Research ArticleCoinfection with Schistosoma haematobium and Plasmodiumfalciparum and Anaemia Severity among Pregnant Women inMunyenge Mount Cameroon Area A Cross-Sectional Study
Judith K Anchang-Kimbi1 Dillys Mansoh Elad1
Gemain Taiwe Sotoing1 and Eric Akum Achidi2
1Department of Zoology and Animal Physiology University of Buea Buea 63 Cameroon2Department of Biochemistry and Molecular Biology University of Buea Buea 63 Cameroon
Correspondence should be addressed to Judith K Anchang-Kimbi kuoh2000yahoofr
Received 4 August 2016 Revised 24 October 2016 Accepted 30 November 2016 Published 11 January 2017
Academic Editor D S Lindsay
Copyright copy 2017 Judith K Anchang-Kimbi et al This is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited
Background Malaria and urogenital schistosomiasis are coendemic in Mount Cameroon Area This study investigated theprevalence of S haematobium P falciparum and coinfections and their effect on anaemia in pregnancyMethods Pregnant womenreporting for antenatal care (ANC) clinic visit in Munyenge were enrolled S haematobium and P falciparum infections weredetermined by urine filtration andmicroscopy respectively Haemoglobin (Hb) levels weremeasured using haemoglobinometer Of250 women 468 392 and 152 had S haematobium P falciparum and coinfections respectively Schistosomes infection washigher in younger women (le25 years) and those who bathe in and had domestic contact with stream compared with older age (gt25years) women and those who had only domestic contact with stream Lower infection rate was associated with less water contact(le2 timesday) compared with more water contact (gt2 timesday) Compared with no sulphadoxine-pyrimethamine (SP) usagemalaria parasitaemia was less among women who used SP Stream usage increased risk of coinfection while less water contact andSP usage decreased its risk All coinfected cases were anaemic and coinfection accounted for 938 of severe anaemia ConclusionCoinfection contributes to anaemia severity Less water contact and SP usage will reduce coinfection in pregnancy in Munyenge
1 Background
Malaria parasite and helminth infections are the most preva-lent parasitic diseases in developing countries and their epi-demiologic coexistence is frequently observed particularlyin Africa [1] The overlap of malaria parasite and helminthinfections is influenced by high frequencies of the parasitesin the same population similar geographical distribution ofparasites shared risk factors common transmission meth-ods [1] and genetic and immunological predisposition [2]Findings from epidemiological studies suggest that interac-tions between malaria parasite and helminth infections canbe antagonistic [3 4] or synergistic [5 6] Some studieshave proposed an immunologic hypothesis based upon thetype T cell response (Th1 or Th2) induced by each para-site [2 7] Synergistic T cell responses could decrease the
pathological impact of the infections whereas antagonisticT cell responses could exacerbate disease Coinfection mayhave considerable health consequences leading to moresevere clinical symptoms and pathology than infection withsingle parasite species [8 9] For example coinfections ofPlasmodium falciparum with hookworms and schistosomestend to exacerbate hepatosplenic anaemia and malnutritionmorbidities [8]
Plasmodium falciparum inflicts the greatest burden andabout 90 of the populations infected with malaria live insub-SaharanAfrica Pregnant women are particularly vulner-able to P falciparum especially in first pregnancy [10] andprotective interventions against malaria include intermit-tent preventive treatment with sulphadoxine-pyrimethamine(IPTp-SP) and use of insecticide treated bed nets (ITNs)[11] Besides malaria schistosomiasis is the second important
HindawiJournal of Parasitology ResearchVolume 2017 Article ID 6173465 12 pageshttpsdoiorg10115520176173465
2 Journal of Parasitology Research
parasitic disease in terms of socioeconomic and publichealth importance [12] More than 90 of the roughly 200million cases of schistosomiasis occur in Africa [13] of whichapproximately two-thirds are caused by Schistosoma haema-tobium [14] the etiologic agent of urogenital schistosomiasisSchistosomiasis is endemic in rural areas where there is a lackof safe water supply poverty ignorance and poor hygienicpractices [15] Forty million women of child bearing age areinfected with younger and pregnant women being at greaterrisk of infection [16 17] Domestic activities such as washingclothes and fetching water in infected water expose womenand children to infection [18] In Cameroon schistosomiasisis endemic in the northern regions [19] Centre East West[20] Littoral North West South and Southwest Regions[21] Urogenital schistosomiasis is endemic in SouthwesternCameroon where Barombi Kotto [22] and Munyenge [23]are identified transmission foci While most of these studieshave focused on school-age children and the communityepidemiological data on the prevalence of urogenital schis-tosomiasis and its burden among pregnant women living inthese endemic foci is lacking
Studies have demonstrated that schistosomiasis infectionin pregnant women results in severe anaemia [16] low birthweight and maternal mortality [24ndash26] However the aeti-ology of anaemia is multifactorial involving complex inter-action between nutrition status infectious disease (malariahuman immunodeficiency virus (HIV) and helminths) andother factors (sociodemographic and economic) [27] Theseconditions are integrally linked and subsequently lead toadverse pregnancy outcomes [27] S haematobium havebeen linked to placental inflammation leading to poor birthoutcomes as a result of placental malfunction Data suggestthat infected women have a higher rate of spontaneousabortions and a higher risk for ectopic pregnancies [2829] Conversely studies have demonstrated the biologicplausibility that female genital schistosomiasis may makewomen more susceptible to HIV [30] Praziquantel (PZQ) isrecommended in pregnancy [31]
Pregnant women living in Munyenge Mount CameroonArea may be exposed to coinfection with S haematobiumand P falciparum and thus may experience anaemia severityThe specific aims of this study were to (i) determine theprevalence and intensity of S haematobium P falciparumand coinfections among pregnant women reporting for ANCclinic visit at the Munyenge Health Centre (ii) determinethe factors associated with prevalence and intensity of theseinfections and (iii) assess the relative effect of S haema-tobium P falciparum and their coinfection on anaemiaprevalence and severity in pregnancy
2 Methods
21 Study Design Malaria and urogenital schistosomiasis arecoendemic in some areas of Mount Cameroon Area South-western Cameroon Munyenge is a rural community situatedat the foot of mount Cameroon at an altitude of 261 above sealevel This village is endemic foci for the transmission of Shaematobium [23] and recent reports of a community-basedstudy show an overall prevalence of 40 [32] In the Mount
Cameroon Area malaria parasite transmission is perennial[33] and P falciparum accounts for 60 of malaria parasiteinfection among pregnant women [34] A cross-sectionalstudy aimed to determine the prevalence of S haematobiumP falciparum and coinfections and evaluate their relativeeffect on anaemia prevalence and severity among pregnantwomen is justified
A sample size of 263 pregnant was determined to beadequate to detect a 5 change in prevalence Sample sizecalculation was based on the estimate of the prevalence of Shaematobium infection in Munyenge according to a baselineepidemiological survey carried out in 2012 by Ntonifor etal [23] The sample size was determined using the formulan = z2pqd2 [35] where n is the sample size required z = 196is confidence level test statistic at the desired level of signifi-cance p = 78 is the proportion of urogenital schistosomi-asis prevalence q = 1 minus p is the proportion of urogenitalschistosomiasis negative and d is the acceptable error willingto be committed However due to logistics we had a samplesize of 250 pregnant women which is well within 90ndash95 ofthe expected sample size calculated
The study was carried out in the Munyenge Health Areawhich is about 27 km fromMuyuka town It is bounded to theWest by Likoko native to the East by Masone to the Northby Mount Cameroon and to the North East by Mbongesubdivision (Figure 1) Munyenge has a heterogenous pop-ulation of 15000 inhabitants consisting of individuals fromseveral cultural backgrounds including natives from OrokoWimbum kom Mettas Ibus Nhies Ndop and Isimbis Thisarea is found in the rain forest of the Southwest Regionwith rich volcanic soil encouraging farming activities Themain occupation of the people is farming with cocoa andplantains being their main cash crops [32] Munyenge HealthArea has four streams with outlet springs (providing naturalwater sources) situated in the middle of the village Thesesprings are habitats for the Bulinus spp intermediate host andthus constitute the main transmission foci of S haematobiumin the community Bulinus snails are found on vegetationand rocks surrounding the water point and on vegetationwithin the streams These springs include the ldquocoast timberrdquoand ldquoKCBrdquo (men and women) The coast timber is a smallcatchment for spring water located within the communitywhere pupils play oftenwhile theKCB ldquomanrdquo and ldquowomanrdquo asthe name suggests are bathing springs for males and femalesrespectively which are found further from the communityMunyenge is characterised by the absence of pipe bornewater and the use of fresh water sources for householdactivities is common All members of the community usethese springs for drinking water bathing washing of clothesand household utensils [32] Munyenge has a temperaturerange of 24∘Cndash27∘C which favours high release of cercariaeinto the waters These conditions make it certain that thepeople will continue to be infected and reinfected
