbeen tested and used to validate performance of CDTI inCameroon and in other onchocerciasis endemic countries[14 15 25]TheUTG treatment coverage results were also cor-roborated by independent monitoring results in unpublishedreports supported by APOC Therefore there is no reason tobelieve that UTG treatment coverage was low and responsible
6 Journal of Parasitology Research
Table2Com
parin
gmfp
revalencea
mon
gadultsatbaselin
e(1996)a
ndfollo
wup
in2005200
6and2011three
mon
thssix
mon
thsandele
venmon
thsrespectiv
elyafte
rmasstreatment
inWestR
egion
Cameroo
n
Distric
tCom
mun
ityBa
selin
e1996
(119899=931)
Follo
wup
2005(119899=878)
Follo
wup
200
6(119899=782)
Follo
wup
2011(119899=2703)
No
exam
ined
No
positive
mf
positive
No
exam
ined
No
positive
mf
positive
No
exam
ined
No
positive
mf
positive
No
exam
ined
No
positive
mf
positive
Bakassa
6136
590
140
214lowast
972
21
251
1456
Bafang
Bakonti
5236
692
993
30lowast
753
40
338
1236
Fond
janti
124
8770
2125
864
Bakambe
122
65533
105
329lowast
916
66
ND
ND
ND
Baham
Bapi
145
77531
ND
ND
ND
ND
ND
ND
189
21111
Band
jaBa
bouantou
(Batou
la)
6849
721
537
132lowast
7614
184
8418
214
Bang
angte
Batchingou
8461
726
102
11108lowast
8014
175
247
45182
NdjiptaIII
(Fop
-Tchui)
8871
807
781
13lowast
576
105lowastlowast
929
98
Foum
bot
Fossang-
chefferielowast
3228
875
7113
183lowast
7219
264lowastlowast
150
19127lowastlowastlowast
Njone
5952
881
135
1181lowast
122
41336lowastlowast
167
70419lowastlowastlowast
Kekem
Mbafam
3927
692
952
21lowast
112
436
163
849
Penk
a-Michel
Bakassa
5732
561
ND
ND
ND
ND
ND
ND
195
736
Foum
ban
Folap
ND
ND
ND
ND
ND
ND
ND
ND
ND
265
000
Kouo
ptam
oNjisseng
ND
ND
ND
ND
ND
ND
ND
ND
ND
168
530
Malantouen
Matou
pou
ND
ND
ND
ND
ND
ND
ND
ND
ND
170
1376
Massang
amMakou
opsap
ND
ND
ND
ND
ND
ND
ND
ND
ND
9959
596
931
621
667
878
5360lowast
782
109
139
2703
308
114
NDnot
done
lowastSign
ificant
(119875lt005)mdash
follo
wup
2005
comparedwith
theb
aseline
lowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2006
comparedwith
2005
follo
wup
lowastlowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2011comparedwith
2006
follo
wup
Journal of Parasitology Research 7
667
6139 114
292
42 45 89
01020304050607080
m
f pre
vale
nce
AdultsChildren
1996119899 = 931 2005 (3 months after treatment)
119899 = 878
2006 (6 months
Baseline Followup
after treatment)119899 = 782
2011 (11 monthafter treatment)
119899 = 2703
Figure 2 Comparison of mf rates among adults and children atbaseline 1996 with followup surveys in 2005 2006 and 2011 inWestRegion of Cameroon
for failure to attain optimal parasitological and entomologicalimpacts
High vector density and mf rates suggest that the forceof transmission may have been very high and most likely thereason for the results obtained [26]The present study did notconsider the standardmeasure of intensity of infection whichis related to force of infection community mf load (CMFL)This requires a calculation that involves weighing the snipand counting the microfilaria which was not done [19] Werecommend that it should be done in future studies
In Massangam Health District it is possible that high mfand nodule rates in the follow-up assessments may be dueto the ldquoforce of infectionrdquo across the neighbouring CentralRegion where peer-reviewed studies indicate considerableonchocerciasis transmission [27 28] River Nja a tributary ofRiver Noun and River Kichi a tributary of River Mbam areknown black fly breeding sites responsible for cross-bordertransmission between West and Central regions Thereforewe recommend collaboration between the regions in order tounderstand the limits of cross-border onchocerciasis affectedarea and harmonize intervention if elimination becomes thegoal in Cameroon
Another possible explanation for high mf rates couldbe related to suboptimal response to ivermectin observedin some onchocerciasis endemic areas of Ghana The adultfemale O volvulus worms were resuming microfilaria repro-duction more rapidly after ivermectin treatment than wouldnormally be expected suggesting possible development ofresistance to ivermectin [29ndash31] We recommend that thepossibility of suboptimal response to ivermectin in WestRegion be investigated
The microfilaria rate in adults and children tended tofollow the expected trend where a single annual dose ofivermectin over a number of years significantly reduced thelow mf rates that tend to persist [3] The observed patternindicated a tendency for themf rate to raise a fewmonths aftermass treatment until another dose of ivermectin is providedconfirming that microfilarial production is not cumulativelyreduced by several annual ivermectin treatments [32] Themf rate trend at three six and eleven months after mass
treatment is usually not different from the infection ratewithin the flies over a period after mass treatment withivermectin [33] Ivermectin kills existing microfilariae andtends to exert an ldquoembryostatic effectrdquo by which microfilarialproduction is suppressed over a few weeks after treatmentbut then after the mf rate begins to increase [32] Underfavourable ecological conditions interruption of onchocer-ciasis transmission with annual mass treatment may requiremany more years before it is attained
As for twice yearly treatment with ivermectin or whenit is coupled with vector control infection rate continuedto fall implying that interruption of transmission could berapidly attained [1 33 34] We recommend that West Regionof Cameroon should consider twice yearly treatment or atleast annual treatment with targeted vector control
In the present study some communities (Folap andNjisseng) in Foumban and Kouoptamo health districts hadmf rates lower than 5 in adults and 0 in children Inthese communities the Diawara et al criteria are closeto being attained and yet with low levels of infectiontransmission is much more efficient than at high levels ofinfection [35ndash37] Thus if low levels of infection are notdetected and controlled they could result in fast diseaserecrudescence Skin snip (microscopy) has low sensitivity ofless than 20 at less than 20 nodule rate and the resultsobtained may not reflect correct mf endemicity levels [38]Therefore interventions in these health districts cannot behalted as disease recrudescence could occur [29 30] Whereinterruption of transmission of onchocerciasis is the objectivewe recommend a search for affordable less intrusive rapidsensitive and highly specific diagnostic tools for low levelinfections in order to validate interruption of onchocerciasistransmission
The APOC threshold for launching mass treatment isan onchocercal nodule rate of ge20 Fondjanti community(Bandja Health District) with nodule rate of 23 and mfrate of 64 would pass for mass treatment while Njonecommunity (Foumbot Health District) with nodule rate of186 and mf rate of 419 would fail [39] Nodule rate couldalso be confounded by the presence of ganglia and Taeniasolium [40 41] The entomological results showed that therisk of contracting onchocerciasis in FoumbotHealthDistrictwas higher than in Bafang Health District confirming thereliability of mf rates compared with nodule rates With theshift from control to elimination of onchocerciasis in Africawe recommend that nodule prevalence should not be usedto determine whether an endemic area should receive masstreatment or not
Annual biting rates with the range of 28560 to 125380are some of the highest observed globally Yet infective ratein Bafang from the western part of the region was zerojustifying low mf rates (06 in children and a mean of52 in adults) The question would be whether annual masstreatment could be withdrawn without resulting in diseaserecrudescence Existing low level transmission with the highannual biting rate of 52610 could still result in onchocerciasisrecrudescence It was also evident in this study that one-month baseline entomological data was likely to miss peakbiting transmission pattern of Simulium vectors and the
8 Journal of Parasitology Research
Table3Com
parin
gmfp
revalencea
mon
gchild
renatbaselin
e(1996)and
follo
wup
in2005200
6and2011three
mon
thssix
mon
thsandele
venmon
thsrespectiv
elyafterm
asstreatment
inWestR
egion
Cameroo
n
Distric
tCom
mun
ityBa
selin
e1996
(119899=185)
Follo
wup
2005(119899=403)
Follo
wup
200
6(119899=134)
Follo
wup
2011(119899=626)
No
Exam
ined
No
positive
mf
positive
No
Exam
ined
No
positive
mf
positive
No
Exam
ined
No
positive
mf
positive
Noexam
No
positive
mf
positive
Bafang
Bakonti-B
akassa
102
13127
740
0lowast43
000
167
106
Bafang
Batchieu
704
57
40
00
Baham
Bapi
ND
ND
ND
292
69
Band
jaBa
bouantou
(Batou
la)lowast
ND
ND
ND
647
109
143
214
193
158
Bang
angte
Batchingoulowast
ND
ND
ND
241
42
152
133
211
48
Bang
angte
NdjiptaIII(Fo
p-Tchu
i)lowastND
ND
ND
632
32
50
00
250
00
FossangCh
efferie
ND
ND
ND
380
00
40
00
252
80
Foum
bot
Njone
2019
950
123
25lowast
161
63
8224
293lowastlowastlowast
Foum
bot
Kousang-Malanden
6322
349
ND
ND
ND
ND
ND
ND
ND
ND
ND
Kekem
Mbafamlowast
ND
ND
ND
580
00
330
00
200
00
Penk
a-Michel
Bakassa
ND
ND
ND
ND
ND
ND
ND
ND
ND
741
14Fo
umban
Folap
ND
ND
ND
ND
ND
ND
ND
ND
ND
108
000
Kouo
ptam
oNjisseng
ND
ND
ND
ND
ND
ND
ND
ND
ND
241
42
Massang
amMakou
opsap
ND
ND
ND
ND
ND
ND
ND
ND
ND
3221
656
12185
5429
240
317
42lowast
134
645
626
5689
NDnot
done
lowastSign
ificant
(119875lt005)mdash
follo
wup
2005
comparedwith
theb
aseline
lowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2006
comparedwith
2005
follo
wup
lowastlowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2011comparedwith
2006
follo
wup
Journal of Parasitology Research 9
Table4
Com
parin
gnod
ulep
revalencea
mon
gadu
ltsatbaselin
e(1996)and
follo
wup
in2005200
6and2011three
mon
thssix
mon
thsandele
venmon
thsrespectiv
elyafterm
asstreatment
inWestR
egion
Cameroo
n
Distric
tCom
mun
ityBa
selin
e1996
(119899=305)
Follo
wup
2005(119899=780)
Follo
wup
200
6(119899=782)
Follo
wup
2011(119899=2703)
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
Bafang
Bakassa
2716
593
139
110
79lowast
9711
113
251
2184
Bakonti
2711
407
9850
51lowast
755
67
338
36107
Fond
janti
2719
704
125
29232
Bakambe
2719
704
105
110
105lowast
9113
143
125
29232
Baham
Bapi
2915
517
ND
ND
ND
ND
ND
ND
189
1579
Band
jaBa
bouantou
(Batou
la)
2616
615
6150
82lowast
7618
237lowastlowast
8412
143
Bang
angte
Batchingou
2922
759
101
160
158lowast
8023
288lowastlowast
247
29117lowastlowastlowast
NdjiptaIII(Fo
p-Tchu
i)29
23793
7850
64lowast
578
140lowastlowast
929
98
Foum
bot
Fossang-chefferie
2824
857
7170
99lowast
7218
250lowastlowast
150
26173lowastlowastlowast
Njone
2926
897
3490
265lowast
122
37303
167
31186lowastlowastlowast
Kekem
Mbafam
2417
708
9350
54lowast
112
12107lowastlowast
163
27166
Penk
a-Michel
Bakassa
3012
400
ND
ND
ND
ND
ND
ND
195
1577
Foum
ban
Folap
ND
ND
ND
ND
ND
ND
ND
ND
ND
265
415
Kouo
ptam
oNjisseng
ND
ND
ND
ND
ND
ND
ND
ND
ND
168
636
Malantouen
Matou
pou
ND
ND
ND
ND
ND
ND
ND
ND
ND
170
953
Massang
amMakou
opsap
ND
ND
ND
ND
ND
ND
ND
ND
ND
9943
434
332
220
663
780
7495lowast
782
145
185lowastlowast
2828
341
121lowastlowastlowast
NDnot
done
lowastSign
ificant
(119875lt005)mdash
follo
wup
2005
comparedwith
theb
aseline
lowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2006
comparedwith
2005
follo
wup
lowastlowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2011comparedwith
2006
follo
wup
10 Journal of Parasitology Research
Table 5 Comparing baseline entomological data of 1996 at two fly collection sites and three during 2011
Monthyear of black fly collection Baseline May 1996 Followup 2011Black fly collection sites Bafang (Basseu) Foumbot (Maka) Bafang Foumbot MassangamNumber of Simulium caught 5 166 5261 2856 12538Number of Simulium dissected 5 142 5261 2856 12138Number of parous flies 1 97 1502 1028 2845Parous rate () 20 683 285 36 234Number of Simulium flies infected (L1 L2 L3] 1 12 3 9 19Infection rate () 2000 845 020 088 067Number of Simulium flies infective L3 larval stage in the head 20 2 0 2 5Infective rate () 200 211 000 019 018Monthly biting rate per person 750 166000 na na naMonthly transmission potentiallowast 150 21040 na na naAnnual biting rate per person Na na 52610 28560 125380Annual transmission potential Na na 0 70 310
0
500
1000
1500
2000
2500
3000
3500
4000
No
of fl
ies c
olle
cted
BafangFoumbotMakouopsap
MarApr2011 2012
May Jun Jul AugSeptOctNovDec Jan Feb
Figure 3 Monthly seasonal biting of Simulium flies at 3 fly catchingsites in West Region
calculation ofATPTherefore collection of entomological dataover several months is required as reflected in the follow-up study The information on peak biting and transmissionpatterns could effectively be utilized for ivermectin treatmentfor maximum impact on transmission especially where theforce of transmission is considerably high if elimination ofonchocerciasis is the goal In the follow-up survey it is onlyat Bafang fly collection site that the entomological criterionfor interruption of transmission was met with an ATP of zero[42]
The present study however did not perform moleculartesting in order to determine if the L3 larvae wereO volvulusor another (animal) Onchocerca species Based on humanmf prevalence in skin and infections in children we thinkthat there is likelihood that some of the larvae observedin vectors were O volvulus However a study conducted inNorth Region of Cameroon during the 1990s showed that
33 of infective larvae in S damnosum were O volvuluswhereas 65 were O ochengi and 2 were O ramachandrini[43] It is until such a study is conducted in West Region ofCameroon that we will know the extent to which O ochengiis responsible for a significant proportion of infected flies thatcould confound the infection rate there
Our findings reflecting an observation period of 15 yearsshowed that annual mass treatment with ivermectin may notinterrupt the transmission of onchocerciasis in all differentecological zones of West Region Therefore the intensive useof ivermectin is recommended if interruption of transmissionof onchocerciasis is to be attained [1]
5 Conclusion
Annual mass treatment with ivermectin through commu-nity-directed treatment was preferred as a good and lessexpensive method for controlling onchocerciasis in endemicAfrican countries with assistance from the African Pro-gramme for Onchocerciasis Control The studies in MaliSenegal and Nigeria have shown that an annual dose ofivermectin had interrupted transmission of the disease andall interventions could be halted without the risk of diseaserecrudescence However an annual dose of ivermectin hasnot interrupted transmission after 15 years of mass treatmentin some areas in West Region of Cameroon just like inNorth region [8] It has also been less effective in someonchocerciasis endemic areas in Ghana The present paperagain highlights the fact that for interruption of onchocer-ciasis transmission feasible and different but complementarystrategic options should be adopted as elimination becomesthe goal in Africa
Acknowledgments
The investigators would like to acknowledge the staff ofMinistry of Health at the national regional and healthdistrict levels in West Region along with Carter CenterCameroon Office for mobilizing and educating selected
Journal of Parasitology Research 11
communities and providing policy and administrative sup-port The involvement of community members in selectedcommunities in mf and nodule assessments and Simulium flycollection is highly appreciated The Carter Center the LionsClubs International Foundation (LCIF) and the African Pro-gramme for onchocerciasis Control (APOC) which fundedthe CDTI activities and the surveys are also highly appreci-ated
References