3 Data Collection
Pregnant women reporting for ANC clinic visit at the Mun-yenge Health Centre between June and September 2014 whohad lived in Munyenge for at least two months and gave
Journal of Parasitology Research 3
9∘12
9984000998400998400E 9
∘15
9984000998400998400E 9
∘18
9984000998400998400E
4∘309984000998400998400N
4∘279984000998400998400N
4∘249984000998400998400N
Settlement
Main road
Secondary
Foot path
Rivers
StreamSpringLake
road
Figure 1 Map showing the location of Munyenge in Mount Cameroon Area
their consent were enrolled consecutively Pregnant womenwere interviewed by a field researcher using a questionnairewhich recorded demographic information (age residence)gynaecologicobstetric history (gravidity status gestationalage and pregnancy complications) socioeconomic indica-tors (educational level occupation) and questions relatedto malaria (IPTp-SP uptake ITN usage) and schistosomiasis(main household water source frequency of contact withopen water source and domestic activities carried out in thestream) In addition to the questionnaire interview womenwere asked to collect urine in supplied 20mL screw top plasticcontainers between 1000 am and 200 pmThe samples werestored in a cool box during transportation to the Universityof Buea Medical Research Laboratory and processed within24 hours of collection
31 Laboratory Analyses
311 Anaemia Status Determination Haemoglobin levelswere determined from finger-prick blood samples using aportable battery-operated photometer (HemoCue) (Hemo-Cue 201+ system HemoCue Angelholm Sweden) (URIT-12) Hb concentration was expressed in gdL Anaemia wasdefined as an Hb value lt 110 gdL [36] Anaemia severitywas defined as follows mild anaemia (Hb 10ndash109 gdL)moderate anaemia (Hb 7ndash99 gdL) and severe anaemia (Hblt 70 gdL) [36]
312 Parasitological Examination Malaria parasites wereidentified on thick and thin blood smears stained with 5Giemsa The smears were observed for 30 minutes underthe times100 (oil immersion) objective of a UNICO lightmicroscope [37] Malaria parasite density was estimated bycounting parasites against 200 leucocytes in thick smearsassuming a white cell count of 8000 leucocytes per 120583Lof blood [38] Malaria parasite density was classified into
lt500 501ndash5000 and gt5000 for low moderate and highparasitaemia respectively [38] S haematobium eggs wereidentified in urine samples using the filtration technique [39]In brief 10mls of urine was filtered using membrane filters(Sterlitech Polycarbonate (PCTE) membrane filters USA)and the egg count was recorded per 10mls of urine Theinfection intensity was classified as light (lt50 eggs10mL ofurine) or heavy (ge50 eggs10mL of urine) as defined by theWorld Health Organization (WHO) [40] Microhaematuriawas used as proxy-diagnosis of urogenital schistosomiasis anaccepted marker in the rapid diagnosis of S haematobiuminfection in urine [41] Samples were tested for microhaema-turia using urine reagent strips (Uripath Plasmatec Labo-ratory UK) (Combi-11) as per manufacturer instructionsResults were expressed as negative or in levels of positivity(+ ++ or +++) and not including traces A pregnant womanwas infected with S haematobium when she was diagnosedpositive by microscopic examination andor urine reagentstrip
32 Statistical Analysis The data was analyzed using SPSSversion 190 (SPSS Inc Chicago IL USA) Proportions ofS haematobium P falciparum and coinfection and anaemiastatus were compared between different groups (age groupsgravidity status educational level occupational status streamusage and activities and IPTp-SP uptake) using Pearson Chi-square test Crude odds ratios were estimated and factorsassociated with infections and anaemia to be included inthe multivariate logistic regression model were identifiedVariables that had a 119875 value lt 020 in bivariate analysiswere included in the multivariate logistic regression modelUsing the enter method variables that showed independentassociation with infections and anaemia status at a signifi-cance level of 119875 lt 005 were retained in the model MeanHb levels were compared between groups using Analysis ofVariance test (ANOVA) and Studentrsquos t-test Independent
4 Journal of Parasitology Research
factors associated with Hb levels were obtained using mul-tilinear regression analysis 119875 values lt 005 were consideredsignificant
33 Ethical Considerations The study protocol and designincluding the consent procedures were approved by the Insti-tutional Ethics ReviewBoard of the Faculty ofHealth ScienceUniversity of Buea and the Buea Regional Delegation ofPublic Health Prior to conducting the study the aim ofthe study and procedures to be used to collect data wereexplained to the pregnant women at the ANC clinic Written(from those who can read and write) or verbal (from thosewho cannot read and write) informed consent from all studyparticipants was obtained Each pregnant womanwho agreedto participate in the study was enrolled and given urinesample container to collect urine Participationwas voluntaryand study participants were assured of confidentiality andanonymity of data
4 Results
41 Characteristics of the Study Population In this cross-sectional study a total of 250 pregnant women reportingfor antenatal care was enrolled The mean age of the studyparticipants was 25 plusmn 521 years (range 14ndash40 years) Themajority (752) of the women were married All the studyparticipants had at least a primary education and about 50had obtained some form of secondary education Although ahigher proportion of the women had been enrolled for firstANC in the second trimester more than 40 had late clinicregistration About two-thirds of women reported taking atleast one dose of IPTp-SP and 46 reported having sleptunder a bed net the previous night The stream was the mainsource of water (99 stream usage) for domestic use andbathing The characteristics of the study sample are shown inTable 1
42 Prevalence and Intensity of Infection
421 S haematobium Infection Of the 250 volunteer preg-nant women enrolled 117 (468 95 CI 41ndash53) were pos-itive for S haematobium infection among whom 53 (453)had heavy (ge50 eggs10mL of urine) infection while 547(64) had light (lt50 eggs10mL of urine) infectionThe preva-lence of microhaematuria was 96 (24250) Using micro-scopic urine examination as gold standard the specificity andsensitivity ofmicrohaematuria in the diagnosis of S haemato-bium infection were 100 (95CI 972ndash100) and 205 (95CI 142ndash287) respectively Microhaematuria was stronglyrelated to egg density categories where microhaematuria wascommon (1205942 = 823 119875 = 0004) among women with heavyegg load (727) than in those with light infection (273)
422 P falciparum Infection The overall prevalence of Pfalciparum parasitaemia among the study participants was392 (98) (95 CI 334ndash454) Of the 98 pregnant womeninfected with P falciparum the proportions of low (lt500parasites120583L of blood) moderate (501ndash5000) and high
Table 1 Characteristics of the study participants
Characteristics Number examined (N) ()Age group (years)le20 56 22421ndash25 79 31626ndash30 71 284gt30 44 176
Activities in the streamDomestic contact and bathing 126 504Domestic contact only 124 496
Frequency to streamsday1 to 2 times 122 4883 to 4 times 57 2285+ times 71 284
IPTp-SP uptakeYes 169 676No 81 324
ITN useYes 115 460No 135 540
(gt5000) parasitaemia were 439 (43) 520 (61) and 41(4) respectively About 15 (38) (95 CI 113ndash202) ofthe pregnant women carried concurrent infections with Shaematobium and P falciparum Seventy-nine (316) andsixty (24) women had single infection with S haematobiumand P falciparum respectively
423 Factors Associated with Prevalence and Intensity ofS haematobium Infection S haematobium infection wasassociated with age gravidity status water contact frequency
Journal of Parasitology Research 5
Table 2 Risk factors associated with S haematobium infection among pregnant women in Munyenge
1205942 P value 417 00411205942 Pearson Chi-square test OR odd ratioOR adjusted using multivariate regression analysis
type of activity carried out in the stream and P falciparumparasitaemia in bivariate analysis (Table 2) The prevalenceof infection did not differ significantly with marital statuseducational level and occupational status In multivariate
analysis (controlling for age and gravidity status as con-founders) younger age groups le20 (aOR = 152 95 CI 17ndash1383) and 21ndash25 years (aOR = 73 95 CI 12ndash443) andbathing and domestic contact with stream (aOR = 335 95
6 Journal of Parasitology Research
CI 97ndash1159)were risk factors associatedwith S haematobiuminfection On the other hand less water contact frequency(1 to 2 times per day) (aOR = 28119864 minus 10 95 CI 94119864 minus11ndash85119864minus10) was associated with decreased risk of infectionSurprisingly primigravidity (OR = 02 95 CI 003ndash09)and secundigravidity (OR = 01 95 CI 002ndash04) wereless likely at risk Intensity of infection was associated withmalaria parasitaemia where light egg density infection wasless common (aOR = 04 95 CI 02ndash07 119875 = 0004)in malaria positive women (219 1464) than in malarianegative women (781 5064)
424 Factors Associated with Prevalence of P falciparumInfection The prevalence of P falciparum infection wasassociated (1205942 = 1782 119875 lt 001) with IPTp-SP uptake wheremalaria parasite infection was greater in women who had nottaken IPTp-SP (580) than in those who had at least one SPdose (302) The occurrence of P falciparum infection didnot differ significantly with maternal age gravidity status orITN usage
425 Factors Associated with Prevalence of Coinfection with Shaematobium and P falciparum Coinfection was associatedwith the type of activity carried out in the stream and watercontact frequency as well as IPTp-SP uptake Bathing anddomestic contact with stream (aOR = 133 95 CI 22ndash795) increased risk of coinfection among pregnant womenmeanwhile less water contact frequency (1 to 2 times per day(aOR = 01 95 CI 001ndash04) and 3 to 4 times per day (aOR =03 95 CI 01ndash09)) decreased risk of coinfection Womenwho had at least one SP dose were less likely (aOR= 006 95CI 002ndash02) to be coinfected (Table 3)
43 Haemoglobin Levels and Anaemia Themean (plusmnSD) hae-moglobin level of the pregnant women enrolled in the studywas 90 plusmn 16 gdL (range 61ndash137 gdL) Coinfection signif-icantly reduced Hb levels of pregnant women in the studyarea where levels in coinfected individuals were significantlylower (119875 lt 0001) when compared with levels seen withsingle infections (S haematobium and P falciparum) and noinfection (Table 4) In addition Hb levels were significantlylower among women coinfected with P falciparum and heavyS haematobium infections than in individuals coinfectedwith P falciparum and light S haematobium infection andthose with no infection (Table 5) Although age maritalstatus educational level occupational status infection statusand IPTp-SP uptake were identified as factors associatedwith Hb levels IPTp-SP was seen as the only independentpredictor of Hb levels taking into consideration all possibleconfounding variables (Table 4)
Anaemia prevalence was 888 (222250) with anaemiaseverity as follows mild (132 119899 = 33) moderate (628119899 = 157) and severe (128 119899 = 32) All cases diagnosedwithcoinfection were anaemic (Table 6) Coinfection accountedfor 938 (3032) of all severe anaemia cases with majority719 (2332) of the severe anaemic cases coinfected withP falciparum and heavy density S haematobium infections(Table 5) Uptake of IPTp-SP (438 1432) was associated
(1205942 = 1132 119875 = 001) with reduced percentage of severeanaemia compared with that observed among women withno SP (563 1832) Risk factors found to be associated withincreased odds of anaemia were P falciparum infection (OR=40 95 CI 10ndash145) and occupation (business) (OR = 20195 CI 40ndash101) (Table 6)
5 Discussion
To our knowledge this is the first study carried out on uro-genital schistosomiasis among pregnant women in Camer-oon This study determined the prevalence of S haemato-bium P falciparum and coinfection factors associated withthese infections and assessed their relative effect on anaemiaprevalence and severity among pregnant women in Mun-yenge S haematobium and P falciparum infections are com-mon among pregnant women living in Munyenge and theircoinfection exacerbates anaemia
The prevalence of S haematobium infection among preg-nant women in our study was 468 The high prevalencereflects high exposure to infection among pregnant womenliving in Munyenge due to absolute dependence on naturalwater sources for domestic activities and bathing Comparedto the level of infection in the present study lower prevalenceof urogenital schistosomiasis among pregnant women hasbeen reported inNigeria by Eyo et al [42] (238) and Salawuand Odaibo [43] (208) Differences in the method usedfor the detection of S haematobium infection may partlyexplain the observed differences in rates Although thesestudies attributed the lower prevalence levels of urinary schis-tosomiasis among pregnant women to a taboo restrictingpregnant women from visiting natural water bodies [42]compared with urine filtration method used in our study thelower sensitive centrifugation method use in the diagnosisof S haematobium infection in the Nigerian studies mayhave underestimated true infection levelsMalaria is commonamong pregnant women in the study area with a prevalenceof 392 The only factor seen to be associated with malariaparasite infection in this study site was IPTp uptake Theeffectiveness of IPTp-SP in the prevention of malaria inpregnancy is well established [34 44]
For transmission of schistosomiasis to take place theschistosomes parasite requires an avenue where it is indirect contact with the human host [9] Pregnant womenliving in Munyenge get in contact with infection duringactivities such as laundry plate washing and water fetchingfor domestic use In addition to domestic activities bathingin streams poses a greater risk of infection among pregnantwomen in this area Analyses from other studies have shownthat regularly bathing in water sources contaminated withthe developmental stages of the schistosomes parasite wasassociated with prevalence and intensity of schistosomiasis[45ndash47]Moreover increased risk of infection associatedwiththe number and duration of water contact with infestedwaters per day has also been reported [47] Women whoreported surface-water contact at least 3 to 5 times perday were at greater risk of infection due to longer periodof contact with contaminated water Health education toinstruct pregnant women to make less surface-water contact
Journal of Parasitology Research 7
Table 3 Risk factors associated with coinfection with S haematobium and P falciparum among pregnant women in Munyenge
1205942 119875 value 1329 lt00011205942 Pearson Chi-square test OR odd ratioAdjusted OR using multivariate regression analysis
frequency and the implication of voiding their bladder inwater bodies is paramount These behavioural changes willsignificantly reduce the risk of S haematobium infectionamong pregnant women and contamination of water sourcesin this setting Ultimately provision of portable water andimproved sanitation system will play a major role in decreas-ing disease transmission and incidence
Age as observed in most schistosomiasis surveys was amajor determinant of schistosomes infection among preg-nant women in our study area The highest prevalence val-ues of urogenital schistosomiasis were recorded in youngerwomen (le25 years) Individuals within le20 age group werefound to be at a greater risk of S haematobium infection withprevalence of 554 This is in agreement with trends estab-lished in schistosomiasis surveys carried out in Cameroon
[32 48] and other parts of Africa [42 43] Alternativelythe decrease risk of infection observed in older age groups(gt25 years) conformed to earlier reports [32 42] Studieshave reported that age-acquired immunity to reinfection andchanges in water contact patterns contribute to the decliningtrend in prevalence with increasing age [49] Older womenare less likely to be engaged in water contact behaviourscompared to younger women Age dependent immunity toS haematobium has been shown to affect mean egg outputof infected persons [49] Socioeconomic status of the womenwas not an independent factor associated with S haema-tobium prevalence in this high-risk community Similarlyreports from other rural settings endemic for schistosomi-asis failed to identify any socioeconomic variables that arestrongly associated with schistosomiasis prevalence [50 51]
8 Journal of Parasitology Research
Table 4 Factors associated with mean (plusmnSD) haemoglobin levels among pregnant women in Munyenge Health Area
Factors Category Mean (plusmnSD) Hblevels Test-value Unadjusted
lowastAnalysis of variance test (ANOVA)$Studentrsquos 119905-testampAdjusted 119875 values using multilinear regression analysisNA not applicable variables with 119875 gt 02 in bivariate analysis were not included in regression analysis
Table 5 Association between S haematobium intensity P falciparum infection and mean (plusmnSD) haemoglobin levels and anaemia severity
lowastSignificance level 119865 = 1240 119875 lt 0001lowastAnalysis of variance test (ANOVA)ampPearson Chi-Square test
The absence of association between socioeconomic variablesand infection prevalencemay be attributed to general povertyand uniformity in high exposure risk in the population [50]