[1] E W Cupp and M S Cupp ldquoShort report impact of iver-mectin community-level treatments on elimination of adultOnchocerca volvulus when individuals receive multiple treat-ments per yearrdquoThe American Journal of Tropical Medicine andHygiene vol 73 no 6 pp 1159ndash1161 2005
[2] H R Taylor M Pacque B Munoz and B M Greene ldquoImpactof mass treatment of onchocerciasis with ivermectin on thetransmission of infectionrdquo Science vol 250 no 4977 pp 116ndash118 1990
[3] G J J M Borsboom B A Boatin N J D Nagelkerkeet al ldquoImpact of ivermectin on onchocerciasis transmissionassessing the empirical evidence that repeated ivermectin masstreatmentsmay lead to eliminationeradication inWest-AfricardquoFilaria Journal vol 2 article 8 2003
[4] A D Hopkins ldquoIvermectin and onchocerciasis is it all solvedrdquoEye vol 19 no 10 pp 1057ndash1066 2005
[5] L Yameogo ldquoSpecial intervention zonesrdquo Annals of TropicalMedicine and Parasitology vol 102 supplement 1 pp 23ndash242008
[6] D H Molyneux and M N Malecela ldquoNeglected tropicaldiseases and themillennium development goals why the ldquootherdiseasesrdquo matter reality versus rhetoricrdquo Parasites amp Vectorsvol 4 2011
[7] WHOReportAcceleratingWorkToOvercome theGlobal Impactof Neglected Tropical Disease A Roadmap For Implementationvol 1211WorldHealthOrganization 20AvenueAppia GenevaSwitzerland 2012
[8] M N Katabarwa A Eyamba P Nwane et al ldquoSeventeenyears of annual distribution of ivermectin has not interruptedonchocerciasis transmission in North Region Cameroonrdquo TheAmerican Journal of Tropical Medicine and Hygiene vol 85 no6 pp 1041ndash1049 2011
[9] B A Boatin and F O Richards ldquoControl of onchocerciasisrdquoAdvances in Parasitology vol 61 pp 349ndash394 2006
[10] D R Hopkins F O Richards and M Katabarwa ldquoWhitheronchocerciasis control in Africardquo American Journal of TropicalMedicine and Hygiene vol 72 no 1 pp 1ndash2 2005
[11] L Diawara M O Traore A Badji et al ldquoFeasibilityof onchocerciasis elimination with ivermectin treatment inendemic foci in Africa first evidence from studies in Mali andSenegalrdquo PLoS Neglected Tropical Diseases vol 3 no 7 articlee497 2009
[12] F O Richards E S Miri M Katabarwa et al ldquoThe carter cen-terrsquos assistance to river blindness control programs establish-ing treatment objectives and goals for monitoring ivermectindelivery systems on two continentsrdquo The American Journal ofTropical Medicine and Hygiene vol 65 no 2 pp 108ndash114 2001
[13] P Salant and D A Dilman How to Conduct Your Own SurveyJohn Wiley amp Sons 1994
[14] M N Katabarwa P Habomugisha and F O Richards ldquoImple-menting community-directed treatmentwith ivermectin for the
control of onchocerciasis in Uganda (1997-2000) an evalua-tionrdquo Annals of Tropical Medicine and Parasitology vol 96 no1 pp 61ndash73 2002
[15] E C Emukah U Enyinnaya N S Olaniran et al ldquoFactorsaffecting the attrition of community-directed distributors ofivermectin in an onchocerciasis-control programme in the Imoand Abia states of south-eastern Nigeriardquo Annals of TropicalMedicine and Parasitology vol 102 no 1 pp 45ndash51 2008
[16] A Prost and J Prodrsquohon ldquoLe diagnostique parasitologique delrsquoonchocercose revue critique des methods en usagerdquoMedicineTropicale vol 38 pp 519ndash532 1978
[17] H Schulz Key ldquoA simple technique to assess the total number ofOnchocerca volvulusmicrofilariae in skin snipsrdquo Tropenmedizinund Parasitologie vol 29 no 1 pp 51ndash54 1978
[18] WHO Report ldquoOnchocerciasis and its control Report of aWHO Expert Committee on Onchocerciasis Controlrdquo TechRep 852 Geneva Switzerland 1995
[19] WHO Report Strategies For Ivermectin Distribution ThroughPrimaryHealth Care SystemWHOPHL91 24WHOGenevaSwitzerland 1991
[20] E J Albiez D W Buttner and B O L Duke ldquoDiagnosisand extirpation of nodules in human onchocerciasisrdquo TropicalMedicine and Parasitology vol 39 no 4 pp 331ndash346 1988
[21] P Ngoumou J F Walsh and J M Mace ldquoA rapid mappingtechnique for the prevalence and distribution of onchocerciasisa Cameroon case studyrdquo Annals of Tropical Medicine andParasitology vol 88 no 5 pp 463ndash474 1994
[22] M Katabarwa A W Onapa and B Nakileza ldquoRapid epidemi-ological mapping of onchocerciasis in areas of uganda whereSimulium neavei SL is the vectorrdquo East African Medical Journalvol 76 no 8 pp 440ndash446 1999
[23] J F Walsh J B Davies R Le Berre and R Garms ldquoStandard-ization of criteria for assessing the effect of Simulium control inonchocerciasis control programmesrdquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 72 no 6 pp 675ndash676 1978
[24] J B Davies ldquoA rapid staining and clearing technique for detect-ing filarial larvae in alcohol-preserved vectorsrdquo Transactions ofthe Royal Society of Tropical Medicine and Hygiene vol 89 no3 p 280 1995
[25] M Katabarwa P Habomugisha A Eyamba S Agunyo andC Mentou ldquoMonitoring ivermectin distributors involved inintegrated health care services through community-directedinterventionsmdasha comparison of Cameroon and Uganda expe-riences over a period of three years (2004ndash2006)rdquo TropicalMedicine and International Health vol 15 no 2 pp 216ndash2232010
[26] J Remme O Ba K Y Dadzie and M Karam ldquoA force-of-infection model for onchocerciasis and its applications inthe epidemiological evaluation of the onchocerciasis controlprogramme in the volta river basin areardquo Bulletin of the WorldHealth Organization vol 64 no 5 pp 667ndash681 1986
[27] P Barbazan H Escaffre R Mbentengam and M BoussinesqldquoEntomologic study on the transmission of onchocerciasis ina forest-savanna transition area of Cameroonrdquo Bulletin de laSociete de Pathologie Exotique vol 91 no 2 pp 178ndash182 1998
[28] E Cadot P Barbazan andM Boussinesq ldquoGeographical deter-minants of onchocerciasis transmission in a forestsavannahtransition zone two villages of the mbam focusrdquo Sante vol 8no 6 pp 429ndash435 1998
[29] K Awadzi S K Attah E T Addy et al ldquoThirty-monthfollow-up of sub-optimal responders to multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in Ghanardquo
12 Journal of Parasitology Research
Annals of Tropical Medicine and Parasitology vol 98 no 4 pp359ndash370 2004
[30] K Awadzi D A Boakye G Edwards et al ldquoAn investigationof persistent microfilaridermias despite multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in GhanardquoAnnals of Tropical Medicine and Parasitology vol 98 no 3 pp231ndash249 2004
[31] M Y Osei-Atweneboana J K Eng D A Boakye J OGyapong and R K Prichard ldquoPrevalence and intensity ofOnchocerca volvulus infection and efficacy of ivermectin inendemic communities in Ghana a two-phase epidemiologicalstudyrdquoThe Lancet vol 369 no 9578 pp 2021ndash2029 2007
[32] C Bottomley V Isham R C Collins and M G BasanezldquoRates of microfilarial production by Onchocerca volvulus arenot cumulatively reduced by multiple ivermectin treatmentsrdquoParasitology vol 135 no 13 pp 1571ndash1581 2008
[33] R Garms T L Lakwo R Ndyomugyenyi et al ldquoThe elimina-tion of the vector Simulium neavei from the Itwara onchocerci-asis focus in Uganda by ground larvicidingrdquo Acta Tropica vol111 no 3 pp 203ndash210 2009
[34] R Ndyomugyenyi E Tukesiga D W Buttner and R GarmsldquoThe impact of ivermectin treatment alone and when inparallel with Simulium neavei elimination on onchocerciasis inUgandardquo Tropical Medicine and International Health vol 9 no8 pp 882ndash886 2004
[35] H P Duerr and M Eichner ldquoEpidemiology and control ofonchocerciasis the threshold biting rate of savannah onchocer-ciasis in Africardquo International Journal for Parasitology vol 40no 6 pp 641ndash650 2010
[36] K Dietz ldquoDensity-dependence in parasite transmissiondynamicsrdquo Parasitology Today vol 4 no 4 pp 91ndash97 1988
[37] M G Basanez J H F Remme E S Alley et al ldquoDensity-dependent processes in the transmission of human onchocerci-asis relationship between the numbers ofmicrofilariae ingestedand successful larval development in the simuliid vectorrdquoParasitology vol 110 no 4 pp 409ndash427 1995
[38] B A Boatin L Toe E S Alley N J D Nagelkerke GBorsboom and J D F Habbema ldquoDetection of Onchocercavolvulus infection in lowprevalence areas a comparison of threediagnostic methodsrdquo Parasitology vol 125 no 6 pp 545ndash5522002
[39] M Noma B E B Nwoke I Nutall et al ldquoRapid epidemio-logical mapping of onchocerciasis (REMO) its application bythe African programme for onchocerciasis control (APOC)rdquoAnnals of Tropical Medicine and Parasitology vol 96 supple-ment 1 pp S29ndashS39 2002
[40] G Fobi J R M Mbina G Ozoh et al ldquoOnchocerciasis inthe area of Lastourville Gabon Clinical and entomologicalaspectsrdquo Bulletin de la Societe de Pathologie Exotique vol 99no 4 pp 269ndash271 2006
[41] M N Katabarwa A Eyamba M Chouaibou et al ldquoDoesonchocerciasis transmission take place in hypoendemic areasa study from theNorth Region of CameroonrdquoTropicalMedicineand International Health vol 15 no 5 pp 645ndash652 2010
[42] WHO Report Certification of Elimination of Human Onchocer-ciasis Criteria and Procedures Criteria For Certification of Inter-ruption of TransmissionElimination of Human OnchocerciasisWorld Health Organization Geneva Switzerland 2001
[43] R Seidenfaden A Fischer I Bonow D Ekale V Tanya andA Renz ldquoCombined benefits of annual mass treatment withivermectin and cattle zooprophylaxis on the severity of humanonchocerciasis in northern Cameroonrdquo Tropical Medicine andInternational Health vol 6 no 9 pp 715ndash725 2001
Figure 2 Comparison of mf rates among adults and children atbaseline 1996 with followup surveys in 2005 2006 and 2011 inWestRegion of Cameroon
for failure to attain optimal parasitological and entomologicalimpacts
High vector density and mf rates suggest that the forceof transmission may have been very high and most likely thereason for the results obtained [26]The present study did notconsider the standardmeasure of intensity of infection whichis related to force of infection community mf load (CMFL)This requires a calculation that involves weighing the snipand counting the microfilaria which was not done [19] Werecommend that it should be done in future studies
In Massangam Health District it is possible that high mfand nodule rates in the follow-up assessments may be dueto the ldquoforce of infectionrdquo across the neighbouring CentralRegion where peer-reviewed studies indicate considerableonchocerciasis transmission [27 28] River Nja a tributary ofRiver Noun and River Kichi a tributary of River Mbam areknown black fly breeding sites responsible for cross-bordertransmission between West and Central regions Thereforewe recommend collaboration between the regions in order tounderstand the limits of cross-border onchocerciasis affectedarea and harmonize intervention if elimination becomes thegoal in Cameroon
Another possible explanation for high mf rates couldbe related to suboptimal response to ivermectin observedin some onchocerciasis endemic areas of Ghana The adultfemale O volvulus worms were resuming microfilaria repro-duction more rapidly after ivermectin treatment than wouldnormally be expected suggesting possible development ofresistance to ivermectin [29ndash31] We recommend that thepossibility of suboptimal response to ivermectin in WestRegion be investigated
The microfilaria rate in adults and children tended tofollow the expected trend where a single annual dose ofivermectin over a number of years significantly reduced thelow mf rates that tend to persist [3] The observed patternindicated a tendency for themf rate to raise a fewmonths aftermass treatment until another dose of ivermectin is providedconfirming that microfilarial production is not cumulativelyreduced by several annual ivermectin treatments [32] Themf rate trend at three six and eleven months after mass
treatment is usually not different from the infection ratewithin the flies over a period after mass treatment withivermectin [33] Ivermectin kills existing microfilariae andtends to exert an ldquoembryostatic effectrdquo by which microfilarialproduction is suppressed over a few weeks after treatmentbut then after the mf rate begins to increase [32] Underfavourable ecological conditions interruption of onchocer-ciasis transmission with annual mass treatment may requiremany more years before it is attained
As for twice yearly treatment with ivermectin or whenit is coupled with vector control infection rate continuedto fall implying that interruption of transmission could berapidly attained [1 33 34] We recommend that West Regionof Cameroon should consider twice yearly treatment or atleast annual treatment with targeted vector control
In the present study some communities (Folap andNjisseng) in Foumban and Kouoptamo health districts hadmf rates lower than 5 in adults and 0 in children Inthese communities the Diawara et al criteria are closeto being attained and yet with low levels of infectiontransmission is much more efficient than at high levels ofinfection [35ndash37] Thus if low levels of infection are notdetected and controlled they could result in fast diseaserecrudescence Skin snip (microscopy) has low sensitivity ofless than 20 at less than 20 nodule rate and the resultsobtained may not reflect correct mf endemicity levels [38]Therefore interventions in these health districts cannot behalted as disease recrudescence could occur [29 30] Whereinterruption of transmission of onchocerciasis is the objectivewe recommend a search for affordable less intrusive rapidsensitive and highly specific diagnostic tools for low levelinfections in order to validate interruption of onchocerciasistransmission
The APOC threshold for launching mass treatment isan onchocercal nodule rate of ge20 Fondjanti community(Bandja Health District) with nodule rate of 23 and mfrate of 64 would pass for mass treatment while Njonecommunity (Foumbot Health District) with nodule rate of186 and mf rate of 419 would fail [39] Nodule rate couldalso be confounded by the presence of ganglia and Taeniasolium [40 41] The entomological results showed that therisk of contracting onchocerciasis in FoumbotHealthDistrictwas higher than in Bafang Health District confirming thereliability of mf rates compared with nodule rates With theshift from control to elimination of onchocerciasis in Africawe recommend that nodule prevalence should not be usedto determine whether an endemic area should receive masstreatment or not
Annual biting rates with the range of 28560 to 125380are some of the highest observed globally Yet infective ratein Bafang from the western part of the region was zerojustifying low mf rates (06 in children and a mean of52 in adults) The question would be whether annual masstreatment could be withdrawn without resulting in diseaserecrudescence Existing low level transmission with the highannual biting rate of 52610 could still result in onchocerciasisrecrudescence It was also evident in this study that one-month baseline entomological data was likely to miss peakbiting transmission pattern of Simulium vectors and the
8 Journal of Parasitology Research
Table3Com
parin
gmfp
revalencea
mon
gchild
renatbaselin
e(1996)and
follo
wup
in2005200
6and2011three
mon
thssix
mon
thsandele
venmon
thsrespectiv
elyafterm
asstreatment
inWestR
egion
Cameroo
n
Distric
tCom
mun
ityBa
selin
e1996
(119899=185)
Follo
wup
2005(119899=403)
Follo
wup
200
6(119899=134)
Follo
wup
2011(119899=626)
No
Exam
ined
No
positive
mf
positive
No
Exam
ined
No
positive
mf
positive
No
Exam
ined
No
positive
mf
positive
Noexam
No
positive
mf
positive
Bafang
Bakonti-B
akassa
102
13127
740
0lowast43
000
167
106
Bafang
Batchieu
704
57
40
00
Baham
Bapi
ND
ND
ND
292
69
Band
jaBa
bouantou
(Batou
la)lowast
ND
ND
ND
647
109
143
214