The overall prevalence of coinfection with S haema-tobium and P falciparum infection was 152 suggestingcoendemicity of both infections in the study area SimilarlyYatich et al [52] reported a helminth andmalaria coinfectionprevalence of 166 among pregnant women in Ghana Theimpact of helminth infections on malaria parasitaemia and
disease during coinfection is an established phenomenonalthough much is still unknown and contradictions persist[53 54]We observed that light S haematobium infectionwasless common (aOR= 04) among pregnant women coinfectedwith P falciparum suggesting a negative interaction betweenboth parasites [4] In accordance with findings of Getie etal [55] schistosomiasis coinfection could affect Plasmodiumparasitemia and vice versa depending on the intensity of theova in coinfected persons Nonetheless a further study is
Journal of Parasitology Research 9
Table 6 Risk factors associated with anaemia among pregnant women in Munyenge Health Area
Factors Category Anaemia prevalence Adjusted OR (95 CI) 119875 value
Adjusted OR using multivariate regression analysisNA not applicable variables with 119875 gt 02 in bivariate analysis were not included in multivariate analysis
needed to explore the underlying mechanisms of interactionbetween malaria parasitaemia and S haematobium
Schistosomiasis causes long term morbidity such asanaemia Our study showed that the magnitude of S haema-tobium egg counts is significantly related to haemoglobinconcentration confirming that urogenital schistosomiasiscontributes to anaemia [24 25] In this study anaemiawas more pronounced in women with heavy infectionintensity than in those with light infection Coinfection ofhelminth infections and P falciparum increases anaemiaseverity [8 9] Coinfection among pregnant women lowersHb concentration compared with single infection This is inagreement with findings of Okafor and Elenwo [56] Moreso coinfected women with heavy intensity S haematobiuminfection had the lowest mean Hb levels (66 gdL) andthis subpopulation of women contributed to about 72of all severe anaemic cases The combined presence and
interaction of S haematobium and P falciparum infectionsis partly responsible for the low haemoglobin concentrationin women with concurrent infectionMalaria causes anaemiaby destruction and removal of parasitized red blood cellsand shortening of the life span of nonparasitized red cellsas well as decreasing the rate of erythrocyte production inbone marrow [57]Themechanism by which schistosomiasiscauses anaemia is not fully understood but it is suggested thathelminth infections could contribute to increase in the preva-lence of inflammatory syndromes impairing erythropoiesisand interfering with mobilization of reticuloendothelial ironstorages and shortening erythrocyte survival [58] Similar toprevious reports of a study in Uganda [59] malaria parasiteinfection was an independent factor associated with increaseanaemia risk
The risk of coinfection was associated with streamusage (bathing and domestic contact with stream) while
10 Journal of Parasitology Research
less water contact and SP usage decreased risk of infectionThis finding suggests that intervention strategies focusingon combating malaria and schistosomiasis respectively byincreasing the uptake of IPTp-SPdoses and less water contactamong pregnant women living in Munyenge represents themost appropriate prevention of coinfection with consequentincrease in Hb levels
This study had one limitation We did not investigate theprevalence of HIV infection among the study participants Ithas been shown that coinfections with helminths andmalariacause considerable morbidity in the host particularly in thepresence of HIV infection [60]
To conclude the study has indicated that S haematobiumand P falciparum infections are common among pregnantwomen living in Munyenge and their coinfection is influ-enced by high frequencies of these parasites in the same pop-ulationThe study also revealed that younger age and bathingand domestic contact with stream are independently associ-ated with prevalence of S haematobium infection while noIPTp-SP was associated with P falciparum infection Streamusage increased risk of coinfection while less water contactand SP usage decreased its risk The fact that light S haema-tobium infection was less common in P falciparum infectedwomen suggests that Plasmodium falciparum parasitaemiamay be associatedwith intensity of urogenital schistosomiasisin coinfected individuals Anaemia is a severe public healthproblem in pregnancy in Munyenge and coinfection withS haematobium and P falciparum exacerbates anaemiaLess water contact frequency and increase uptake of IPTp-SPdoses will significantly reduce risk of coinfection andconsequently anaemia severity in pregnancy in this setting
Abbreviations
IPTp-SP Intermittent preventive treatment in pregnancy(IPTp) with sulfadoxine-pyrimethamine (SP)
ITN Insecticide treated bed netsHIV Human immunodeficiency virusANC Antenatal care
Competing Interests
The authors declare that they do not have any competinginterests
Authorsrsquo Contributions
Judith K Anchang-Kimbi conceived and designed the studyanalyzed the data and wrote the manuscript Dillys MansohElad participated in the design of the study performedthe experiments and made inputs in manuscript write-upGemain Taiwe Sotoing and Eric Akum Achidi supervisedreviewed and provided inputs to the manuscript All authorsread and approved the final manuscript
Acknowledgments
The authors are grateful to all the pregnant women whogave their consent to participate in the study Special thanks
are due to the chief medical officer nurses and laboratorytechnician of the Munyenge Health Centre for their cooper-ation and contribution This study received financial supportfrom the Ministry of Higher Education University ResearchModernisation grant given to authors Judith K Anchang-Kimbi and Eric Akum Achidi
References
[1] T N Petney and R H Andrews ldquoMultiparasite communitiesin animals and humans frequency structure and pathogenicsignificancerdquo International Journal for Parasitology vol 28 no3 pp 377ndash393 1998
[2] F E G Cox ldquoConcomitant infections parasites and immuneresponsesrdquo Parasitology vol 122 supplement 1 pp S23ndashS382001
[3] M Nacher P Singhasivanon S Yimsamran et al ldquoIntestinalhelminth infections are associated with increased incidenceof Plasmodium falciparum malaria in Thailandrdquo Journal ofParasitology vol 88 no 1 pp 55ndash58 2002
[4] J-Y Le Hesran J Akiana E H M Ndiaye M Dia P Senghorand L Konate ldquoSevere malaria attack is associated with highprevalence of Ascaris lumbricoides infection among childrenin rural Senegalrdquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 98 no 7 pp 397ndash399 2004
[5] M Nacher F Gay P Singhasivanon et al ldquoAscaris lumbricoidesinfection is associated with protection from cerebral malariardquoParasite Immunology vol 22 no 3 pp 107ndash113 2000
[6] V Briand L Watier J-Y Le Hesran A Garcia and M CotldquoCoinfection with Plasmodium falciparum and Schistosomahaematobium protective effect of schistosomiasis on malariain Senegalese childrenrdquo American Journal of Tropical Medicineand Hygiene vol 72 no 6 pp 702ndash707 2005
[7] N Oslash Christensen P Furu J Kurtzhals and A OdaiboldquoHeterologous synergistic interactions in concurrent experi-mental infection in the mouse with Schistosoma mansoniEchinostoma revolution Plasmodium yoelii Babesia microtiand Trypanosoma bruceirdquo Parasitology Research vol 74 no 6pp 544ndash551 1988
[8] G Raso A Luginbuhl C A Adjoua et al ldquoMultiple parasiteinfections and their relationship to self-reported morbidity ina community of rural Cote drsquoIvoirerdquo International Journal ofEpidemiology vol 33 no 5 pp 1092ndash1102 2004
[9] S Brooker W Akhwale R Pullan et al ldquoEpidemiology ofPlasmodium-helminth co-infection in Africa populations atrisk potential impact on anemia and prospects for combiningcontrolrdquo American Journal of Tropical Medicine and Hygienevol 77 no 6 pp 88ndash98 2007
[10] C E Shulman and E K Dorman ldquoReducing childhood mor-tality in poor countries importance and prevention of malariain pregnancyrdquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 97 no 1 pp 30ndash35 2003
[11] WorldHealthOrganisation andAfrica Regional OfficeMalariaPrevention and Control during Pregnancy in the African RegionWHOAFRO Brazzaville Congo 2004
[12] D Engels L Chitsulo A Montresor and L Savioli ldquoTheglobal epidemiological situation of schistosomiasis and newapproaches to control and researchrdquo Acta Tropica vol 82 no2 pp 139ndash146 2002
[13] P J Hotez and A Kamath ldquoNeglected tropical diseases in sub-Saharan Africa review of their prevalence distribution and
[14] M J Van Der Werf S J De Vlas S Brooker et al ldquoQuantifica-tion of clinical morbidity associated with schistosome infectionin sub-Saharan Africardquo Acta Tropica vol 86 no 2-3 pp 125ndash139 2003
[15] M N Nour ldquoSchistosomias health effect on womenrdquo Reviewsin Obstetrics amp Gynecology vol 3 no 1 pp 28ndash32 2010
[16] J F Friedman P Mital H K Kanzaria G R Olds and J DKurtis ldquoSchistosomiasis and pregnancyrdquo Trends in Parasitologyvol 23 no 4 pp 159ndash164 2007
[17] httpwwwwhointschistosomiasisstrategyen[18] H N Ntonifor and J A Ajayi ldquoWater contact and Schistosoma