193
158
Bang
angte
Batchingoulowast
ND
ND
ND
241
42
152
133
211
48
Bang
angte
NdjiptaIII(Fo
p-Tchu
i)lowastND
ND
ND
632
32
50
00
250
00
FossangCh
efferie
ND
ND
ND
380
00
40
00
252
80
Foum
bot
Njone
2019
950
123
25lowast
161
63
8224
293lowastlowastlowast
Foum
bot
Kousang-Malanden
6322
349
ND
ND
ND
ND
ND
ND
ND
ND
ND
Kekem
Mbafamlowast
ND
ND
ND
580
00
330
00
200
00
Penk
a-Michel
Bakassa
ND
ND
ND
ND
ND
ND
ND
ND
ND
741
14Fo
umban
Folap
ND
ND
ND
ND
ND
ND
ND
ND
ND
108
000
Kouo
ptam
oNjisseng
ND
ND
ND
ND
ND
ND
ND
ND
ND
241
42
Massang
amMakou
opsap
ND
ND
ND
ND
ND
ND
ND
ND
ND
3221
656
12185
5429
240
317
42lowast
134
645
626
5689
NDnot
done
lowastSign
ificant
(119875lt005)mdash
follo
wup
2005
comparedwith
theb
aseline
lowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2006
comparedwith
2005
follo
wup
lowastlowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2011comparedwith
2006
follo
wup
Journal of Parasitology Research 9
Table4
Com
parin
gnod
ulep
revalencea
mon
gadu
ltsatbaselin
e(1996)and
follo
wup
in2005200
6and2011three
mon
thssix
mon
thsandele
venmon
thsrespectiv
elyafterm
asstreatment
inWestR
egion
Cameroo
n
Distric
tCom
mun
ityBa
selin
e1996
(119899=305)
Follo
wup
2005(119899=780)
Follo
wup
200
6(119899=782)
Follo
wup
2011(119899=2703)
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
Bafang
Bakassa
2716
593
139
110
79lowast
9711
113
251
2184
Bakonti
2711
407
9850
51lowast
755
67
338
36107
Fond
janti
2719
704
125
29232
Bakambe
2719
704
105
110
105lowast
9113
143
125
29232
Baham
Bapi
2915
517
ND
ND
ND
ND
ND
ND
189
1579
Band
jaBa
bouantou
(Batou
la)
2616
615
6150
82lowast
7618
237lowastlowast
8412
143
Bang
angte
Batchingou
2922
759
101
160
158lowast
8023
288lowastlowast
247
29117lowastlowastlowast
NdjiptaIII(Fo
p-Tchu
i)29
23793
7850
64lowast
578
140lowastlowast
929
98
Foum
bot
Fossang-chefferie
2824
857
7170
99lowast
7218
250lowastlowast
150
26173lowastlowastlowast
Njone
2926
897
3490
265lowast
122
37303
167
31186lowastlowastlowast
Kekem
Mbafam
2417
708
9350
54lowast
112
12107lowastlowast
163
27166
Penk
a-Michel
Bakassa
3012
400
ND
ND
ND
ND
ND
ND
195
1577
Foum
ban
Folap
ND
ND
ND
ND
ND
ND
ND
ND
ND
265
415
Kouo
ptam
oNjisseng
ND
ND
ND
ND
ND
ND
ND
ND
ND
168
636
Malantouen
Matou
pou
ND
ND
ND
ND
ND
ND
ND
ND
ND
170
953
Massang
amMakou
opsap
ND
ND
ND
ND
ND
ND
ND
ND
ND
9943
434
332
220
663
780
7495lowast
782
145
185lowastlowast
2828
341
121lowastlowastlowast
NDnot
done
lowastSign
ificant
(119875lt005)mdash
follo
wup
2005
comparedwith
theb
aseline
lowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2006
comparedwith
2005
follo
wup
lowastlowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2011comparedwith
2006
follo
wup
10 Journal of Parasitology Research
Table 5 Comparing baseline entomological data of 1996 at two fly collection sites and three during 2011
Monthyear of black fly collection Baseline May 1996 Followup 2011Black fly collection sites Bafang (Basseu) Foumbot (Maka) Bafang Foumbot MassangamNumber of Simulium caught 5 166 5261 2856 12538Number of Simulium dissected 5 142 5261 2856 12138Number of parous flies 1 97 1502 1028 2845Parous rate () 20 683 285 36 234Number of Simulium flies infected (L1 L2 L3] 1 12 3 9 19Infection rate () 2000 845 020 088 067Number of Simulium flies infective L3 larval stage in the head 20 2 0 2 5Infective rate () 200 211 000 019 018Monthly biting rate per person 750 166000 na na naMonthly transmission potentiallowast 150 21040 na na naAnnual biting rate per person Na na 52610 28560 125380Annual transmission potential Na na 0 70 310
0
500
1000
1500
2000
2500
3000
3500
4000
No
of fl
ies c
olle
cted
BafangFoumbotMakouopsap
MarApr2011 2012
May Jun Jul AugSeptOctNovDec Jan Feb
Figure 3 Monthly seasonal biting of Simulium flies at 3 fly catchingsites in West Region
calculation ofATPTherefore collection of entomological dataover several months is required as reflected in the follow-up study The information on peak biting and transmissionpatterns could effectively be utilized for ivermectin treatmentfor maximum impact on transmission especially where theforce of transmission is considerably high if elimination ofonchocerciasis is the goal In the follow-up survey it is onlyat Bafang fly collection site that the entomological criterionfor interruption of transmission was met with an ATP of zero[42]
The present study however did not perform moleculartesting in order to determine if the L3 larvae wereO volvulusor another (animal) Onchocerca species Based on humanmf prevalence in skin and infections in children we thinkthat there is likelihood that some of the larvae observedin vectors were O volvulus However a study conducted inNorth Region of Cameroon during the 1990s showed that
33 of infective larvae in S damnosum were O volvuluswhereas 65 were O ochengi and 2 were O ramachandrini[43] It is until such a study is conducted in West Region ofCameroon that we will know the extent to which O ochengiis responsible for a significant proportion of infected flies thatcould confound the infection rate there
Our findings reflecting an observation period of 15 yearsshowed that annual mass treatment with ivermectin may notinterrupt the transmission of onchocerciasis in all differentecological zones of West Region Therefore the intensive useof ivermectin is recommended if interruption of transmissionof onchocerciasis is to be attained [1]
5 Conclusion
Annual mass treatment with ivermectin through commu-nity-directed treatment was preferred as a good and lessexpensive method for controlling onchocerciasis in endemicAfrican countries with assistance from the African Pro-gramme for Onchocerciasis Control The studies in MaliSenegal and Nigeria have shown that an annual dose ofivermectin had interrupted transmission of the disease andall interventions could be halted without the risk of diseaserecrudescence However an annual dose of ivermectin hasnot interrupted transmission after 15 years of mass treatmentin some areas in West Region of Cameroon just like inNorth region [8] It has also been less effective in someonchocerciasis endemic areas in Ghana The present paperagain highlights the fact that for interruption of onchocer-ciasis transmission feasible and different but complementarystrategic options should be adopted as elimination becomesthe goal in Africa
Acknowledgments
The investigators would like to acknowledge the staff ofMinistry of Health at the national regional and healthdistrict levels in West Region along with Carter CenterCameroon Office for mobilizing and educating selected
Journal of Parasitology Research 11
communities and providing policy and administrative sup-port The involvement of community members in selectedcommunities in mf and nodule assessments and Simulium flycollection is highly appreciated The Carter Center the LionsClubs International Foundation (LCIF) and the African Pro-gramme for onchocerciasis Control (APOC) which fundedthe CDTI activities and the surveys are also highly appreci-ated
References
[1] E W Cupp and M S Cupp ldquoShort report impact of iver-mectin community-level treatments on elimination of adultOnchocerca volvulus when individuals receive multiple treat-ments per yearrdquoThe American Journal of Tropical Medicine andHygiene vol 73 no 6 pp 1159ndash1161 2005
[2] H R Taylor M Pacque B Munoz and B M Greene ldquoImpactof mass treatment of onchocerciasis with ivermectin on thetransmission of infectionrdquo Science vol 250 no 4977 pp 116ndash118 1990
[3] G J J M Borsboom B A Boatin N J D Nagelkerkeet al ldquoImpact of ivermectin on onchocerciasis transmissionassessing the empirical evidence that repeated ivermectin masstreatmentsmay lead to eliminationeradication inWest-AfricardquoFilaria Journal vol 2 article 8 2003
[4] A D Hopkins ldquoIvermectin and onchocerciasis is it all solvedrdquoEye vol 19 no 10 pp 1057ndash1066 2005
[5] L Yameogo ldquoSpecial intervention zonesrdquo Annals of TropicalMedicine and Parasitology vol 102 supplement 1 pp 23ndash242008
[6] D H Molyneux and M N Malecela ldquoNeglected tropicaldiseases and themillennium development goals why the ldquootherdiseasesrdquo matter reality versus rhetoricrdquo Parasites amp Vectorsvol 4 2011
[7] WHOReportAcceleratingWorkToOvercome theGlobal Impactof Neglected Tropical Disease A Roadmap For Implementationvol 1211WorldHealthOrganization 20AvenueAppia GenevaSwitzerland 2012
[8] M N Katabarwa A Eyamba P Nwane et al ldquoSeventeenyears of annual distribution of ivermectin has not interruptedonchocerciasis transmission in North Region Cameroonrdquo TheAmerican Journal of Tropical Medicine and Hygiene vol 85 no6 pp 1041ndash1049 2011
[9] B A Boatin and F O Richards ldquoControl of onchocerciasisrdquoAdvances in Parasitology vol 61 pp 349ndash394 2006
[10] D R Hopkins F O Richards and M Katabarwa ldquoWhitheronchocerciasis control in Africardquo American Journal of TropicalMedicine and Hygiene vol 72 no 1 pp 1ndash2 2005
[11] L Diawara M O Traore A Badji et al ldquoFeasibilityof onchocerciasis elimination with ivermectin treatment inendemic foci in Africa first evidence from studies in Mali andSenegalrdquo PLoS Neglected Tropical Diseases vol 3 no 7 articlee497 2009
[12] F O Richards E S Miri M Katabarwa et al ldquoThe carter cen-terrsquos assistance to river blindness control programs establish-ing treatment objectives and goals for monitoring ivermectindelivery systems on two continentsrdquo The American Journal ofTropical Medicine and Hygiene vol 65 no 2 pp 108ndash114 2001
[13] P Salant and D A Dilman How to Conduct Your Own SurveyJohn Wiley amp Sons 1994
[14] M N Katabarwa P Habomugisha and F O Richards ldquoImple-menting community-directed treatmentwith ivermectin for the
control of onchocerciasis in Uganda (1997-2000) an evalua-tionrdquo Annals of Tropical Medicine and Parasitology vol 96 no1 pp 61ndash73 2002
[15] E C Emukah U Enyinnaya N S Olaniran et al ldquoFactorsaffecting the attrition of community-directed distributors ofivermectin in an onchocerciasis-control programme in the Imoand Abia states of south-eastern Nigeriardquo Annals of TropicalMedicine and Parasitology vol 102 no 1 pp 45ndash51 2008
[16] A Prost and J Prodrsquohon ldquoLe diagnostique parasitologique delrsquoonchocercose revue critique des methods en usagerdquoMedicineTropicale vol 38 pp 519ndash532 1978
[17] H Schulz Key ldquoA simple technique to assess the total number ofOnchocerca volvulusmicrofilariae in skin snipsrdquo Tropenmedizinund Parasitologie vol 29 no 1 pp 51ndash54 1978
[18] WHO Report ldquoOnchocerciasis and its control Report of aWHO Expert Committee on Onchocerciasis Controlrdquo TechRep 852 Geneva Switzerland 1995
[19] WHO Report Strategies For Ivermectin Distribution ThroughPrimaryHealth Care SystemWHOPHL91 24WHOGenevaSwitzerland 1991
[20] E J Albiez D W Buttner and B O L Duke ldquoDiagnosisand extirpation of nodules in human onchocerciasisrdquo TropicalMedicine and Parasitology vol 39 no 4 pp 331ndash346 1988
[21] P Ngoumou J F Walsh and J M Mace ldquoA rapid mappingtechnique for the prevalence and distribution of onchocerciasisa Cameroon case studyrdquo Annals of Tropical Medicine andParasitology vol 88 no 5 pp 463ndash474 1994
[22] M Katabarwa A W Onapa and B Nakileza ldquoRapid epidemi-ological mapping of onchocerciasis in areas of uganda whereSimulium neavei SL is the vectorrdquo East African Medical Journalvol 76 no 8 pp 440ndash446 1999
[23] J F Walsh J B Davies R Le Berre and R Garms ldquoStandard-ization of criteria for assessing the effect of Simulium control inonchocerciasis control programmesrdquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 72 no 6 pp 675ndash676 1978
[24] J B Davies ldquoA rapid staining and clearing technique for detect-ing filarial larvae in alcohol-preserved vectorsrdquo Transactions ofthe Royal Society of Tropical Medicine and Hygiene vol 89 no3 p 280 1995
[25] M Katabarwa P Habomugisha A Eyamba S Agunyo andC Mentou ldquoMonitoring ivermectin distributors involved inintegrated health care services through community-directedinterventionsmdasha comparison of Cameroon and Uganda expe-riences over a period of three years (2004ndash2006)rdquo TropicalMedicine and International Health vol 15 no 2 pp 216ndash2232010
[26] J Remme O Ba K Y Dadzie and M Karam ldquoA force-of-infection model for onchocerciasis and its applications inthe epidemiological evaluation of the onchocerciasis controlprogramme in the volta river basin areardquo Bulletin of the WorldHealth Organization vol 64 no 5 pp 667ndash681 1986
[27] P Barbazan H Escaffre R Mbentengam and M BoussinesqldquoEntomologic study on the transmission of onchocerciasis ina forest-savanna transition area of Cameroonrdquo Bulletin de laSociete de Pathologie Exotique vol 91 no 2 pp 178ndash182 1998
[28] E Cadot P Barbazan andM Boussinesq ldquoGeographical deter-minants of onchocerciasis transmission in a forestsavannahtransition zone two villages of the mbam focusrdquo Sante vol 8no 6 pp 429ndash435 1998
[29] K Awadzi S K Attah E T Addy et al ldquoThirty-monthfollow-up of sub-optimal responders to multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in Ghanardquo
12 Journal of Parasitology Research
Annals of Tropical Medicine and Parasitology vol 98 no 4 pp359ndash370 2004
[30] K Awadzi D A Boakye G Edwards et al ldquoAn investigationof persistent microfilaridermias despite multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in GhanardquoAnnals of Tropical Medicine and Parasitology vol 98 no 3 pp231ndash249 2004
[31] M Y Osei-Atweneboana J K Eng D A Boakye J OGyapong and R K Prichard ldquoPrevalence and intensity ofOnchocerca volvulus infection and efficacy of ivermectin inendemic communities in Ghana a two-phase epidemiologicalstudyrdquoThe Lancet vol 369 no 9578 pp 2021ndash2029 2007
[32] C Bottomley V Isham R C Collins and M G BasanezldquoRates of microfilarial production by Onchocerca volvulus arenot cumulatively reduced by multiple ivermectin treatmentsrdquoParasitology vol 135 no 13 pp 1571ndash1581 2008
[33] R Garms T L Lakwo R Ndyomugyenyi et al ldquoThe elimina-tion of the vector Simulium neavei from the Itwara onchocerci-asis focus in Uganda by ground larvicidingrdquo Acta Tropica vol111 no 3 pp 203ndash210 2009
[34] R Ndyomugyenyi E Tukesiga D W Buttner and R GarmsldquoThe impact of ivermectin treatment alone and when inparallel with Simulium neavei elimination on onchocerciasis inUgandardquo Tropical Medicine and International Health vol 9 no8 pp 882ndash886 2004
[35] H P Duerr and M Eichner ldquoEpidemiology and control ofonchocerciasis the threshold biting rate of savannah onchocer-ciasis in Africardquo International Journal for Parasitology vol 40no 6 pp 641ndash650 2010
[36] K Dietz ldquoDensity-dependence in parasite transmissiondynamicsrdquo Parasitology Today vol 4 no 4 pp 91ndash97 1988
[37] M G Basanez J H F Remme E S Alley et al ldquoDensity-dependent processes in the transmission of human onchocerci-asis relationship between the numbers ofmicrofilariae ingestedand successful larval development in the simuliid vectorrdquoParasitology vol 110 no 4 pp 409ndash427 1995
[38] B A Boatin L Toe E S Alley N J D Nagelkerke GBorsboom and J D F Habbema ldquoDetection of Onchocercavolvulus infection in lowprevalence areas a comparison of threediagnostic methodsrdquo Parasitology vol 125 no 6 pp 545ndash5522002
[39] M Noma B E B Nwoke I Nutall et al ldquoRapid epidemio-logical mapping of onchocerciasis (REMO) its application bythe African programme for onchocerciasis control (APOC)rdquoAnnals of Tropical Medicine and Parasitology vol 96 supple-ment 1 pp S29ndashS39 2002
[40] G Fobi J R M Mbina G Ozoh et al ldquoOnchocerciasis inthe area of Lastourville Gabon Clinical and entomologicalaspectsrdquo Bulletin de la Societe de Pathologie Exotique vol 99no 4 pp 269ndash271 2006
[41] M N Katabarwa A Eyamba M Chouaibou et al ldquoDoesonchocerciasis transmission take place in hypoendemic areasa study from theNorth Region of CameroonrdquoTropicalMedicineand International Health vol 15 no 5 pp 645ndash652 2010
[42] WHO Report Certification of Elimination of Human Onchocer-ciasis Criteria and Procedures Criteria For Certification of Inter-ruption of TransmissionElimination of Human OnchocerciasisWorld Health Organization Geneva Switzerland 2001
[43] R Seidenfaden A Fischer I Bonow D Ekale V Tanya andA Renz ldquoCombined benefits of annual mass treatment withivermectin and cattle zooprophylaxis on the severity of humanonchocerciasis in northern Cameroonrdquo Tropical Medicine andInternational Health vol 6 no 9 pp 715ndash725 2001
Figure 2 Comparison of mf rates among adults and children atbaseline 1996 with followup surveys in 2005 2006 and 2011 inWestRegion of Cameroon
for failure to attain optimal parasitological and entomologicalimpacts
High vector density and mf rates suggest that the forceof transmission may have been very high and most likely thereason for the results obtained [26]The present study did notconsider the standardmeasure of intensity of infection whichis related to force of infection community mf load (CMFL)This requires a calculation that involves weighing the snipand counting the microfilaria which was not done [19] Werecommend that it should be done in future studies
In Massangam Health District it is possible that high mfand nodule rates in the follow-up assessments may be dueto the ldquoforce of infectionrdquo across the neighbouring CentralRegion where peer-reviewed studies indicate considerableonchocerciasis transmission [27 28] River Nja a tributary ofRiver Noun and River Kichi a tributary of River Mbam areknown black fly breeding sites responsible for cross-bordertransmission between West and Central regions Thereforewe recommend collaboration between the regions in order tounderstand the limits of cross-border onchocerciasis affectedarea and harmonize intervention if elimination becomes thegoal in Cameroon
Another possible explanation for high mf rates couldbe related to suboptimal response to ivermectin observedin some onchocerciasis endemic areas of Ghana The adultfemale O volvulus worms were resuming microfilaria repro-duction more rapidly after ivermectin treatment than wouldnormally be expected suggesting possible development ofresistance to ivermectin [29ndash31] We recommend that thepossibility of suboptimal response to ivermectin in WestRegion be investigated
The microfilaria rate in adults and children tended tofollow the expected trend where a single annual dose ofivermectin over a number of years significantly reduced thelow mf rates that tend to persist [3] The observed patternindicated a tendency for themf rate to raise a fewmonths aftermass treatment until another dose of ivermectin is providedconfirming that microfilarial production is not cumulativelyreduced by several annual ivermectin treatments [32] Themf rate trend at three six and eleven months after mass
treatment is usually not different from the infection ratewithin the flies over a period after mass treatment withivermectin [33] Ivermectin kills existing microfilariae andtends to exert an ldquoembryostatic effectrdquo by which microfilarialproduction is suppressed over a few weeks after treatmentbut then after the mf rate begins to increase [32] Underfavourable ecological conditions interruption of onchocer-ciasis transmission with annual mass treatment may requiremany more years before it is attained
As for twice yearly treatment with ivermectin or whenit is coupled with vector control infection rate continuedto fall implying that interruption of transmission could berapidly attained [1 33 34] We recommend that West Regionof Cameroon should consider twice yearly treatment or atleast annual treatment with targeted vector control
In the present study some communities (Folap andNjisseng) in Foumban and Kouoptamo health districts hadmf rates lower than 5 in adults and 0 in children Inthese communities the Diawara et al criteria are closeto being attained and yet with low levels of infectiontransmission is much more efficient than at high levels ofinfection [35ndash37] Thus if low levels of infection are notdetected and controlled they could result in fast diseaserecrudescence Skin snip (microscopy) has low sensitivity ofless than 20 at less than 20 nodule rate and the resultsobtained may not reflect correct mf endemicity levels [38]Therefore interventions in these health districts cannot behalted as disease recrudescence could occur [29 30] Whereinterruption of transmission of onchocerciasis is the objectivewe recommend a search for affordable less intrusive rapidsensitive and highly specific diagnostic tools for low levelinfections in order to validate interruption of onchocerciasistransmission
The APOC threshold for launching mass treatment isan onchocercal nodule rate of ge20 Fondjanti community(Bandja Health District) with nodule rate of 23 and mfrate of 64 would pass for mass treatment while Njonecommunity (Foumbot Health District) with nodule rate of186 and mf rate of 419 would fail [39] Nodule rate couldalso be confounded by the presence of ganglia and Taeniasolium [40 41] The entomological results showed that therisk of contracting onchocerciasis in FoumbotHealthDistrictwas higher than in Bafang Health District confirming thereliability of mf rates compared with nodule rates With theshift from control to elimination of onchocerciasis in Africawe recommend that nodule prevalence should not be usedto determine whether an endemic area should receive masstreatment or not
Annual biting rates with the range of 28560 to 125380are some of the highest observed globally Yet infective ratein Bafang from the western part of the region was zerojustifying low mf rates (06 in children and a mean of52 in adults) The question would be whether annual masstreatment could be withdrawn without resulting in diseaserecrudescence Existing low level transmission with the highannual biting rate of 52610 could still result in onchocerciasisrecrudescence It was also evident in this study that one-month baseline entomological data was likely to miss peakbiting transmission pattern of Simulium vectors and the
8 Journal of Parasitology Research
Table3Com
parin
gmfp
revalencea
mon
gchild
renatbaselin
e(1996)and
follo
wup
in2005200
6and2011three
mon
thssix
mon
thsandele
venmon
thsrespectiv
elyafterm
asstreatment
inWestR
egion
Cameroo
n
Distric
tCom
mun
ityBa
selin
e1996
(119899=185)
Follo
wup
2005(119899=403)
Follo
wup
200
6(119899=134)
Follo
wup
2011(119899=626)
No
Exam
ined
No
positive
mf
positive
No
Exam
ined
No
positive
mf
positive
No
Exam
ined
No
positive
mf
positive
Noexam
No
positive
mf
positive
Bafang
Bakonti-B
akassa
102
13127
740
0lowast43
000
167
106
Bafang
Batchieu
704
57
40
00
Baham
Bapi
ND
ND
ND
292
69
Band
jaBa
bouantou
(Batou
la)lowast
ND
ND
ND
647
109
143
214
193
158
Bang
angte
Batchingoulowast
ND
ND
ND
241
42
152
133
211
48
Bang
angte
NdjiptaIII(Fo
p-Tchu
i)lowastND
ND
ND
632
32
50
00
250
00
FossangCh
efferie
ND
ND
ND
380
00
40
00
252
80
Foum
bot
Njone
2019
950
123
25lowast
161
63
8224
293lowastlowastlowast
Foum
bot
Kousang-Malanden
6322
349
ND
ND
ND
ND
ND
ND
ND
ND
ND
Kekem
Mbafamlowast
ND
ND
ND
580
00
330
00
200
00
Penk
a-Michel
Bakassa
ND
ND
ND
ND
ND
ND
ND
ND
ND
741
14Fo
umban
Folap
ND
ND
ND
ND
ND
ND
ND
ND
ND
108
000
Kouo
ptam
oNjisseng
ND
ND
ND
ND
ND
ND
ND
ND
ND
241
42
Massang
amMakou
opsap
ND
ND
ND
ND
ND
ND
ND
ND
ND
3221
656
12185
5429
240
317
42lowast
134
645
626
5689
NDnot
done
lowastSign
ificant
(119875lt005)mdash
follo
wup
2005
comparedwith
theb
aseline
lowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2006
comparedwith
2005
follo
wup
lowastlowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2011comparedwith
2006
follo
wup
Journal of Parasitology Research 9
Table4
Com
parin
gnod
ulep
revalencea
mon
gadu
ltsatbaselin
e(1996)and
follo
wup
in2005200
6and2011three
mon
thssix
mon
thsandele
venmon
thsrespectiv
elyafterm
asstreatment
inWestR
egion
Cameroo
n
Distric
tCom
mun
ityBa
selin
e1996
(119899=305)
Follo
wup
2005(119899=780)
Follo
wup
200
6(119899=782)
Follo
wup
2011(119899=2703)
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
No
exam
ined
No
positive
no
dule
positive
Bafang
Bakassa
2716
593
139
110
79lowast
9711
113
251
2184
Bakonti
2711
407
9850
51lowast
755
67
338
36107
Fond
janti
2719
704
125
29232
Bakambe
2719
704
105
110
105lowast
9113
143
125
29232
Baham
Bapi
2915
517
ND
ND
ND
ND
ND
ND
189
1579
Band
jaBa
bouantou
(Batou
la)
2616
615
6150
82lowast
7618
237lowastlowast
8412
143
Bang
angte
Batchingou
2922
759
101
160
158lowast
8023
288lowastlowast
247
29117lowastlowastlowast
NdjiptaIII(Fo
p-Tchu
i)29
23793
7850
64lowast
578
140lowastlowast
929
98
Foum
bot
Fossang-chefferie
2824
857
7170
99lowast
7218
250lowastlowast
150
26173lowastlowastlowast
Njone
2926
897
3490
265lowast
122
37303
167
31186lowastlowastlowast
Kekem
Mbafam
2417
708
9350
54lowast
112
12107lowastlowast
163
27166
Penk
a-Michel
Bakassa
3012
400
ND
ND
ND
ND
ND
ND
195
1577
Foum
ban
Folap
ND
ND
ND
ND
ND
ND
ND
ND
ND
265
415
Kouo
ptam
oNjisseng
ND
ND
ND
ND
ND
ND
ND
ND
ND
168
636
Malantouen
Matou
pou
ND
ND
ND
ND
ND
ND
ND
ND
ND
170
953
Massang
amMakou
opsap
ND
ND
ND
ND
ND
ND
ND
ND
ND
9943
434
332
220
663
780
7495lowast
782
145
185lowastlowast
2828
341
121lowastlowastlowast
NDnot
done
lowastSign
ificant
(119875lt005)mdash
follo
wup
2005
comparedwith
theb
aseline
lowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2006
comparedwith
2005
follo
wup
lowastlowastlowastSign
ificant
(119875lt005)mdash
follo
wup
2011comparedwith
2006
follo
wup
10 Journal of Parasitology Research
Table 5 Comparing baseline entomological data of 1996 at two fly collection sites and three during 2011
Monthyear of black fly collection Baseline May 1996 Followup 2011Black fly collection sites Bafang (Basseu) Foumbot (Maka) Bafang Foumbot MassangamNumber of Simulium caught 5 166 5261 2856 12538Number of Simulium dissected 5 142 5261 2856 12138Number of parous flies 1 97 1502 1028 2845Parous rate () 20 683 285 36 234Number of Simulium flies infected (L1 L2 L3] 1 12 3 9 19Infection rate () 2000 845 020 088 067Number of Simulium flies infective L3 larval stage in the head 20 2 0 2 5Infective rate () 200 211 000 019 018Monthly biting rate per person 750 166000 na na naMonthly transmission potentiallowast 150 21040 na na naAnnual biting rate per person Na na 52610 28560 125380Annual transmission potential Na na 0 70 310
0
500
1000
1500
2000
2500
3000
3500
4000
No
of fl
ies c
olle
cted
BafangFoumbotMakouopsap
MarApr2011 2012
May Jun Jul AugSeptOctNovDec Jan Feb
Figure 3 Monthly seasonal biting of Simulium flies at 3 fly catchingsites in West Region
calculation ofATPTherefore collection of entomological dataover several months is required as reflected in the follow-up study The information on peak biting and transmissionpatterns could effectively be utilized for ivermectin treatmentfor maximum impact on transmission especially where theforce of transmission is considerably high if elimination ofonchocerciasis is the goal In the follow-up survey it is onlyat Bafang fly collection site that the entomological criterionfor interruption of transmission was met with an ATP of zero[42]
The present study however did not perform moleculartesting in order to determine if the L3 larvae wereO volvulusor another (animal) Onchocerca species Based on humanmf prevalence in skin and infections in children we thinkthat there is likelihood that some of the larvae observedin vectors were O volvulus However a study conducted inNorth Region of Cameroon during the 1990s showed that
33 of infective larvae in S damnosum were O volvuluswhereas 65 were O ochengi and 2 were O ramachandrini[43] It is until such a study is conducted in West Region ofCameroon that we will know the extent to which O ochengiis responsible for a significant proportion of infected flies thatcould confound the infection rate there
Our findings reflecting an observation period of 15 yearsshowed that annual mass treatment with ivermectin may notinterrupt the transmission of onchocerciasis in all differentecological zones of West Region Therefore the intensive useof ivermectin is recommended if interruption of transmissionof onchocerciasis is to be attained [1]
5 Conclusion
Annual mass treatment with ivermectin through commu-nity-directed treatment was preferred as a good and lessexpensive method for controlling onchocerciasis in endemicAfrican countries with assistance from the African Pro-gramme for Onchocerciasis Control The studies in MaliSenegal and Nigeria have shown that an annual dose ofivermectin had interrupted transmission of the disease andall interventions could be halted without the risk of diseaserecrudescence However an annual dose of ivermectin hasnot interrupted transmission after 15 years of mass treatmentin some areas in West Region of Cameroon just like inNorth region [8] It has also been less effective in someonchocerciasis endemic areas in Ghana The present paperagain highlights the fact that for interruption of onchocer-ciasis transmission feasible and different but complementarystrategic options should be adopted as elimination becomesthe goal in Africa
Acknowledgments
The investigators would like to acknowledge the staff ofMinistry of Health at the national regional and healthdistrict levels in West Region along with Carter CenterCameroon Office for mobilizing and educating selected
Journal of Parasitology Research 11
communities and providing policy and administrative sup-port The involvement of community members in selectedcommunities in mf and nodule assessments and Simulium flycollection is highly appreciated The Carter Center the LionsClubs International Foundation (LCIF) and the African Pro-gramme for onchocerciasis Control (APOC) which fundedthe CDTI activities and the surveys are also highly appreci-ated
References
[1] E W Cupp and M S Cupp ldquoShort report impact of iver-mectin community-level treatments on elimination of adultOnchocerca volvulus when individuals receive multiple treat-ments per yearrdquoThe American Journal of Tropical Medicine andHygiene vol 73 no 6 pp 1159ndash1161 2005
[2] H R Taylor M Pacque B Munoz and B M Greene ldquoImpactof mass treatment of onchocerciasis with ivermectin on thetransmission of infectionrdquo Science vol 250 no 4977 pp 116ndash118 1990
[3] G J J M Borsboom B A Boatin N J D Nagelkerkeet al ldquoImpact of ivermectin on onchocerciasis transmissionassessing the empirical evidence that repeated ivermectin masstreatmentsmay lead to eliminationeradication inWest-AfricardquoFilaria Journal vol 2 article 8 2003
[4] A D Hopkins ldquoIvermectin and onchocerciasis is it all solvedrdquoEye vol 19 no 10 pp 1057ndash1066 2005
[5] L Yameogo ldquoSpecial intervention zonesrdquo Annals of TropicalMedicine and Parasitology vol 102 supplement 1 pp 23ndash242008
[6] D H Molyneux and M N Malecela ldquoNeglected tropicaldiseases and themillennium development goals why the ldquootherdiseasesrdquo matter reality versus rhetoricrdquo Parasites amp Vectorsvol 4 2011
[7] WHOReportAcceleratingWorkToOvercome theGlobal Impactof Neglected Tropical Disease A Roadmap For Implementationvol 1211WorldHealthOrganization 20AvenueAppia GenevaSwitzerland 2012
[8] M N Katabarwa A Eyamba P Nwane et al ldquoSeventeenyears of annual distribution of ivermectin has not interruptedonchocerciasis transmission in North Region Cameroonrdquo TheAmerican Journal of Tropical Medicine and Hygiene vol 85 no6 pp 1041ndash1049 2011