haematobium infection A case study of some communitiesin Toro Local Government council Area (TLGCA) of BauchiStaterdquoNigeria Journal of Natural and Applied Sciences vol 1 no1 pp 54ndash59 2005
[19] P Saotoing T Vroumsia A M Njan F N Tchuenguem andJ Messi ldquoEpidemiological survey of schistosomiasis due toSchistosoma haematobium in some primary schools in thetown of Maroua far north region Cameroonrdquo InternationalJournal of Tropical Medicine vol 6 no 2 pp 19ndash24 2011
[20] L A Tchuem Tchuente R I K Ngassam L Sumo et al ldquoMap-ping of schistosomiasis and soil- transmitted helminthiasis inthe regions of centre east and west cameroonrdquo PLoS NeglectedTropical Diseases vol 6 no 3 p e1553 2012
[21] L A Tchuem Tchuente N C Dongmo P Ngassam et alldquoMapping of schistosomiasis and soil- transmitted helminthi-asis in the regions of Littoral North-West South and South-West Cameroon and recommendations for treatmentrdquo BMCInfectious Disease vol 13 article 602 2013
[22] K J N Ndamukong M A Ayuk J S Dinga T N Akenji VA Ndiforchu and V P K Titanji ldquoPrevalence and intensity ofurinary schistosomiasis in primary school children of the KottoBarombi health area Cameroonrdquo East African Medical Journalvol 78 no 6 pp 287ndash289 2001
[23] H N Ntonifor G N Mbunkur and N W Ndaleh ldquoEpidemi-ological survey of urinary schistosomiasis in some primaryschools in a new focus behind Mount Cameroon (Munyenge)South West Region Cameroonrdquo East African Medical Journalvol 89 no 3 pp 82ndash88 2012
[24] J F Friedman H K Kanzaria and S T McGarvey ldquoHumanschistosomiasis and anemia the relationship and potentialmechanismsrdquo Trends in Parasitology vol 21 no 8 pp 386ndash3922005
[25] A Ajanga N J S Lwambo L Blair U Nyandindi A Fenwickand S Brooker ldquoSchistosoma mansoni in pregnancy andassociations with anaemia in northwest Tanzaniardquo Transactionsof the Royal Society of Tropical Medicine and Hygiene vol 100no 1 pp 59ndash63 2006
[26] G Helling-Giese E F Kjetland S G Gundersen et al ldquoSchis-tosomiasis in women manifestations in the upper reproductivetractrdquo Acta Tropica vol 62 no 4 pp 225ndash238 1996
[27] R W Steketee B L Nahlen M E Parise and C MenendezldquoTheburden ofmalaria in pregnancy inmalaria-endemic areasrdquoAmerican Journal of Tropical Medicine and Hygiene vol 64 no1-2 pp 28ndash35 2001
[28] V V Laxman B Adamson and T Mahmood ldquoRecurrentectopic pregnancy due to Schistosoma hematobiumrdquo Journal ofObstetrics and Gynaecology vol 28 no 4 pp 461ndash462 2008
[29] S Bahrami H Alatassi S P Slone and D M OrsquoConnorldquoTubal gestation and schistosomiasis a case reportrdquo Journal ofReproductiveMedicine for theObstetrician andGynecologist vol51 no 7 pp 595ndash598 2006
[30] P S Mbabazi O Andan D W Fitzgerald L Chitsulo DEngels and J A Downs ldquoExamining the relationship betweenurogenital schistosomiasis and HIV infectionrdquo PLoS NeglectedTropical Diseases vol 5 no 12 Article ID e1396 2011
[31] R Tweyongyere P A Mawa N O Emojong et al ldquoEffectof praziquantel treatment of Schistosomamansoni during preg-nancy on intensity of infection and antibody responses to schis-tosome antigens results of a randomised placebo-controlledtrialrdquo BMC Infectious Diseases vol 9 article 32 2009
[32] H N Ntonifor A E Green M O S Bopda et al ldquoEpi-demiology of urinary schistosomiasis and soil transmittedhelminthiasis in a recently established focus behind MountCameroonrdquo International Journal of Current Microbiology andApplied Sciences vol 4 no 3 pp 1056ndash1066 2015
[33] S Wanji A J Kengne-Ouafo E E Joan Eyong et al ldquoGeneticdiversity of Plasmodium falciparummerozoite surface protein-1 block 2 in sites of contrasting altitudes and malaria endemic-ities in the Mount Cameroon Regionrdquo American Journal ofTropical Medicine and Hygiene vol 86 no 5 pp 764ndash774 2012
[34] J K Anchang-Kimbi E A Achidi B Nkegoum E Sverremark-Ekstrom and M Troye-Blomberg ldquoDiagnostic comparisonof malaria infection in peripheral blood placental blood andplacental biopsies in Cameroonian parturient womenrdquoMalariaJournal vol 8 no 1 article 126 2009
[35] F J Bryan The Design and Analysis of Research Studies Uni-versity ofOtago Dunedin NewZealand CambridgeUniversityPress Cambridge UK 1992
[36] World Health Organisation Haemoglobin Concentrations forthe Diagnosis of Anaemia and Assessment of Severity Vitaminand mineral Nutrition Information System WHO GenevaSwitzerland 2011
[37] M CheesbroughDistrict Laboratory Practice in Tropical Coun-tries Cambridge University Press Cambridge UK 2006
[39] N O Christensen G Gotsche and F Frandsen ParasitologicalTechniques for Use in Routine Laboratory Maintainance of Schis-tosomes and Used in Studies on the Epidemiology of Human andBovine Schistosomiasis Danish Bilhaziasis Laboratory Manual1984
[40] World Health OrganizationmdashTropical Disease Research TDRstrategic direction Schistosomiasis WHO-TDR 2002
[41] World Health OrganizationGuidelines for the Evaluation of SoilTransmitted Helminthiasis and Schistosomiasis at CommunityLevel A Guide for Managers of Control Programme WHOGeneva Switzerland 1993
[42] J E Eyo G C Onyishi and F C Okafor ldquoUrinary schisto-somiasis among pregnant women in some endemic tropicalsemi-urban communities of Anambra State Nigeriardquo TropicalBiomedicine vol 29 no 4 pp 575ndash579 2012
[43] O T Salawu and A B Odaibo ldquoSchistosomiasis among preg-nant women in rural communities in Nigeriardquo InternationalJournal of Gynecology andObstetrics vol 122 no 1 pp 1ndash4 2013
[44] K R Tan B L Katalenich K E Mace et al ldquoEfficacyof sulphadoxine-pyrimethamine for intermittent preventivetreatment of malaria in pregnancy Mansa Zambiardquo MalariaJournal vol 13 no 1 article 227 2014
12 Journal of Parasitology Research
[45] J Bethony J T Williams H Kloos et al ldquoExposure toSchistosoma mansoni infection in a rural area in Brazil IIhousehold risk factorsrdquo Tropical Medicine and InternationalHealth vol 6 no 2 pp 136ndash145 2001
[46] J C Sousa-Figueiredo D Gamboa J M Pedro et al ldquoEpi-demiology of malaria schistosomiasis geohelminths anemiaand malnutrition in the context of a demographic surveillancesystem in northern Angolardquo PLoS ONE vol 7 no 4 Article IDe33189 2012
[47] F Anto V Asoala M Adjuik et al ldquoWater contact activitiesand prevalence of schistosomiasis infection among school-agechildren in communities along an irrigation scheme in RuralNorthern Ghanardquo Journal of Bacteriology amp Parasitology vol 4article 177 2013
[48] L-A Tchuem Tchuente J M Behnke F S Gilbert V RSouthgate and J Vercruysse ldquoPolyparasitism with Schistosomahaematobium and soil-transmitted helminth infections amongschool children in Loum Cameroonrdquo Tropical Medicine andInternational Health vol 8 no 11 pp 975ndash986 2003
[49] J-F Etard M Audibert and A Dabo ldquoAge-acquired resistanceand predisposition to reinfection with Schistosoma haemato-bium after treatment with praziquantel in Malirdquo The AmericanJournal of TropicalMedicine andHygiene vol 52 no 6 pp 549ndash558 1995
[50] A Gazzinelli G Velasquez-Melendez S B Crawford P TLoVerde R Correa-Oliveira and H Kloos ldquoSocioeconomicdeterminants of schistosomiasis in a poor rural area in BrazilrdquoActa Tropica vol 99 no 2-3 pp 260ndash271 2006
[51] A P Kapito-Tembo V Mwapasa S R Meshnick et al ldquoPreva-lence distribution and risk factors for Schistosoma hematobiuminfection among school children in Blantyre Malawirdquo PLoSNeglected Tropical Diseases vol 3 no 1 article e361 2009
[52] N J Yatich J Yi T Agbenyega et al ldquoMalaria and intestinalhelminth co-infection among pregnant women in Ghanaprevalence and risk factorsrdquo The American Journal of TropicalMedicine and Hygiene vol 80 no 6 pp 896ndash901 2009
[53] M Nacher ldquoInteractions between worms and malaria goodworms or bad wormsrdquoMalaria Journal vol 10 article no 2592011
[54] A A Adegnika and P G Kremsner ldquoEpidemiology of malariaand helminth interaction a review from 2001 to 2011rdquo CurrentOpinion in HIV and AIDS vol 7 no 3 pp 221ndash224 2012
[55] S Getie Y Wondimeneh G Getnet et al ldquoPrevalence andclinical correlates of Schistosoma mansoni co-infection amongmalaria infected patients Northwest Ethiopiardquo BMC ResearchNotes vol 8 no 1 article no 480 2015
[56] E Okafor and A Elenwo ldquoHaemoglobin status of children withmixed infection ofmalaria and urinary schistosomiasis inOdauCommunity Rivers state Nigeriardquo Journal of Agriculture andSocial Research vol 7 no 1 pp 56ndash62 2008
[57] M A McDevitt J Xie V Gordeuk and R Bucala ldquoThe anemiaof malaria infection role of inflammatory cytokinesrdquo CurrentHematology Reports vol 3 no 2 pp 97ndash106 2004
[58] J G Shaw and J F Friedman ldquoIron deficiency anemia focus oninfectious diseases in lesser developed countriesrdquo Anemia vol2011 Article ID 260380 10 pages 2011
[59] H K Green J C Sousa-Figueiredo M-G Basanez et alldquoAnaemia in Ugandan preschool-aged children the relativecontribution of intestinal parasites and malariardquo Parasitologyvol 138 no 12 pp 1534ndash1545 2011
[60] E Ivan N J Crowther E Mutimura L O Osuwat S Janssenand M P Grobusch ldquoHelminthic infections rates and malaria
in HIV-infected pregnant women on anti-retroviral therapy inRwandardquo PLoS Neglected Tropical Diseases vol 7 no 8 ArticleID e2380 2013