[9] B A Boatin and F O Richards ldquoControl of onchocerciasisrdquoAdvances in Parasitology vol 61 pp 349ndash394 2006
[10] D R Hopkins F O Richards and M Katabarwa ldquoWhitheronchocerciasis control in Africardquo American Journal of TropicalMedicine and Hygiene vol 72 no 1 pp 1ndash2 2005
[11] L Diawara M O Traore A Badji et al ldquoFeasibilityof onchocerciasis elimination with ivermectin treatment inendemic foci in Africa first evidence from studies in Mali andSenegalrdquo PLoS Neglected Tropical Diseases vol 3 no 7 articlee497 2009
[12] F O Richards E S Miri M Katabarwa et al ldquoThe carter cen-terrsquos assistance to river blindness control programs establish-ing treatment objectives and goals for monitoring ivermectindelivery systems on two continentsrdquo The American Journal ofTropical Medicine and Hygiene vol 65 no 2 pp 108ndash114 2001
[13] P Salant and D A Dilman How to Conduct Your Own SurveyJohn Wiley amp Sons 1994
[14] M N Katabarwa P Habomugisha and F O Richards ldquoImple-menting community-directed treatmentwith ivermectin for the
control of onchocerciasis in Uganda (1997-2000) an evalua-tionrdquo Annals of Tropical Medicine and Parasitology vol 96 no1 pp 61ndash73 2002
[15] E C Emukah U Enyinnaya N S Olaniran et al ldquoFactorsaffecting the attrition of community-directed distributors ofivermectin in an onchocerciasis-control programme in the Imoand Abia states of south-eastern Nigeriardquo Annals of TropicalMedicine and Parasitology vol 102 no 1 pp 45ndash51 2008
[16] A Prost and J Prodrsquohon ldquoLe diagnostique parasitologique delrsquoonchocercose revue critique des methods en usagerdquoMedicineTropicale vol 38 pp 519ndash532 1978
[17] H Schulz Key ldquoA simple technique to assess the total number ofOnchocerca volvulusmicrofilariae in skin snipsrdquo Tropenmedizinund Parasitologie vol 29 no 1 pp 51ndash54 1978
[18] WHO Report ldquoOnchocerciasis and its control Report of aWHO Expert Committee on Onchocerciasis Controlrdquo TechRep 852 Geneva Switzerland 1995
[19] WHO Report Strategies For Ivermectin Distribution ThroughPrimaryHealth Care SystemWHOPHL91 24WHOGenevaSwitzerland 1991
[20] E J Albiez D W Buttner and B O L Duke ldquoDiagnosisand extirpation of nodules in human onchocerciasisrdquo TropicalMedicine and Parasitology vol 39 no 4 pp 331ndash346 1988
[21] P Ngoumou J F Walsh and J M Mace ldquoA rapid mappingtechnique for the prevalence and distribution of onchocerciasisa Cameroon case studyrdquo Annals of Tropical Medicine andParasitology vol 88 no 5 pp 463ndash474 1994
[22] M Katabarwa A W Onapa and B Nakileza ldquoRapid epidemi-ological mapping of onchocerciasis in areas of uganda whereSimulium neavei SL is the vectorrdquo East African Medical Journalvol 76 no 8 pp 440ndash446 1999
[23] J F Walsh J B Davies R Le Berre and R Garms ldquoStandard-ization of criteria for assessing the effect of Simulium control inonchocerciasis control programmesrdquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 72 no 6 pp 675ndash676 1978
[24] J B Davies ldquoA rapid staining and clearing technique for detect-ing filarial larvae in alcohol-preserved vectorsrdquo Transactions ofthe Royal Society of Tropical Medicine and Hygiene vol 89 no3 p 280 1995
[25] M Katabarwa P Habomugisha A Eyamba S Agunyo andC Mentou ldquoMonitoring ivermectin distributors involved inintegrated health care services through community-directedinterventionsmdasha comparison of Cameroon and Uganda expe-riences over a period of three years (2004ndash2006)rdquo TropicalMedicine and International Health vol 15 no 2 pp 216ndash2232010
[26] J Remme O Ba K Y Dadzie and M Karam ldquoA force-of-infection model for onchocerciasis and its applications inthe epidemiological evaluation of the onchocerciasis controlprogramme in the volta river basin areardquo Bulletin of the WorldHealth Organization vol 64 no 5 pp 667ndash681 1986
[27] P Barbazan H Escaffre R Mbentengam and M BoussinesqldquoEntomologic study on the transmission of onchocerciasis ina forest-savanna transition area of Cameroonrdquo Bulletin de laSociete de Pathologie Exotique vol 91 no 2 pp 178ndash182 1998
[28] E Cadot P Barbazan andM Boussinesq ldquoGeographical deter-minants of onchocerciasis transmission in a forestsavannahtransition zone two villages of the mbam focusrdquo Sante vol 8no 6 pp 429ndash435 1998
[29] K Awadzi S K Attah E T Addy et al ldquoThirty-monthfollow-up of sub-optimal responders to multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in Ghanardquo
12 Journal of Parasitology Research
Annals of Tropical Medicine and Parasitology vol 98 no 4 pp359ndash370 2004
[30] K Awadzi D A Boakye G Edwards et al ldquoAn investigationof persistent microfilaridermias despite multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in GhanardquoAnnals of Tropical Medicine and Parasitology vol 98 no 3 pp231ndash249 2004
[31] M Y Osei-Atweneboana J K Eng D A Boakye J OGyapong and R K Prichard ldquoPrevalence and intensity ofOnchocerca volvulus infection and efficacy of ivermectin inendemic communities in Ghana a two-phase epidemiologicalstudyrdquoThe Lancet vol 369 no 9578 pp 2021ndash2029 2007
[32] C Bottomley V Isham R C Collins and M G BasanezldquoRates of microfilarial production by Onchocerca volvulus arenot cumulatively reduced by multiple ivermectin treatmentsrdquoParasitology vol 135 no 13 pp 1571ndash1581 2008
[33] R Garms T L Lakwo R Ndyomugyenyi et al ldquoThe elimina-tion of the vector Simulium neavei from the Itwara onchocerci-asis focus in Uganda by ground larvicidingrdquo Acta Tropica vol111 no 3 pp 203ndash210 2009
[34] R Ndyomugyenyi E Tukesiga D W Buttner and R GarmsldquoThe impact of ivermectin treatment alone and when inparallel with Simulium neavei elimination on onchocerciasis inUgandardquo Tropical Medicine and International Health vol 9 no8 pp 882ndash886 2004
[35] H P Duerr and M Eichner ldquoEpidemiology and control ofonchocerciasis the threshold biting rate of savannah onchocer-ciasis in Africardquo International Journal for Parasitology vol 40no 6 pp 641ndash650 2010
[36] K Dietz ldquoDensity-dependence in parasite transmissiondynamicsrdquo Parasitology Today vol 4 no 4 pp 91ndash97 1988
[37] M G Basanez J H F Remme E S Alley et al ldquoDensity-dependent processes in the transmission of human onchocerci-asis relationship between the numbers ofmicrofilariae ingestedand successful larval development in the simuliid vectorrdquoParasitology vol 110 no 4 pp 409ndash427 1995
[38] B A Boatin L Toe E S Alley N J D Nagelkerke GBorsboom and J D F Habbema ldquoDetection of Onchocercavolvulus infection in lowprevalence areas a comparison of threediagnostic methodsrdquo Parasitology vol 125 no 6 pp 545ndash5522002
[39] M Noma B E B Nwoke I Nutall et al ldquoRapid epidemio-logical mapping of onchocerciasis (REMO) its application bythe African programme for onchocerciasis control (APOC)rdquoAnnals of Tropical Medicine and Parasitology vol 96 supple-ment 1 pp S29ndashS39 2002
[40] G Fobi J R M Mbina G Ozoh et al ldquoOnchocerciasis inthe area of Lastourville Gabon Clinical and entomologicalaspectsrdquo Bulletin de la Societe de Pathologie Exotique vol 99no 4 pp 269ndash271 2006
[41] M N Katabarwa A Eyamba M Chouaibou et al ldquoDoesonchocerciasis transmission take place in hypoendemic areasa study from theNorth Region of CameroonrdquoTropicalMedicineand International Health vol 15 no 5 pp 645ndash652 2010
[42] WHO Report Certification of Elimination of Human Onchocer-ciasis Criteria and Procedures Criteria For Certification of Inter-ruption of TransmissionElimination of Human OnchocerciasisWorld Health Organization Geneva Switzerland 2001
[43] R Seidenfaden A Fischer I Bonow D Ekale V Tanya andA Renz ldquoCombined benefits of annual mass treatment withivermectin and cattle zooprophylaxis on the severity of humanonchocerciasis in northern Cameroonrdquo Tropical Medicine andInternational Health vol 6 no 9 pp 715ndash725 2001
Table 5 Comparing baseline entomological data of 1996 at two fly collection sites and three during 2011
Monthyear of black fly collection Baseline May 1996 Followup 2011Black fly collection sites Bafang (Basseu) Foumbot (Maka) Bafang Foumbot MassangamNumber of Simulium caught 5 166 5261 2856 12538Number of Simulium dissected 5 142 5261 2856 12138Number of parous flies 1 97 1502 1028 2845Parous rate () 20 683 285 36 234Number of Simulium flies infected (L1 L2 L3] 1 12 3 9 19Infection rate () 2000 845 020 088 067Number of Simulium flies infective L3 larval stage in the head 20 2 0 2 5Infective rate () 200 211 000 019 018Monthly biting rate per person 750 166000 na na naMonthly transmission potentiallowast 150 21040 na na naAnnual biting rate per person Na na 52610 28560 125380Annual transmission potential Na na 0 70 310
0
500
1000
1500
2000
2500
3000
3500
4000
No
of fl
ies c
olle
cted
BafangFoumbotMakouopsap
MarApr2011 2012
May Jun Jul AugSeptOctNovDec Jan Feb
Figure 3 Monthly seasonal biting of Simulium flies at 3 fly catchingsites in West Region
calculation ofATPTherefore collection of entomological dataover several months is required as reflected in the follow-up study The information on peak biting and transmissionpatterns could effectively be utilized for ivermectin treatmentfor maximum impact on transmission especially where theforce of transmission is considerably high if elimination ofonchocerciasis is the goal In the follow-up survey it is onlyat Bafang fly collection site that the entomological criterionfor interruption of transmission was met with an ATP of zero[42]
The present study however did not perform moleculartesting in order to determine if the L3 larvae wereO volvulusor another (animal) Onchocerca species Based on humanmf prevalence in skin and infections in children we thinkthat there is likelihood that some of the larvae observedin vectors were O volvulus However a study conducted inNorth Region of Cameroon during the 1990s showed that
33 of infective larvae in S damnosum were O volvuluswhereas 65 were O ochengi and 2 were O ramachandrini[43] It is until such a study is conducted in West Region ofCameroon that we will know the extent to which O ochengiis responsible for a significant proportion of infected flies thatcould confound the infection rate there
Our findings reflecting an observation period of 15 yearsshowed that annual mass treatment with ivermectin may notinterrupt the transmission of onchocerciasis in all differentecological zones of West Region Therefore the intensive useof ivermectin is recommended if interruption of transmissionof onchocerciasis is to be attained [1]
5 Conclusion
Annual mass treatment with ivermectin through commu-nity-directed treatment was preferred as a good and lessexpensive method for controlling onchocerciasis in endemicAfrican countries with assistance from the African Pro-gramme for Onchocerciasis Control The studies in MaliSenegal and Nigeria have shown that an annual dose ofivermectin had interrupted transmission of the disease andall interventions could be halted without the risk of diseaserecrudescence However an annual dose of ivermectin hasnot interrupted transmission after 15 years of mass treatmentin some areas in West Region of Cameroon just like inNorth region [8] It has also been less effective in someonchocerciasis endemic areas in Ghana The present paperagain highlights the fact that for interruption of onchocer-ciasis transmission feasible and different but complementarystrategic options should be adopted as elimination becomesthe goal in Africa
Acknowledgments
The investigators would like to acknowledge the staff ofMinistry of Health at the national regional and healthdistrict levels in West Region along with Carter CenterCameroon Office for mobilizing and educating selected
Journal of Parasitology Research 11
communities and providing policy and administrative sup-port The involvement of community members in selectedcommunities in mf and nodule assessments and Simulium flycollection is highly appreciated The Carter Center the LionsClubs International Foundation (LCIF) and the African Pro-gramme for onchocerciasis Control (APOC) which fundedthe CDTI activities and the surveys are also highly appreci-ated
References
[1] E W Cupp and M S Cupp ldquoShort report impact of iver-mectin community-level treatments on elimination of adultOnchocerca volvulus when individuals receive multiple treat-ments per yearrdquoThe American Journal of Tropical Medicine andHygiene vol 73 no 6 pp 1159ndash1161 2005
[2] H R Taylor M Pacque B Munoz and B M Greene ldquoImpactof mass treatment of onchocerciasis with ivermectin on thetransmission of infectionrdquo Science vol 250 no 4977 pp 116ndash118 1990
[3] G J J M Borsboom B A Boatin N J D Nagelkerkeet al ldquoImpact of ivermectin on onchocerciasis transmissionassessing the empirical evidence that repeated ivermectin masstreatmentsmay lead to eliminationeradication inWest-AfricardquoFilaria Journal vol 2 article 8 2003
[4] A D Hopkins ldquoIvermectin and onchocerciasis is it all solvedrdquoEye vol 19 no 10 pp 1057ndash1066 2005
[5] L Yameogo ldquoSpecial intervention zonesrdquo Annals of TropicalMedicine and Parasitology vol 102 supplement 1 pp 23ndash242008
[6] D H Molyneux and M N Malecela ldquoNeglected tropicaldiseases and themillennium development goals why the ldquootherdiseasesrdquo matter reality versus rhetoricrdquo Parasites amp Vectorsvol 4 2011
[7] WHOReportAcceleratingWorkToOvercome theGlobal Impactof Neglected Tropical Disease A Roadmap For Implementationvol 1211WorldHealthOrganization 20AvenueAppia GenevaSwitzerland 2012
[8] M N Katabarwa A Eyamba P Nwane et al ldquoSeventeenyears of annual distribution of ivermectin has not interruptedonchocerciasis transmission in North Region Cameroonrdquo TheAmerican Journal of Tropical Medicine and Hygiene vol 85 no6 pp 1041ndash1049 2011
[9] B A Boatin and F O Richards ldquoControl of onchocerciasisrdquoAdvances in Parasitology vol 61 pp 349ndash394 2006
[10] D R Hopkins F O Richards and M Katabarwa ldquoWhitheronchocerciasis control in Africardquo American Journal of TropicalMedicine and Hygiene vol 72 no 1 pp 1ndash2 2005
[11] L Diawara M O Traore A Badji et al ldquoFeasibilityof onchocerciasis elimination with ivermectin treatment inendemic foci in Africa first evidence from studies in Mali andSenegalrdquo PLoS Neglected Tropical Diseases vol 3 no 7 articlee497 2009
[12] F O Richards E S Miri M Katabarwa et al ldquoThe carter cen-terrsquos assistance to river blindness control programs establish-ing treatment objectives and goals for monitoring ivermectindelivery systems on two continentsrdquo The American Journal ofTropical Medicine and Hygiene vol 65 no 2 pp 108ndash114 2001
[13] P Salant and D A Dilman How to Conduct Your Own SurveyJohn Wiley amp Sons 1994
[14] M N Katabarwa P Habomugisha and F O Richards ldquoImple-menting community-directed treatmentwith ivermectin for the
control of onchocerciasis in Uganda (1997-2000) an evalua-tionrdquo Annals of Tropical Medicine and Parasitology vol 96 no1 pp 61ndash73 2002
[15] E C Emukah U Enyinnaya N S Olaniran et al ldquoFactorsaffecting the attrition of community-directed distributors ofivermectin in an onchocerciasis-control programme in the Imoand Abia states of south-eastern Nigeriardquo Annals of TropicalMedicine and Parasitology vol 102 no 1 pp 45ndash51 2008
[16] A Prost and J Prodrsquohon ldquoLe diagnostique parasitologique delrsquoonchocercose revue critique des methods en usagerdquoMedicineTropicale vol 38 pp 519ndash532 1978
[17] H Schulz Key ldquoA simple technique to assess the total number ofOnchocerca volvulusmicrofilariae in skin snipsrdquo Tropenmedizinund Parasitologie vol 29 no 1 pp 51ndash54 1978
[18] WHO Report ldquoOnchocerciasis and its control Report of aWHO Expert Committee on Onchocerciasis Controlrdquo TechRep 852 Geneva Switzerland 1995
[19] WHO Report Strategies For Ivermectin Distribution ThroughPrimaryHealth Care SystemWHOPHL91 24WHOGenevaSwitzerland 1991
[20] E J Albiez D W Buttner and B O L Duke ldquoDiagnosisand extirpation of nodules in human onchocerciasisrdquo TropicalMedicine and Parasitology vol 39 no 4 pp 331ndash346 1988
[21] P Ngoumou J F Walsh and J M Mace ldquoA rapid mappingtechnique for the prevalence and distribution of onchocerciasisa Cameroon case studyrdquo Annals of Tropical Medicine andParasitology vol 88 no 5 pp 463ndash474 1994
[22] M Katabarwa A W Onapa and B Nakileza ldquoRapid epidemi-ological mapping of onchocerciasis in areas of uganda whereSimulium neavei SL is the vectorrdquo East African Medical Journalvol 76 no 8 pp 440ndash446 1999
[23] J F Walsh J B Davies R Le Berre and R Garms ldquoStandard-ization of criteria for assessing the effect of Simulium control inonchocerciasis control programmesrdquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 72 no 6 pp 675ndash676 1978
[24] J B Davies ldquoA rapid staining and clearing technique for detect-ing filarial larvae in alcohol-preserved vectorsrdquo Transactions ofthe Royal Society of Tropical Medicine and Hygiene vol 89 no3 p 280 1995
[25] M Katabarwa P Habomugisha A Eyamba S Agunyo andC Mentou ldquoMonitoring ivermectin distributors involved inintegrated health care services through community-directedinterventionsmdasha comparison of Cameroon and Uganda expe-riences over a period of three years (2004ndash2006)rdquo TropicalMedicine and International Health vol 15 no 2 pp 216ndash2232010
[26] J Remme O Ba K Y Dadzie and M Karam ldquoA force-of-infection model for onchocerciasis and its applications inthe epidemiological evaluation of the onchocerciasis controlprogramme in the volta river basin areardquo Bulletin of the WorldHealth Organization vol 64 no 5 pp 667ndash681 1986
[27] P Barbazan H Escaffre R Mbentengam and M BoussinesqldquoEntomologic study on the transmission of onchocerciasis ina forest-savanna transition area of Cameroonrdquo Bulletin de laSociete de Pathologie Exotique vol 91 no 2 pp 178ndash182 1998
[28] E Cadot P Barbazan andM Boussinesq ldquoGeographical deter-minants of onchocerciasis transmission in a forestsavannahtransition zone two villages of the mbam focusrdquo Sante vol 8no 6 pp 429ndash435 1998
[29] K Awadzi S K Attah E T Addy et al ldquoThirty-monthfollow-up of sub-optimal responders to multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in Ghanardquo
12 Journal of Parasitology Research
Annals of Tropical Medicine and Parasitology vol 98 no 4 pp359ndash370 2004
[30] K Awadzi D A Boakye G Edwards et al ldquoAn investigationof persistent microfilaridermias despite multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in GhanardquoAnnals of Tropical Medicine and Parasitology vol 98 no 3 pp231ndash249 2004
[31] M Y Osei-Atweneboana J K Eng D A Boakye J OGyapong and R K Prichard ldquoPrevalence and intensity ofOnchocerca volvulus infection and efficacy of ivermectin inendemic communities in Ghana a two-phase epidemiologicalstudyrdquoThe Lancet vol 369 no 9578 pp 2021ndash2029 2007
[32] C Bottomley V Isham R C Collins and M G BasanezldquoRates of microfilarial production by Onchocerca volvulus arenot cumulatively reduced by multiple ivermectin treatmentsrdquoParasitology vol 135 no 13 pp 1571ndash1581 2008
[33] R Garms T L Lakwo R Ndyomugyenyi et al ldquoThe elimina-tion of the vector Simulium neavei from the Itwara onchocerci-asis focus in Uganda by ground larvicidingrdquo Acta Tropica vol111 no 3 pp 203ndash210 2009
[34] R Ndyomugyenyi E Tukesiga D W Buttner and R GarmsldquoThe impact of ivermectin treatment alone and when inparallel with Simulium neavei elimination on onchocerciasis inUgandardquo Tropical Medicine and International Health vol 9 no8 pp 882ndash886 2004
[35] H P Duerr and M Eichner ldquoEpidemiology and control ofonchocerciasis the threshold biting rate of savannah onchocer-ciasis in Africardquo International Journal for Parasitology vol 40no 6 pp 641ndash650 2010
[36] K Dietz ldquoDensity-dependence in parasite transmissiondynamicsrdquo Parasitology Today vol 4 no 4 pp 91ndash97 1988
[37] M G Basanez J H F Remme E S Alley et al ldquoDensity-dependent processes in the transmission of human onchocerci-asis relationship between the numbers ofmicrofilariae ingestedand successful larval development in the simuliid vectorrdquoParasitology vol 110 no 4 pp 409ndash427 1995
[38] B A Boatin L Toe E S Alley N J D Nagelkerke GBorsboom and J D F Habbema ldquoDetection of Onchocercavolvulus infection in lowprevalence areas a comparison of threediagnostic methodsrdquo Parasitology vol 125 no 6 pp 545ndash5522002
[39] M Noma B E B Nwoke I Nutall et al ldquoRapid epidemio-logical mapping of onchocerciasis (REMO) its application bythe African programme for onchocerciasis control (APOC)rdquoAnnals of Tropical Medicine and Parasitology vol 96 supple-ment 1 pp S29ndashS39 2002
[40] G Fobi J R M Mbina G Ozoh et al ldquoOnchocerciasis inthe area of Lastourville Gabon Clinical and entomologicalaspectsrdquo Bulletin de la Societe de Pathologie Exotique vol 99no 4 pp 269ndash271 2006
[41] M N Katabarwa A Eyamba M Chouaibou et al ldquoDoesonchocerciasis transmission take place in hypoendemic areasa study from theNorth Region of CameroonrdquoTropicalMedicineand International Health vol 15 no 5 pp 645ndash652 2010
[42] WHO Report Certification of Elimination of Human Onchocer-ciasis Criteria and Procedures Criteria For Certification of Inter-ruption of TransmissionElimination of Human OnchocerciasisWorld Health Organization Geneva Switzerland 2001
[43] R Seidenfaden A Fischer I Bonow D Ekale V Tanya andA Renz ldquoCombined benefits of annual mass treatment withivermectin and cattle zooprophylaxis on the severity of humanonchocerciasis in northern Cameroonrdquo Tropical Medicine andInternational Health vol 6 no 9 pp 715ndash725 2001
Table 5 Comparing baseline entomological data of 1996 at two fly collection sites and three during 2011
Monthyear of black fly collection Baseline May 1996 Followup 2011Black fly collection sites Bafang (Basseu) Foumbot (Maka) Bafang Foumbot MassangamNumber of Simulium caught 5 166 5261 2856 12538Number of Simulium dissected 5 142 5261 2856 12138Number of parous flies 1 97 1502 1028 2845Parous rate () 20 683 285 36 234Number of Simulium flies infected (L1 L2 L3] 1 12 3 9 19Infection rate () 2000 845 020 088 067Number of Simulium flies infective L3 larval stage in the head 20 2 0 2 5Infective rate () 200 211 000 019 018Monthly biting rate per person 750 166000 na na naMonthly transmission potentiallowast 150 21040 na na naAnnual biting rate per person Na na 52610 28560 125380Annual transmission potential Na na 0 70 310
0
500
1000
1500
2000
2500
3000
3500
4000
No
of fl
ies c
olle
cted
BafangFoumbotMakouopsap
MarApr2011 2012
May Jun Jul AugSeptOctNovDec Jan Feb
Figure 3 Monthly seasonal biting of Simulium flies at 3 fly catchingsites in West Region
calculation ofATPTherefore collection of entomological dataover several months is required as reflected in the follow-up study The information on peak biting and transmissionpatterns could effectively be utilized for ivermectin treatmentfor maximum impact on transmission especially where theforce of transmission is considerably high if elimination ofonchocerciasis is the goal In the follow-up survey it is onlyat Bafang fly collection site that the entomological criterionfor interruption of transmission was met with an ATP of zero[42]
The present study however did not perform moleculartesting in order to determine if the L3 larvae wereO volvulusor another (animal) Onchocerca species Based on humanmf prevalence in skin and infections in children we thinkthat there is likelihood that some of the larvae observedin vectors were O volvulus However a study conducted inNorth Region of Cameroon during the 1990s showed that
33 of infective larvae in S damnosum were O volvuluswhereas 65 were O ochengi and 2 were O ramachandrini[43] It is until such a study is conducted in West Region ofCameroon that we will know the extent to which O ochengiis responsible for a significant proportion of infected flies thatcould confound the infection rate there
Our findings reflecting an observation period of 15 yearsshowed that annual mass treatment with ivermectin may notinterrupt the transmission of onchocerciasis in all differentecological zones of West Region Therefore the intensive useof ivermectin is recommended if interruption of transmissionof onchocerciasis is to be attained [1]
5 Conclusion
Annual mass treatment with ivermectin through commu-nity-directed treatment was preferred as a good and lessexpensive method for controlling onchocerciasis in endemicAfrican countries with assistance from the African Pro-gramme for Onchocerciasis Control The studies in MaliSenegal and Nigeria have shown that an annual dose ofivermectin had interrupted transmission of the disease andall interventions could be halted without the risk of diseaserecrudescence However an annual dose of ivermectin hasnot interrupted transmission after 15 years of mass treatmentin some areas in West Region of Cameroon just like inNorth region [8] It has also been less effective in someonchocerciasis endemic areas in Ghana The present paperagain highlights the fact that for interruption of onchocer-ciasis transmission feasible and different but complementarystrategic options should be adopted as elimination becomesthe goal in Africa
Acknowledgments
The investigators would like to acknowledge the staff ofMinistry of Health at the national regional and healthdistrict levels in West Region along with Carter CenterCameroon Office for mobilizing and educating selected
Journal of Parasitology Research 11
communities and providing policy and administrative sup-port The involvement of community members in selectedcommunities in mf and nodule assessments and Simulium flycollection is highly appreciated The Carter Center the LionsClubs International Foundation (LCIF) and the African Pro-gramme for onchocerciasis Control (APOC) which fundedthe CDTI activities and the surveys are also highly appreci-ated
References
[1] E W Cupp and M S Cupp ldquoShort report impact of iver-mectin community-level treatments on elimination of adultOnchocerca volvulus when individuals receive multiple treat-ments per yearrdquoThe American Journal of Tropical Medicine andHygiene vol 73 no 6 pp 1159ndash1161 2005
[2] H R Taylor M Pacque B Munoz and B M Greene ldquoImpactof mass treatment of onchocerciasis with ivermectin on thetransmission of infectionrdquo Science vol 250 no 4977 pp 116ndash118 1990
[3] G J J M Borsboom B A Boatin N J D Nagelkerkeet al ldquoImpact of ivermectin on onchocerciasis transmissionassessing the empirical evidence that repeated ivermectin masstreatmentsmay lead to eliminationeradication inWest-AfricardquoFilaria Journal vol 2 article 8 2003
[4] A D Hopkins ldquoIvermectin and onchocerciasis is it all solvedrdquoEye vol 19 no 10 pp 1057ndash1066 2005
[5] L Yameogo ldquoSpecial intervention zonesrdquo Annals of TropicalMedicine and Parasitology vol 102 supplement 1 pp 23ndash242008
[6] D H Molyneux and M N Malecela ldquoNeglected tropicaldiseases and themillennium development goals why the ldquootherdiseasesrdquo matter reality versus rhetoricrdquo Parasites amp Vectorsvol 4 2011
[7] WHOReportAcceleratingWorkToOvercome theGlobal Impactof Neglected Tropical Disease A Roadmap For Implementationvol 1211WorldHealthOrganization 20AvenueAppia GenevaSwitzerland 2012
[8] M N Katabarwa A Eyamba P Nwane et al ldquoSeventeenyears of annual distribution of ivermectin has not interruptedonchocerciasis transmission in North Region Cameroonrdquo TheAmerican Journal of Tropical Medicine and Hygiene vol 85 no6 pp 1041ndash1049 2011
[9] B A Boatin and F O Richards ldquoControl of onchocerciasisrdquoAdvances in Parasitology vol 61 pp 349ndash394 2006
[10] D R Hopkins F O Richards and M Katabarwa ldquoWhitheronchocerciasis control in Africardquo American Journal of TropicalMedicine and Hygiene vol 72 no 1 pp 1ndash2 2005
[11] L Diawara M O Traore A Badji et al ldquoFeasibilityof onchocerciasis elimination with ivermectin treatment inendemic foci in Africa first evidence from studies in Mali andSenegalrdquo PLoS Neglected Tropical Diseases vol 3 no 7 articlee497 2009
[12] F O Richards E S Miri M Katabarwa et al ldquoThe carter cen-terrsquos assistance to river blindness control programs establish-ing treatment objectives and goals for monitoring ivermectindelivery systems on two continentsrdquo The American Journal ofTropical Medicine and Hygiene vol 65 no 2 pp 108ndash114 2001
[13] P Salant and D A Dilman How to Conduct Your Own SurveyJohn Wiley amp Sons 1994
[14] M N Katabarwa P Habomugisha and F O Richards ldquoImple-menting community-directed treatmentwith ivermectin for the
control of onchocerciasis in Uganda (1997-2000) an evalua-tionrdquo Annals of Tropical Medicine and Parasitology vol 96 no1 pp 61ndash73 2002
[15] E C Emukah U Enyinnaya N S Olaniran et al ldquoFactorsaffecting the attrition of community-directed distributors ofivermectin in an onchocerciasis-control programme in the Imoand Abia states of south-eastern Nigeriardquo Annals of TropicalMedicine and Parasitology vol 102 no 1 pp 45ndash51 2008
[16] A Prost and J Prodrsquohon ldquoLe diagnostique parasitologique delrsquoonchocercose revue critique des methods en usagerdquoMedicineTropicale vol 38 pp 519ndash532 1978
[17] H Schulz Key ldquoA simple technique to assess the total number ofOnchocerca volvulusmicrofilariae in skin snipsrdquo Tropenmedizinund Parasitologie vol 29 no 1 pp 51ndash54 1978
[18] WHO Report ldquoOnchocerciasis and its control Report of aWHO Expert Committee on Onchocerciasis Controlrdquo TechRep 852 Geneva Switzerland 1995
[19] WHO Report Strategies For Ivermectin Distribution ThroughPrimaryHealth Care SystemWHOPHL91 24WHOGenevaSwitzerland 1991
[20] E J Albiez D W Buttner and B O L Duke ldquoDiagnosisand extirpation of nodules in human onchocerciasisrdquo TropicalMedicine and Parasitology vol 39 no 4 pp 331ndash346 1988
[21] P Ngoumou J F Walsh and J M Mace ldquoA rapid mappingtechnique for the prevalence and distribution of onchocerciasisa Cameroon case studyrdquo Annals of Tropical Medicine andParasitology vol 88 no 5 pp 463ndash474 1994
[22] M Katabarwa A W Onapa and B Nakileza ldquoRapid epidemi-ological mapping of onchocerciasis in areas of uganda whereSimulium neavei SL is the vectorrdquo East African Medical Journalvol 76 no 8 pp 440ndash446 1999
[23] J F Walsh J B Davies R Le Berre and R Garms ldquoStandard-ization of criteria for assessing the effect of Simulium control inonchocerciasis control programmesrdquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 72 no 6 pp 675ndash676 1978
[24] J B Davies ldquoA rapid staining and clearing technique for detect-ing filarial larvae in alcohol-preserved vectorsrdquo Transactions ofthe Royal Society of Tropical Medicine and Hygiene vol 89 no3 p 280 1995
[25] M Katabarwa P Habomugisha A Eyamba S Agunyo andC Mentou ldquoMonitoring ivermectin distributors involved inintegrated health care services through community-directedinterventionsmdasha comparison of Cameroon and Uganda expe-riences over a period of three years (2004ndash2006)rdquo TropicalMedicine and International Health vol 15 no 2 pp 216ndash2232010
[26] J Remme O Ba K Y Dadzie and M Karam ldquoA force-of-infection model for onchocerciasis and its applications inthe epidemiological evaluation of the onchocerciasis controlprogramme in the volta river basin areardquo Bulletin of the WorldHealth Organization vol 64 no 5 pp 667ndash681 1986