parasitic disease in terms of socioeconomic and publichealth importance [12] More than 90 of the roughly 200million cases of schistosomiasis occur in Africa [13] of whichapproximately two-thirds are caused by Schistosoma haema-tobium [14] the etiologic agent of urogenital schistosomiasisSchistosomiasis is endemic in rural areas where there is a lackof safe water supply poverty ignorance and poor hygienicpractices [15] Forty million women of child bearing age areinfected with younger and pregnant women being at greaterrisk of infection [16 17] Domestic activities such as washingclothes and fetching water in infected water expose womenand children to infection [18] In Cameroon schistosomiasisis endemic in the northern regions [19] Centre East West[20] Littoral North West South and Southwest Regions[21] Urogenital schistosomiasis is endemic in SouthwesternCameroon where Barombi Kotto [22] and Munyenge [23]are identified transmission foci While most of these studieshave focused on school-age children and the communityepidemiological data on the prevalence of urogenital schis-tosomiasis and its burden among pregnant women living inthese endemic foci is lacking
Studies have demonstrated that schistosomiasis infectionin pregnant women results in severe anaemia [16] low birthweight and maternal mortality [24ndash26] However the aeti-ology of anaemia is multifactorial involving complex inter-action between nutrition status infectious disease (malariahuman immunodeficiency virus (HIV) and helminths) andother factors (sociodemographic and economic) [27] Theseconditions are integrally linked and subsequently lead toadverse pregnancy outcomes [27] S haematobium havebeen linked to placental inflammation leading to poor birthoutcomes as a result of placental malfunction Data suggestthat infected women have a higher rate of spontaneousabortions and a higher risk for ectopic pregnancies [2829] Conversely studies have demonstrated the biologicplausibility that female genital schistosomiasis may makewomen more susceptible to HIV [30] Praziquantel (PZQ) isrecommended in pregnancy [31]
Pregnant women living in Munyenge Mount CameroonArea may be exposed to coinfection with S haematobiumand P falciparum and thus may experience anaemia severityThe specific aims of this study were to (i) determine theprevalence and intensity of S haematobium P falciparumand coinfections among pregnant women reporting for ANCclinic visit at the Munyenge Health Centre (ii) determinethe factors associated with prevalence and intensity of theseinfections and (iii) assess the relative effect of S haema-tobium P falciparum and their coinfection on anaemiaprevalence and severity in pregnancy
2 Methods
21 Study Design Malaria and urogenital schistosomiasis arecoendemic in some areas of Mount Cameroon Area South-western Cameroon Munyenge is a rural community situatedat the foot of mount Cameroon at an altitude of 261 above sealevel This village is endemic foci for the transmission of Shaematobium [23] and recent reports of a community-basedstudy show an overall prevalence of 40 [32] In the Mount
Cameroon Area malaria parasite transmission is perennial[33] and P falciparum accounts for 60 of malaria parasiteinfection among pregnant women [34] A cross-sectionalstudy aimed to determine the prevalence of S haematobiumP falciparum and coinfections and evaluate their relativeeffect on anaemia prevalence and severity among pregnantwomen is justified
A sample size of 263 pregnant was determined to beadequate to detect a 5 change in prevalence Sample sizecalculation was based on the estimate of the prevalence of Shaematobium infection in Munyenge according to a baselineepidemiological survey carried out in 2012 by Ntonifor etal [23] The sample size was determined using the formulan = z2pqd2 [35] where n is the sample size required z = 196is confidence level test statistic at the desired level of signifi-cance p = 78 is the proportion of urogenital schistosomi-asis prevalence q = 1 minus p is the proportion of urogenitalschistosomiasis negative and d is the acceptable error willingto be committed However due to logistics we had a samplesize of 250 pregnant women which is well within 90ndash95 ofthe expected sample size calculated
The study was carried out in the Munyenge Health Areawhich is about 27 km fromMuyuka town It is bounded to theWest by Likoko native to the East by Masone to the Northby Mount Cameroon and to the North East by Mbongesubdivision (Figure 1) Munyenge has a heterogenous pop-ulation of 15000 inhabitants consisting of individuals fromseveral cultural backgrounds including natives from OrokoWimbum kom Mettas Ibus Nhies Ndop and Isimbis Thisarea is found in the rain forest of the Southwest Regionwith rich volcanic soil encouraging farming activities Themain occupation of the people is farming with cocoa andplantains being their main cash crops [32] Munyenge HealthArea has four streams with outlet springs (providing naturalwater sources) situated in the middle of the village Thesesprings are habitats for the Bulinus spp intermediate host andthus constitute the main transmission foci of S haematobiumin the community Bulinus snails are found on vegetationand rocks surrounding the water point and on vegetationwithin the streams These springs include the ldquocoast timberrdquoand ldquoKCBrdquo (men and women) The coast timber is a smallcatchment for spring water located within the communitywhere pupils play oftenwhile theKCB ldquomanrdquo and ldquowomanrdquo asthe name suggests are bathing springs for males and femalesrespectively which are found further from the communityMunyenge is characterised by the absence of pipe bornewater and the use of fresh water sources for householdactivities is common All members of the community usethese springs for drinking water bathing washing of clothesand household utensils [32] Munyenge has a temperaturerange of 24∘Cndash27∘C which favours high release of cercariaeinto the waters These conditions make it certain that thepeople will continue to be infected and reinfected
3 Data Collection
Pregnant women reporting for ANC clinic visit at the Mun-yenge Health Centre between June and September 2014 whohad lived in Munyenge for at least two months and gave
Journal of Parasitology Research 3
9∘12
9984000998400998400E 9
∘15
9984000998400998400E 9
∘18
9984000998400998400E
4∘309984000998400998400N
4∘279984000998400998400N
4∘249984000998400998400N
Settlement
Main road
Secondary
Foot path
Rivers
StreamSpringLake
road
Figure 1 Map showing the location of Munyenge in Mount Cameroon Area
their consent were enrolled consecutively Pregnant womenwere interviewed by a field researcher using a questionnairewhich recorded demographic information (age residence)gynaecologicobstetric history (gravidity status gestationalage and pregnancy complications) socioeconomic indica-tors (educational level occupation) and questions relatedto malaria (IPTp-SP uptake ITN usage) and schistosomiasis(main household water source frequency of contact withopen water source and domestic activities carried out in thestream) In addition to the questionnaire interview womenwere asked to collect urine in supplied 20mL screw top plasticcontainers between 1000 am and 200 pmThe samples werestored in a cool box during transportation to the Universityof Buea Medical Research Laboratory and processed within24 hours of collection
31 Laboratory Analyses
311 Anaemia Status Determination Haemoglobin levelswere determined from finger-prick blood samples using aportable battery-operated photometer (HemoCue) (Hemo-Cue 201+ system HemoCue Angelholm Sweden) (URIT-12) Hb concentration was expressed in gdL Anaemia wasdefined as an Hb value lt 110 gdL [36] Anaemia severitywas defined as follows mild anaemia (Hb 10ndash109 gdL)moderate anaemia (Hb 7ndash99 gdL) and severe anaemia (Hblt 70 gdL) [36]
312 Parasitological Examination Malaria parasites wereidentified on thick and thin blood smears stained with 5Giemsa The smears were observed for 30 minutes underthe times100 (oil immersion) objective of a UNICO lightmicroscope [37] Malaria parasite density was estimated bycounting parasites against 200 leucocytes in thick smearsassuming a white cell count of 8000 leucocytes per 120583Lof blood [38] Malaria parasite density was classified into
lt500 501ndash5000 and gt5000 for low moderate and highparasitaemia respectively [38] S haematobium eggs wereidentified in urine samples using the filtration technique [39]In brief 10mls of urine was filtered using membrane filters(Sterlitech Polycarbonate (PCTE) membrane filters USA)and the egg count was recorded per 10mls of urine Theinfection intensity was classified as light (lt50 eggs10mL ofurine) or heavy (ge50 eggs10mL of urine) as defined by theWorld Health Organization (WHO) [40] Microhaematuriawas used as proxy-diagnosis of urogenital schistosomiasis anaccepted marker in the rapid diagnosis of S haematobiuminfection in urine [41] Samples were tested for microhaema-turia using urine reagent strips (Uripath Plasmatec Labo-ratory UK) (Combi-11) as per manufacturer instructionsResults were expressed as negative or in levels of positivity(+ ++ or +++) and not including traces A pregnant womanwas infected with S haematobium when she was diagnosedpositive by microscopic examination andor urine reagentstrip
32 Statistical Analysis The data was analyzed using SPSSversion 190 (SPSS Inc Chicago IL USA) Proportions ofS haematobium P falciparum and coinfection and anaemiastatus were compared between different groups (age groupsgravidity status educational level occupational status streamusage and activities and IPTp-SP uptake) using Pearson Chi-square test Crude odds ratios were estimated and factorsassociated with infections and anaemia to be included inthe multivariate logistic regression model were identifiedVariables that had a 119875 value lt 020 in bivariate analysiswere included in the multivariate logistic regression modelUsing the enter method variables that showed independentassociation with infections and anaemia status at a signifi-cance level of 119875 lt 005 were retained in the model MeanHb levels were compared between groups using Analysis ofVariance test (ANOVA) and Studentrsquos t-test Independent
4 Journal of Parasitology Research
factors associated with Hb levels were obtained using mul-tilinear regression analysis 119875 values lt 005 were consideredsignificant
33 Ethical Considerations The study protocol and designincluding the consent procedures were approved by the Insti-tutional Ethics ReviewBoard of the Faculty ofHealth ScienceUniversity of Buea and the Buea Regional Delegation ofPublic Health Prior to conducting the study the aim ofthe study and procedures to be used to collect data wereexplained to the pregnant women at the ANC clinic Written(from those who can read and write) or verbal (from thosewho cannot read and write) informed consent from all studyparticipants was obtained Each pregnant womanwho agreedto participate in the study was enrolled and given urinesample container to collect urine Participationwas voluntaryand study participants were assured of confidentiality andanonymity of data
4 Results
41 Characteristics of the Study Population In this cross-sectional study a total of 250 pregnant women reportingfor antenatal care was enrolled The mean age of the studyparticipants was 25 plusmn 521 years (range 14ndash40 years) Themajority (752) of the women were married All the studyparticipants had at least a primary education and about 50had obtained some form of secondary education Although ahigher proportion of the women had been enrolled for firstANC in the second trimester more than 40 had late clinicregistration About two-thirds of women reported taking atleast one dose of IPTp-SP and 46 reported having sleptunder a bed net the previous night The stream was the mainsource of water (99 stream usage) for domestic use andbathing The characteristics of the study sample are shown inTable 1
42 Prevalence and Intensity of Infection
421 S haematobium Infection Of the 250 volunteer preg-nant women enrolled 117 (468 95 CI 41ndash53) were pos-itive for S haematobium infection among whom 53 (453)had heavy (ge50 eggs10mL of urine) infection while 547(64) had light (lt50 eggs10mL of urine) infectionThe preva-lence of microhaematuria was 96 (24250) Using micro-scopic urine examination as gold standard the specificity andsensitivity ofmicrohaematuria in the diagnosis of S haemato-bium infection were 100 (95CI 972ndash100) and 205 (95CI 142ndash287) respectively Microhaematuria was stronglyrelated to egg density categories where microhaematuria wascommon (1205942 = 823 119875 = 0004) among women with heavyegg load (727) than in those with light infection (273)
422 P falciparum Infection The overall prevalence of Pfalciparum parasitaemia among the study participants was392 (98) (95 CI 334ndash454) Of the 98 pregnant womeninfected with P falciparum the proportions of low (lt500parasites120583L of blood) moderate (501ndash5000) and high
Table 1 Characteristics of the study participants
Characteristics Number examined (N) ()Age group (years)le20 56 22421ndash25 79 31626ndash30 71 284gt30 44 176
Activities in the streamDomestic contact and bathing 126 504Domestic contact only 124 496
Frequency to streamsday1 to 2 times 122 4883 to 4 times 57 2285+ times 71 284
IPTp-SP uptakeYes 169 676No 81 324
ITN useYes 115 460No 135 540
(gt5000) parasitaemia were 439 (43) 520 (61) and 41(4) respectively About 15 (38) (95 CI 113ndash202) ofthe pregnant women carried concurrent infections with Shaematobium and P falciparum Seventy-nine (316) andsixty (24) women had single infection with S haematobiumand P falciparum respectively
423 Factors Associated with Prevalence and Intensity ofS haematobium Infection S haematobium infection wasassociated with age gravidity status water contact frequency
Journal of Parasitology Research 5
Table 2 Risk factors associated with S haematobium infection among pregnant women in Munyenge
1205942 P value 417 00411205942 Pearson Chi-square test OR odd ratioOR adjusted using multivariate regression analysis
type of activity carried out in the stream and P falciparumparasitaemia in bivariate analysis (Table 2) The prevalenceof infection did not differ significantly with marital statuseducational level and occupational status In multivariate
analysis (controlling for age and gravidity status as con-founders) younger age groups le20 (aOR = 152 95 CI 17ndash1383) and 21ndash25 years (aOR = 73 95 CI 12ndash443) andbathing and domestic contact with stream (aOR = 335 95
6 Journal of Parasitology Research
CI 97ndash1159)were risk factors associatedwith S haematobiuminfection On the other hand less water contact frequency(1 to 2 times per day) (aOR = 28119864 minus 10 95 CI 94119864 minus11ndash85119864minus10) was associated with decreased risk of infectionSurprisingly primigravidity (OR = 02 95 CI 003ndash09)and secundigravidity (OR = 01 95 CI 002ndash04) wereless likely at risk Intensity of infection was associated withmalaria parasitaemia where light egg density infection wasless common (aOR = 04 95 CI 02ndash07 119875 = 0004)in malaria positive women (219 1464) than in malarianegative women (781 5064)
424 Factors Associated with Prevalence of P falciparumInfection The prevalence of P falciparum infection wasassociated (1205942 = 1782 119875 lt 001) with IPTp-SP uptake wheremalaria parasite infection was greater in women who had nottaken IPTp-SP (580) than in those who had at least one SPdose (302) The occurrence of P falciparum infection didnot differ significantly with maternal age gravidity status orITN usage
425 Factors Associated with Prevalence of Coinfection with Shaematobium and P falciparum Coinfection was associatedwith the type of activity carried out in the stream and watercontact frequency as well as IPTp-SP uptake Bathing anddomestic contact with stream (aOR = 133 95 CI 22ndash795) increased risk of coinfection among pregnant womenmeanwhile less water contact frequency (1 to 2 times per day(aOR = 01 95 CI 001ndash04) and 3 to 4 times per day (aOR =03 95 CI 01ndash09)) decreased risk of coinfection Womenwho had at least one SP dose were less likely (aOR= 006 95CI 002ndash02) to be coinfected (Table 3)
43 Haemoglobin Levels and Anaemia Themean (plusmnSD) hae-moglobin level of the pregnant women enrolled in the studywas 90 plusmn 16 gdL (range 61ndash137 gdL) Coinfection signif-icantly reduced Hb levels of pregnant women in the studyarea where levels in coinfected individuals were significantlylower (119875 lt 0001) when compared with levels seen withsingle infections (S haematobium and P falciparum) and noinfection (Table 4) In addition Hb levels were significantlylower among women coinfected with P falciparum and heavyS haematobium infections than in individuals coinfectedwith P falciparum and light S haematobium infection andthose with no infection (Table 5) Although age maritalstatus educational level occupational status infection statusand IPTp-SP uptake were identified as factors associatedwith Hb levels IPTp-SP was seen as the only independentpredictor of Hb levels taking into consideration all possibleconfounding variables (Table 4)
Anaemia prevalence was 888 (222250) with anaemiaseverity as follows mild (132 119899 = 33) moderate (628119899 = 157) and severe (128 119899 = 32) All cases diagnosedwithcoinfection were anaemic (Table 6) Coinfection accountedfor 938 (3032) of all severe anaemia cases with majority719 (2332) of the severe anaemic cases coinfected withP falciparum and heavy density S haematobium infections(Table 5) Uptake of IPTp-SP (438 1432) was associated
(1205942 = 1132 119875 = 001) with reduced percentage of severeanaemia compared with that observed among women withno SP (563 1832) Risk factors found to be associated withincreased odds of anaemia were P falciparum infection (OR=40 95 CI 10ndash145) and occupation (business) (OR = 20195 CI 40ndash101) (Table 6)
5 Discussion
To our knowledge this is the first study carried out on uro-genital schistosomiasis among pregnant women in Camer-oon This study determined the prevalence of S haemato-bium P falciparum and coinfection factors associated withthese infections and assessed their relative effect on anaemiaprevalence and severity among pregnant women in Mun-yenge S haematobium and P falciparum infections are com-mon among pregnant women living in Munyenge and theircoinfection exacerbates anaemia