[27] P Barbazan H Escaffre R Mbentengam and M BoussinesqldquoEntomologic study on the transmission of onchocerciasis ina forest-savanna transition area of Cameroonrdquo Bulletin de laSociete de Pathologie Exotique vol 91 no 2 pp 178ndash182 1998
[28] E Cadot P Barbazan andM Boussinesq ldquoGeographical deter-minants of onchocerciasis transmission in a forestsavannahtransition zone two villages of the mbam focusrdquo Sante vol 8no 6 pp 429ndash435 1998
[29] K Awadzi S K Attah E T Addy et al ldquoThirty-monthfollow-up of sub-optimal responders to multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in Ghanardquo
12 Journal of Parasitology Research
Annals of Tropical Medicine and Parasitology vol 98 no 4 pp359ndash370 2004
[30] K Awadzi D A Boakye G Edwards et al ldquoAn investigationof persistent microfilaridermias despite multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in GhanardquoAnnals of Tropical Medicine and Parasitology vol 98 no 3 pp231ndash249 2004
[31] M Y Osei-Atweneboana J K Eng D A Boakye J OGyapong and R K Prichard ldquoPrevalence and intensity ofOnchocerca volvulus infection and efficacy of ivermectin inendemic communities in Ghana a two-phase epidemiologicalstudyrdquoThe Lancet vol 369 no 9578 pp 2021ndash2029 2007
[32] C Bottomley V Isham R C Collins and M G BasanezldquoRates of microfilarial production by Onchocerca volvulus arenot cumulatively reduced by multiple ivermectin treatmentsrdquoParasitology vol 135 no 13 pp 1571ndash1581 2008
[33] R Garms T L Lakwo R Ndyomugyenyi et al ldquoThe elimina-tion of the vector Simulium neavei from the Itwara onchocerci-asis focus in Uganda by ground larvicidingrdquo Acta Tropica vol111 no 3 pp 203ndash210 2009
[34] R Ndyomugyenyi E Tukesiga D W Buttner and R GarmsldquoThe impact of ivermectin treatment alone and when inparallel with Simulium neavei elimination on onchocerciasis inUgandardquo Tropical Medicine and International Health vol 9 no8 pp 882ndash886 2004
[35] H P Duerr and M Eichner ldquoEpidemiology and control ofonchocerciasis the threshold biting rate of savannah onchocer-ciasis in Africardquo International Journal for Parasitology vol 40no 6 pp 641ndash650 2010
[36] K Dietz ldquoDensity-dependence in parasite transmissiondynamicsrdquo Parasitology Today vol 4 no 4 pp 91ndash97 1988
[37] M G Basanez J H F Remme E S Alley et al ldquoDensity-dependent processes in the transmission of human onchocerci-asis relationship between the numbers ofmicrofilariae ingestedand successful larval development in the simuliid vectorrdquoParasitology vol 110 no 4 pp 409ndash427 1995
[38] B A Boatin L Toe E S Alley N J D Nagelkerke GBorsboom and J D F Habbema ldquoDetection of Onchocercavolvulus infection in lowprevalence areas a comparison of threediagnostic methodsrdquo Parasitology vol 125 no 6 pp 545ndash5522002
[39] M Noma B E B Nwoke I Nutall et al ldquoRapid epidemio-logical mapping of onchocerciasis (REMO) its application bythe African programme for onchocerciasis control (APOC)rdquoAnnals of Tropical Medicine and Parasitology vol 96 supple-ment 1 pp S29ndashS39 2002
[40] G Fobi J R M Mbina G Ozoh et al ldquoOnchocerciasis inthe area of Lastourville Gabon Clinical and entomologicalaspectsrdquo Bulletin de la Societe de Pathologie Exotique vol 99no 4 pp 269ndash271 2006
[41] M N Katabarwa A Eyamba M Chouaibou et al ldquoDoesonchocerciasis transmission take place in hypoendemic areasa study from theNorth Region of CameroonrdquoTropicalMedicineand International Health vol 15 no 5 pp 645ndash652 2010
[42] WHO Report Certification of Elimination of Human Onchocer-ciasis Criteria and Procedures Criteria For Certification of Inter-ruption of TransmissionElimination of Human OnchocerciasisWorld Health Organization Geneva Switzerland 2001
[43] R Seidenfaden A Fischer I Bonow D Ekale V Tanya andA Renz ldquoCombined benefits of annual mass treatment withivermectin and cattle zooprophylaxis on the severity of humanonchocerciasis in northern Cameroonrdquo Tropical Medicine andInternational Health vol 6 no 9 pp 715ndash725 2001
Table 5 Comparing baseline entomological data of 1996 at two fly collection sites and three during 2011
Monthyear of black fly collection Baseline May 1996 Followup 2011Black fly collection sites Bafang (Basseu) Foumbot (Maka) Bafang Foumbot MassangamNumber of Simulium caught 5 166 5261 2856 12538Number of Simulium dissected 5 142 5261 2856 12138Number of parous flies 1 97 1502 1028 2845Parous rate () 20 683 285 36 234Number of Simulium flies infected (L1 L2 L3] 1 12 3 9 19Infection rate () 2000 845 020 088 067Number of Simulium flies infective L3 larval stage in the head 20 2 0 2 5Infective rate () 200 211 000 019 018Monthly biting rate per person 750 166000 na na naMonthly transmission potentiallowast 150 21040 na na naAnnual biting rate per person Na na 52610 28560 125380Annual transmission potential Na na 0 70 310
0
500
1000
1500
2000
2500
3000
3500
4000
No
of fl
ies c
olle
cted
BafangFoumbotMakouopsap
MarApr2011 2012
May Jun Jul AugSeptOctNovDec Jan Feb
Figure 3 Monthly seasonal biting of Simulium flies at 3 fly catchingsites in West Region
calculation ofATPTherefore collection of entomological dataover several months is required as reflected in the follow-up study The information on peak biting and transmissionpatterns could effectively be utilized for ivermectin treatmentfor maximum impact on transmission especially where theforce of transmission is considerably high if elimination ofonchocerciasis is the goal In the follow-up survey it is onlyat Bafang fly collection site that the entomological criterionfor interruption of transmission was met with an ATP of zero[42]
The present study however did not perform moleculartesting in order to determine if the L3 larvae wereO volvulusor another (animal) Onchocerca species Based on humanmf prevalence in skin and infections in children we thinkthat there is likelihood that some of the larvae observedin vectors were O volvulus However a study conducted inNorth Region of Cameroon during the 1990s showed that
33 of infective larvae in S damnosum were O volvuluswhereas 65 were O ochengi and 2 were O ramachandrini[43] It is until such a study is conducted in West Region ofCameroon that we will know the extent to which O ochengiis responsible for a significant proportion of infected flies thatcould confound the infection rate there
Our findings reflecting an observation period of 15 yearsshowed that annual mass treatment with ivermectin may notinterrupt the transmission of onchocerciasis in all differentecological zones of West Region Therefore the intensive useof ivermectin is recommended if interruption of transmissionof onchocerciasis is to be attained [1]
5 Conclusion
Annual mass treatment with ivermectin through commu-nity-directed treatment was preferred as a good and lessexpensive method for controlling onchocerciasis in endemicAfrican countries with assistance from the African Pro-gramme for Onchocerciasis Control The studies in MaliSenegal and Nigeria have shown that an annual dose ofivermectin had interrupted transmission of the disease andall interventions could be halted without the risk of diseaserecrudescence However an annual dose of ivermectin hasnot interrupted transmission after 15 years of mass treatmentin some areas in West Region of Cameroon just like inNorth region [8] It has also been less effective in someonchocerciasis endemic areas in Ghana The present paperagain highlights the fact that for interruption of onchocer-ciasis transmission feasible and different but complementarystrategic options should be adopted as elimination becomesthe goal in Africa
Acknowledgments
The investigators would like to acknowledge the staff ofMinistry of Health at the national regional and healthdistrict levels in West Region along with Carter CenterCameroon Office for mobilizing and educating selected
Journal of Parasitology Research 11
communities and providing policy and administrative sup-port The involvement of community members in selectedcommunities in mf and nodule assessments and Simulium flycollection is highly appreciated The Carter Center the LionsClubs International Foundation (LCIF) and the African Pro-gramme for onchocerciasis Control (APOC) which fundedthe CDTI activities and the surveys are also highly appreci-ated
References
[1] E W Cupp and M S Cupp ldquoShort report impact of iver-mectin community-level treatments on elimination of adultOnchocerca volvulus when individuals receive multiple treat-ments per yearrdquoThe American Journal of Tropical Medicine andHygiene vol 73 no 6 pp 1159ndash1161 2005
[2] H R Taylor M Pacque B Munoz and B M Greene ldquoImpactof mass treatment of onchocerciasis with ivermectin on thetransmission of infectionrdquo Science vol 250 no 4977 pp 116ndash118 1990
[3] G J J M Borsboom B A Boatin N J D Nagelkerkeet al ldquoImpact of ivermectin on onchocerciasis transmissionassessing the empirical evidence that repeated ivermectin masstreatmentsmay lead to eliminationeradication inWest-AfricardquoFilaria Journal vol 2 article 8 2003
[4] A D Hopkins ldquoIvermectin and onchocerciasis is it all solvedrdquoEye vol 19 no 10 pp 1057ndash1066 2005
[5] L Yameogo ldquoSpecial intervention zonesrdquo Annals of TropicalMedicine and Parasitology vol 102 supplement 1 pp 23ndash242008
[6] D H Molyneux and M N Malecela ldquoNeglected tropicaldiseases and themillennium development goals why the ldquootherdiseasesrdquo matter reality versus rhetoricrdquo Parasites amp Vectorsvol 4 2011
[7] WHOReportAcceleratingWorkToOvercome theGlobal Impactof Neglected Tropical Disease A Roadmap For Implementationvol 1211WorldHealthOrganization 20AvenueAppia GenevaSwitzerland 2012
[8] M N Katabarwa A Eyamba P Nwane et al ldquoSeventeenyears of annual distribution of ivermectin has not interruptedonchocerciasis transmission in North Region Cameroonrdquo TheAmerican Journal of Tropical Medicine and Hygiene vol 85 no6 pp 1041ndash1049 2011
[9] B A Boatin and F O Richards ldquoControl of onchocerciasisrdquoAdvances in Parasitology vol 61 pp 349ndash394 2006
[10] D R Hopkins F O Richards and M Katabarwa ldquoWhitheronchocerciasis control in Africardquo American Journal of TropicalMedicine and Hygiene vol 72 no 1 pp 1ndash2 2005
[11] L Diawara M O Traore A Badji et al ldquoFeasibilityof onchocerciasis elimination with ivermectin treatment inendemic foci in Africa first evidence from studies in Mali andSenegalrdquo PLoS Neglected Tropical Diseases vol 3 no 7 articlee497 2009
[12] F O Richards E S Miri M Katabarwa et al ldquoThe carter cen-terrsquos assistance to river blindness control programs establish-ing treatment objectives and goals for monitoring ivermectindelivery systems on two continentsrdquo The American Journal ofTropical Medicine and Hygiene vol 65 no 2 pp 108ndash114 2001
[13] P Salant and D A Dilman How to Conduct Your Own SurveyJohn Wiley amp Sons 1994
[14] M N Katabarwa P Habomugisha and F O Richards ldquoImple-menting community-directed treatmentwith ivermectin for the
control of onchocerciasis in Uganda (1997-2000) an evalua-tionrdquo Annals of Tropical Medicine and Parasitology vol 96 no1 pp 61ndash73 2002
[15] E C Emukah U Enyinnaya N S Olaniran et al ldquoFactorsaffecting the attrition of community-directed distributors ofivermectin in an onchocerciasis-control programme in the Imoand Abia states of south-eastern Nigeriardquo Annals of TropicalMedicine and Parasitology vol 102 no 1 pp 45ndash51 2008
[16] A Prost and J Prodrsquohon ldquoLe diagnostique parasitologique delrsquoonchocercose revue critique des methods en usagerdquoMedicineTropicale vol 38 pp 519ndash532 1978
[17] H Schulz Key ldquoA simple technique to assess the total number ofOnchocerca volvulusmicrofilariae in skin snipsrdquo Tropenmedizinund Parasitologie vol 29 no 1 pp 51ndash54 1978
[18] WHO Report ldquoOnchocerciasis and its control Report of aWHO Expert Committee on Onchocerciasis Controlrdquo TechRep 852 Geneva Switzerland 1995
[19] WHO Report Strategies For Ivermectin Distribution ThroughPrimaryHealth Care SystemWHOPHL91 24WHOGenevaSwitzerland 1991
[20] E J Albiez D W Buttner and B O L Duke ldquoDiagnosisand extirpation of nodules in human onchocerciasisrdquo TropicalMedicine and Parasitology vol 39 no 4 pp 331ndash346 1988
[21] P Ngoumou J F Walsh and J M Mace ldquoA rapid mappingtechnique for the prevalence and distribution of onchocerciasisa Cameroon case studyrdquo Annals of Tropical Medicine andParasitology vol 88 no 5 pp 463ndash474 1994
[22] M Katabarwa A W Onapa and B Nakileza ldquoRapid epidemi-ological mapping of onchocerciasis in areas of uganda whereSimulium neavei SL is the vectorrdquo East African Medical Journalvol 76 no 8 pp 440ndash446 1999
[23] J F Walsh J B Davies R Le Berre and R Garms ldquoStandard-ization of criteria for assessing the effect of Simulium control inonchocerciasis control programmesrdquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 72 no 6 pp 675ndash676 1978
[24] J B Davies ldquoA rapid staining and clearing technique for detect-ing filarial larvae in alcohol-preserved vectorsrdquo Transactions ofthe Royal Society of Tropical Medicine and Hygiene vol 89 no3 p 280 1995
[25] M Katabarwa P Habomugisha A Eyamba S Agunyo andC Mentou ldquoMonitoring ivermectin distributors involved inintegrated health care services through community-directedinterventionsmdasha comparison of Cameroon and Uganda expe-riences over a period of three years (2004ndash2006)rdquo TropicalMedicine and International Health vol 15 no 2 pp 216ndash2232010
[26] J Remme O Ba K Y Dadzie and M Karam ldquoA force-of-infection model for onchocerciasis and its applications inthe epidemiological evaluation of the onchocerciasis controlprogramme in the volta river basin areardquo Bulletin of the WorldHealth Organization vol 64 no 5 pp 667ndash681 1986
[27] P Barbazan H Escaffre R Mbentengam and M BoussinesqldquoEntomologic study on the transmission of onchocerciasis ina forest-savanna transition area of Cameroonrdquo Bulletin de laSociete de Pathologie Exotique vol 91 no 2 pp 178ndash182 1998
[28] E Cadot P Barbazan andM Boussinesq ldquoGeographical deter-minants of onchocerciasis transmission in a forestsavannahtransition zone two villages of the mbam focusrdquo Sante vol 8no 6 pp 429ndash435 1998
[29] K Awadzi S K Attah E T Addy et al ldquoThirty-monthfollow-up of sub-optimal responders to multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in Ghanardquo
12 Journal of Parasitology Research
Annals of Tropical Medicine and Parasitology vol 98 no 4 pp359ndash370 2004
[30] K Awadzi D A Boakye G Edwards et al ldquoAn investigationof persistent microfilaridermias despite multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in GhanardquoAnnals of Tropical Medicine and Parasitology vol 98 no 3 pp231ndash249 2004
[31] M Y Osei-Atweneboana J K Eng D A Boakye J OGyapong and R K Prichard ldquoPrevalence and intensity ofOnchocerca volvulus infection and efficacy of ivermectin inendemic communities in Ghana a two-phase epidemiologicalstudyrdquoThe Lancet vol 369 no 9578 pp 2021ndash2029 2007
[32] C Bottomley V Isham R C Collins and M G BasanezldquoRates of microfilarial production by Onchocerca volvulus arenot cumulatively reduced by multiple ivermectin treatmentsrdquoParasitology vol 135 no 13 pp 1571ndash1581 2008
[33] R Garms T L Lakwo R Ndyomugyenyi et al ldquoThe elimina-tion of the vector Simulium neavei from the Itwara onchocerci-asis focus in Uganda by ground larvicidingrdquo Acta Tropica vol111 no 3 pp 203ndash210 2009
[34] R Ndyomugyenyi E Tukesiga D W Buttner and R GarmsldquoThe impact of ivermectin treatment alone and when inparallel with Simulium neavei elimination on onchocerciasis inUgandardquo Tropical Medicine and International Health vol 9 no8 pp 882ndash886 2004
[35] H P Duerr and M Eichner ldquoEpidemiology and control ofonchocerciasis the threshold biting rate of savannah onchocer-ciasis in Africardquo International Journal for Parasitology vol 40no 6 pp 641ndash650 2010
[36] K Dietz ldquoDensity-dependence in parasite transmissiondynamicsrdquo Parasitology Today vol 4 no 4 pp 91ndash97 1988
[37] M G Basanez J H F Remme E S Alley et al ldquoDensity-dependent processes in the transmission of human onchocerci-asis relationship between the numbers ofmicrofilariae ingestedand successful larval development in the simuliid vectorrdquoParasitology vol 110 no 4 pp 409ndash427 1995
[38] B A Boatin L Toe E S Alley N J D Nagelkerke GBorsboom and J D F Habbema ldquoDetection of Onchocercavolvulus infection in lowprevalence areas a comparison of threediagnostic methodsrdquo Parasitology vol 125 no 6 pp 545ndash5522002
[39] M Noma B E B Nwoke I Nutall et al ldquoRapid epidemio-logical mapping of onchocerciasis (REMO) its application bythe African programme for onchocerciasis control (APOC)rdquoAnnals of Tropical Medicine and Parasitology vol 96 supple-ment 1 pp S29ndashS39 2002
[40] G Fobi J R M Mbina G Ozoh et al ldquoOnchocerciasis inthe area of Lastourville Gabon Clinical and entomologicalaspectsrdquo Bulletin de la Societe de Pathologie Exotique vol 99no 4 pp 269ndash271 2006
[41] M N Katabarwa A Eyamba M Chouaibou et al ldquoDoesonchocerciasis transmission take place in hypoendemic areasa study from theNorth Region of CameroonrdquoTropicalMedicineand International Health vol 15 no 5 pp 645ndash652 2010
[42] WHO Report Certification of Elimination of Human Onchocer-ciasis Criteria and Procedures Criteria For Certification of Inter-ruption of TransmissionElimination of Human OnchocerciasisWorld Health Organization Geneva Switzerland 2001
[43] R Seidenfaden A Fischer I Bonow D Ekale V Tanya andA Renz ldquoCombined benefits of annual mass treatment withivermectin and cattle zooprophylaxis on the severity of humanonchocerciasis in northern Cameroonrdquo Tropical Medicine andInternational Health vol 6 no 9 pp 715ndash725 2001
communities and providing policy and administrative sup-port The involvement of community members in selectedcommunities in mf and nodule assessments and Simulium flycollection is highly appreciated The Carter Center the LionsClubs International Foundation (LCIF) and the African Pro-gramme for onchocerciasis Control (APOC) which fundedthe CDTI activities and the surveys are also highly appreci-ated
References
[1] E W Cupp and M S Cupp ldquoShort report impact of iver-mectin community-level treatments on elimination of adultOnchocerca volvulus when individuals receive multiple treat-ments per yearrdquoThe American Journal of Tropical Medicine andHygiene vol 73 no 6 pp 1159ndash1161 2005
[2] H R Taylor M Pacque B Munoz and B M Greene ldquoImpactof mass treatment of onchocerciasis with ivermectin on thetransmission of infectionrdquo Science vol 250 no 4977 pp 116ndash118 1990
[3] G J J M Borsboom B A Boatin N J D Nagelkerkeet al ldquoImpact of ivermectin on onchocerciasis transmissionassessing the empirical evidence that repeated ivermectin masstreatmentsmay lead to eliminationeradication inWest-AfricardquoFilaria Journal vol 2 article 8 2003
[4] A D Hopkins ldquoIvermectin and onchocerciasis is it all solvedrdquoEye vol 19 no 10 pp 1057ndash1066 2005
[5] L Yameogo ldquoSpecial intervention zonesrdquo Annals of TropicalMedicine and Parasitology vol 102 supplement 1 pp 23ndash242008
[6] D H Molyneux and M N Malecela ldquoNeglected tropicaldiseases and themillennium development goals why the ldquootherdiseasesrdquo matter reality versus rhetoricrdquo Parasites amp Vectorsvol 4 2011
[7] WHOReportAcceleratingWorkToOvercome theGlobal Impactof Neglected Tropical Disease A Roadmap For Implementationvol 1211WorldHealthOrganization 20AvenueAppia GenevaSwitzerland 2012
[8] M N Katabarwa A Eyamba P Nwane et al ldquoSeventeenyears of annual distribution of ivermectin has not interruptedonchocerciasis transmission in North Region Cameroonrdquo TheAmerican Journal of Tropical Medicine and Hygiene vol 85 no6 pp 1041ndash1049 2011
[9] B A Boatin and F O Richards ldquoControl of onchocerciasisrdquoAdvances in Parasitology vol 61 pp 349ndash394 2006
[10] D R Hopkins F O Richards and M Katabarwa ldquoWhitheronchocerciasis control in Africardquo American Journal of TropicalMedicine and Hygiene vol 72 no 1 pp 1ndash2 2005
[11] L Diawara M O Traore A Badji et al ldquoFeasibilityof onchocerciasis elimination with ivermectin treatment inendemic foci in Africa first evidence from studies in Mali andSenegalrdquo PLoS Neglected Tropical Diseases vol 3 no 7 articlee497 2009
[12] F O Richards E S Miri M Katabarwa et al ldquoThe carter cen-terrsquos assistance to river blindness control programs establish-ing treatment objectives and goals for monitoring ivermectindelivery systems on two continentsrdquo The American Journal ofTropical Medicine and Hygiene vol 65 no 2 pp 108ndash114 2001
[13] P Salant and D A Dilman How to Conduct Your Own SurveyJohn Wiley amp Sons 1994
[14] M N Katabarwa P Habomugisha and F O Richards ldquoImple-menting community-directed treatmentwith ivermectin for the
control of onchocerciasis in Uganda (1997-2000) an evalua-tionrdquo Annals of Tropical Medicine and Parasitology vol 96 no1 pp 61ndash73 2002
[15] E C Emukah U Enyinnaya N S Olaniran et al ldquoFactorsaffecting the attrition of community-directed distributors ofivermectin in an onchocerciasis-control programme in the Imoand Abia states of south-eastern Nigeriardquo Annals of TropicalMedicine and Parasitology vol 102 no 1 pp 45ndash51 2008
[16] A Prost and J Prodrsquohon ldquoLe diagnostique parasitologique delrsquoonchocercose revue critique des methods en usagerdquoMedicineTropicale vol 38 pp 519ndash532 1978
[17] H Schulz Key ldquoA simple technique to assess the total number ofOnchocerca volvulusmicrofilariae in skin snipsrdquo Tropenmedizinund Parasitologie vol 29 no 1 pp 51ndash54 1978
[18] WHO Report ldquoOnchocerciasis and its control Report of aWHO Expert Committee on Onchocerciasis Controlrdquo TechRep 852 Geneva Switzerland 1995
[19] WHO Report Strategies For Ivermectin Distribution ThroughPrimaryHealth Care SystemWHOPHL91 24WHOGenevaSwitzerland 1991
[20] E J Albiez D W Buttner and B O L Duke ldquoDiagnosisand extirpation of nodules in human onchocerciasisrdquo TropicalMedicine and Parasitology vol 39 no 4 pp 331ndash346 1988
[21] P Ngoumou J F Walsh and J M Mace ldquoA rapid mappingtechnique for the prevalence and distribution of onchocerciasisa Cameroon case studyrdquo Annals of Tropical Medicine andParasitology vol 88 no 5 pp 463ndash474 1994
[22] M Katabarwa A W Onapa and B Nakileza ldquoRapid epidemi-ological mapping of onchocerciasis in areas of uganda whereSimulium neavei SL is the vectorrdquo East African Medical Journalvol 76 no 8 pp 440ndash446 1999
[23] J F Walsh J B Davies R Le Berre and R Garms ldquoStandard-ization of criteria for assessing the effect of Simulium control inonchocerciasis control programmesrdquo Transactions of the RoyalSociety of Tropical Medicine and Hygiene vol 72 no 6 pp 675ndash676 1978
[24] J B Davies ldquoA rapid staining and clearing technique for detect-ing filarial larvae in alcohol-preserved vectorsrdquo Transactions ofthe Royal Society of Tropical Medicine and Hygiene vol 89 no3 p 280 1995
[25] M Katabarwa P Habomugisha A Eyamba S Agunyo andC Mentou ldquoMonitoring ivermectin distributors involved inintegrated health care services through community-directedinterventionsmdasha comparison of Cameroon and Uganda expe-riences over a period of three years (2004ndash2006)rdquo TropicalMedicine and International Health vol 15 no 2 pp 216ndash2232010
[26] J Remme O Ba K Y Dadzie and M Karam ldquoA force-of-infection model for onchocerciasis and its applications inthe epidemiological evaluation of the onchocerciasis controlprogramme in the volta river basin areardquo Bulletin of the WorldHealth Organization vol 64 no 5 pp 667ndash681 1986
[27] P Barbazan H Escaffre R Mbentengam and M BoussinesqldquoEntomologic study on the transmission of onchocerciasis ina forest-savanna transition area of Cameroonrdquo Bulletin de laSociete de Pathologie Exotique vol 91 no 2 pp 178ndash182 1998
[28] E Cadot P Barbazan andM Boussinesq ldquoGeographical deter-minants of onchocerciasis transmission in a forestsavannahtransition zone two villages of the mbam focusrdquo Sante vol 8no 6 pp 429ndash435 1998
[29] K Awadzi S K Attah E T Addy et al ldquoThirty-monthfollow-up of sub-optimal responders to multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in Ghanardquo
12 Journal of Parasitology Research
Annals of Tropical Medicine and Parasitology vol 98 no 4 pp359ndash370 2004
[30] K Awadzi D A Boakye G Edwards et al ldquoAn investigationof persistent microfilaridermias despite multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in GhanardquoAnnals of Tropical Medicine and Parasitology vol 98 no 3 pp231ndash249 2004
[31] M Y Osei-Atweneboana J K Eng D A Boakye J OGyapong and R K Prichard ldquoPrevalence and intensity ofOnchocerca volvulus infection and efficacy of ivermectin inendemic communities in Ghana a two-phase epidemiologicalstudyrdquoThe Lancet vol 369 no 9578 pp 2021ndash2029 2007
[32] C Bottomley V Isham R C Collins and M G BasanezldquoRates of microfilarial production by Onchocerca volvulus arenot cumulatively reduced by multiple ivermectin treatmentsrdquoParasitology vol 135 no 13 pp 1571ndash1581 2008
[33] R Garms T L Lakwo R Ndyomugyenyi et al ldquoThe elimina-tion of the vector Simulium neavei from the Itwara onchocerci-asis focus in Uganda by ground larvicidingrdquo Acta Tropica vol111 no 3 pp 203ndash210 2009
[34] R Ndyomugyenyi E Tukesiga D W Buttner and R GarmsldquoThe impact of ivermectin treatment alone and when inparallel with Simulium neavei elimination on onchocerciasis inUgandardquo Tropical Medicine and International Health vol 9 no8 pp 882ndash886 2004
[35] H P Duerr and M Eichner ldquoEpidemiology and control ofonchocerciasis the threshold biting rate of savannah onchocer-ciasis in Africardquo International Journal for Parasitology vol 40no 6 pp 641ndash650 2010
[36] K Dietz ldquoDensity-dependence in parasite transmissiondynamicsrdquo Parasitology Today vol 4 no 4 pp 91ndash97 1988
[37] M G Basanez J H F Remme E S Alley et al ldquoDensity-dependent processes in the transmission of human onchocerci-asis relationship between the numbers ofmicrofilariae ingestedand successful larval development in the simuliid vectorrdquoParasitology vol 110 no 4 pp 409ndash427 1995
[38] B A Boatin L Toe E S Alley N J D Nagelkerke GBorsboom and J D F Habbema ldquoDetection of Onchocercavolvulus infection in lowprevalence areas a comparison of threediagnostic methodsrdquo Parasitology vol 125 no 6 pp 545ndash5522002
[39] M Noma B E B Nwoke I Nutall et al ldquoRapid epidemio-logical mapping of onchocerciasis (REMO) its application bythe African programme for onchocerciasis control (APOC)rdquoAnnals of Tropical Medicine and Parasitology vol 96 supple-ment 1 pp S29ndashS39 2002
[40] G Fobi J R M Mbina G Ozoh et al ldquoOnchocerciasis inthe area of Lastourville Gabon Clinical and entomologicalaspectsrdquo Bulletin de la Societe de Pathologie Exotique vol 99no 4 pp 269ndash271 2006
[41] M N Katabarwa A Eyamba M Chouaibou et al ldquoDoesonchocerciasis transmission take place in hypoendemic areasa study from theNorth Region of CameroonrdquoTropicalMedicineand International Health vol 15 no 5 pp 645ndash652 2010
[42] WHO Report Certification of Elimination of Human Onchocer-ciasis Criteria and Procedures Criteria For Certification of Inter-ruption of TransmissionElimination of Human OnchocerciasisWorld Health Organization Geneva Switzerland 2001
[43] R Seidenfaden A Fischer I Bonow D Ekale V Tanya andA Renz ldquoCombined benefits of annual mass treatment withivermectin and cattle zooprophylaxis on the severity of humanonchocerciasis in northern Cameroonrdquo Tropical Medicine andInternational Health vol 6 no 9 pp 715ndash725 2001
Annals of Tropical Medicine and Parasitology vol 98 no 4 pp359ndash370 2004
[30] K Awadzi D A Boakye G Edwards et al ldquoAn investigationof persistent microfilaridermias despite multiple treatmentswith ivermectin in two onchocerciasis-endemic foci in GhanardquoAnnals of Tropical Medicine and Parasitology vol 98 no 3 pp231ndash249 2004
[31] M Y Osei-Atweneboana J K Eng D A Boakye J OGyapong and R K Prichard ldquoPrevalence and intensity ofOnchocerca volvulus infection and efficacy of ivermectin inendemic communities in Ghana a two-phase epidemiologicalstudyrdquoThe Lancet vol 369 no 9578 pp 2021ndash2029 2007
[32] C Bottomley V Isham R C Collins and M G BasanezldquoRates of microfilarial production by Onchocerca volvulus arenot cumulatively reduced by multiple ivermectin treatmentsrdquoParasitology vol 135 no 13 pp 1571ndash1581 2008
[33] R Garms T L Lakwo R Ndyomugyenyi et al ldquoThe elimina-tion of the vector Simulium neavei from the Itwara onchocerci-asis focus in Uganda by ground larvicidingrdquo Acta Tropica vol111 no 3 pp 203ndash210 2009
[34] R Ndyomugyenyi E Tukesiga D W Buttner and R GarmsldquoThe impact of ivermectin treatment alone and when inparallel with Simulium neavei elimination on onchocerciasis inUgandardquo Tropical Medicine and International Health vol 9 no8 pp 882ndash886 2004
[35] H P Duerr and M Eichner ldquoEpidemiology and control ofonchocerciasis the threshold biting rate of savannah onchocer-ciasis in Africardquo International Journal for Parasitology vol 40no 6 pp 641ndash650 2010
[36] K Dietz ldquoDensity-dependence in parasite transmissiondynamicsrdquo Parasitology Today vol 4 no 4 pp 91ndash97 1988
[37] M G Basanez J H F Remme E S Alley et al ldquoDensity-dependent processes in the transmission of human onchocerci-asis relationship between the numbers ofmicrofilariae ingestedand successful larval development in the simuliid vectorrdquoParasitology vol 110 no 4 pp 409ndash427 1995
[38] B A Boatin L Toe E S Alley N J D Nagelkerke GBorsboom and J D F Habbema ldquoDetection of Onchocercavolvulus infection in lowprevalence areas a comparison of threediagnostic methodsrdquo Parasitology vol 125 no 6 pp 545ndash5522002
[39] M Noma B E B Nwoke I Nutall et al ldquoRapid epidemio-logical mapping of onchocerciasis (REMO) its application bythe African programme for onchocerciasis control (APOC)rdquoAnnals of Tropical Medicine and Parasitology vol 96 supple-ment 1 pp S29ndashS39 2002
[40] G Fobi J R M Mbina G Ozoh et al ldquoOnchocerciasis inthe area of Lastourville Gabon Clinical and entomologicalaspectsrdquo Bulletin de la Societe de Pathologie Exotique vol 99no 4 pp 269ndash271 2006
[41] M N Katabarwa A Eyamba M Chouaibou et al ldquoDoesonchocerciasis transmission take place in hypoendemic areasa study from theNorth Region of CameroonrdquoTropicalMedicineand International Health vol 15 no 5 pp 645ndash652 2010
[42] WHO Report Certification of Elimination of Human Onchocer-ciasis Criteria and Procedures Criteria For Certification of Inter-ruption of TransmissionElimination of Human OnchocerciasisWorld Health Organization Geneva Switzerland 2001
[43] R Seidenfaden A Fischer I Bonow D Ekale V Tanya andA Renz ldquoCombined benefits of annual mass treatment withivermectin and cattle zooprophylaxis on the severity of humanonchocerciasis in northern Cameroonrdquo Tropical Medicine andInternational Health vol 6 no 9 pp 715ndash725 2001