The prevalence of S haematobium infection among preg-nant women in our study was 468 The high prevalencereflects high exposure to infection among pregnant womenliving in Munyenge due to absolute dependence on naturalwater sources for domestic activities and bathing Comparedto the level of infection in the present study lower prevalenceof urogenital schistosomiasis among pregnant women hasbeen reported inNigeria by Eyo et al [42] (238) and Salawuand Odaibo [43] (208) Differences in the method usedfor the detection of S haematobium infection may partlyexplain the observed differences in rates Although thesestudies attributed the lower prevalence levels of urinary schis-tosomiasis among pregnant women to a taboo restrictingpregnant women from visiting natural water bodies [42]compared with urine filtration method used in our study thelower sensitive centrifugation method use in the diagnosisof S haematobium infection in the Nigerian studies mayhave underestimated true infection levelsMalaria is commonamong pregnant women in the study area with a prevalenceof 392 The only factor seen to be associated with malariaparasite infection in this study site was IPTp uptake Theeffectiveness of IPTp-SP in the prevention of malaria inpregnancy is well established [34 44]
For transmission of schistosomiasis to take place theschistosomes parasite requires an avenue where it is indirect contact with the human host [9] Pregnant womenliving in Munyenge get in contact with infection duringactivities such as laundry plate washing and water fetchingfor domestic use In addition to domestic activities bathingin streams poses a greater risk of infection among pregnantwomen in this area Analyses from other studies have shownthat regularly bathing in water sources contaminated withthe developmental stages of the schistosomes parasite wasassociated with prevalence and intensity of schistosomiasis[45ndash47]Moreover increased risk of infection associatedwiththe number and duration of water contact with infestedwaters per day has also been reported [47] Women whoreported surface-water contact at least 3 to 5 times perday were at greater risk of infection due to longer periodof contact with contaminated water Health education toinstruct pregnant women to make less surface-water contact
Journal of Parasitology Research 7
Table 3 Risk factors associated with coinfection with S haematobium and P falciparum among pregnant women in Munyenge
1205942 119875 value 1329 lt00011205942 Pearson Chi-square test OR odd ratioAdjusted OR using multivariate regression analysis
frequency and the implication of voiding their bladder inwater bodies is paramount These behavioural changes willsignificantly reduce the risk of S haematobium infectionamong pregnant women and contamination of water sourcesin this setting Ultimately provision of portable water andimproved sanitation system will play a major role in decreas-ing disease transmission and incidence
Age as observed in most schistosomiasis surveys was amajor determinant of schistosomes infection among preg-nant women in our study area The highest prevalence val-ues of urogenital schistosomiasis were recorded in youngerwomen (le25 years) Individuals within le20 age group werefound to be at a greater risk of S haematobium infection withprevalence of 554 This is in agreement with trends estab-lished in schistosomiasis surveys carried out in Cameroon
[32 48] and other parts of Africa [42 43] Alternativelythe decrease risk of infection observed in older age groups(gt25 years) conformed to earlier reports [32 42] Studieshave reported that age-acquired immunity to reinfection andchanges in water contact patterns contribute to the decliningtrend in prevalence with increasing age [49] Older womenare less likely to be engaged in water contact behaviourscompared to younger women Age dependent immunity toS haematobium has been shown to affect mean egg outputof infected persons [49] Socioeconomic status of the womenwas not an independent factor associated with S haema-tobium prevalence in this high-risk community Similarlyreports from other rural settings endemic for schistosomi-asis failed to identify any socioeconomic variables that arestrongly associated with schistosomiasis prevalence [50 51]
8 Journal of Parasitology Research
Table 4 Factors associated with mean (plusmnSD) haemoglobin levels among pregnant women in Munyenge Health Area
Factors Category Mean (plusmnSD) Hblevels Test-value Unadjusted
lowastAnalysis of variance test (ANOVA)$Studentrsquos 119905-testampAdjusted 119875 values using multilinear regression analysisNA not applicable variables with 119875 gt 02 in bivariate analysis were not included in regression analysis
Table 5 Association between S haematobium intensity P falciparum infection and mean (plusmnSD) haemoglobin levels and anaemia severity
lowastSignificance level 119865 = 1240 119875 lt 0001lowastAnalysis of variance test (ANOVA)ampPearson Chi-Square test
The absence of association between socioeconomic variablesand infection prevalencemay be attributed to general povertyand uniformity in high exposure risk in the population [50]
The overall prevalence of coinfection with S haema-tobium and P falciparum infection was 152 suggestingcoendemicity of both infections in the study area SimilarlyYatich et al [52] reported a helminth andmalaria coinfectionprevalence of 166 among pregnant women in Ghana Theimpact of helminth infections on malaria parasitaemia and
disease during coinfection is an established phenomenonalthough much is still unknown and contradictions persist[53 54]We observed that light S haematobium infectionwasless common (aOR= 04) among pregnant women coinfectedwith P falciparum suggesting a negative interaction betweenboth parasites [4] In accordance with findings of Getie etal [55] schistosomiasis coinfection could affect Plasmodiumparasitemia and vice versa depending on the intensity of theova in coinfected persons Nonetheless a further study is
Journal of Parasitology Research 9
Table 6 Risk factors associated with anaemia among pregnant women in Munyenge Health Area
Factors Category Anaemia prevalence Adjusted OR (95 CI) 119875 value
Adjusted OR using multivariate regression analysisNA not applicable variables with 119875 gt 02 in bivariate analysis were not included in multivariate analysis
needed to explore the underlying mechanisms of interactionbetween malaria parasitaemia and S haematobium
Schistosomiasis causes long term morbidity such asanaemia Our study showed that the magnitude of S haema-tobium egg counts is significantly related to haemoglobinconcentration confirming that urogenital schistosomiasiscontributes to anaemia [24 25] In this study anaemiawas more pronounced in women with heavy infectionintensity than in those with light infection Coinfection ofhelminth infections and P falciparum increases anaemiaseverity [8 9] Coinfection among pregnant women lowersHb concentration compared with single infection This is inagreement with findings of Okafor and Elenwo [56] Moreso coinfected women with heavy intensity S haematobiuminfection had the lowest mean Hb levels (66 gdL) andthis subpopulation of women contributed to about 72of all severe anaemic cases The combined presence and
interaction of S haematobium and P falciparum infectionsis partly responsible for the low haemoglobin concentrationin women with concurrent infectionMalaria causes anaemiaby destruction and removal of parasitized red blood cellsand shortening of the life span of nonparasitized red cellsas well as decreasing the rate of erythrocyte production inbone marrow [57]Themechanism by which schistosomiasiscauses anaemia is not fully understood but it is suggested thathelminth infections could contribute to increase in the preva-lence of inflammatory syndromes impairing erythropoiesisand interfering with mobilization of reticuloendothelial ironstorages and shortening erythrocyte survival [58] Similar toprevious reports of a study in Uganda [59] malaria parasiteinfection was an independent factor associated with increaseanaemia risk
The risk of coinfection was associated with streamusage (bathing and domestic contact with stream) while
10 Journal of Parasitology Research
less water contact and SP usage decreased risk of infectionThis finding suggests that intervention strategies focusingon combating malaria and schistosomiasis respectively byincreasing the uptake of IPTp-SPdoses and less water contactamong pregnant women living in Munyenge represents themost appropriate prevention of coinfection with consequentincrease in Hb levels
This study had one limitation We did not investigate theprevalence of HIV infection among the study participants Ithas been shown that coinfections with helminths andmalariacause considerable morbidity in the host particularly in thepresence of HIV infection [60]
To conclude the study has indicated that S haematobiumand P falciparum infections are common among pregnantwomen living in Munyenge and their coinfection is influ-enced by high frequencies of these parasites in the same pop-ulationThe study also revealed that younger age and bathingand domestic contact with stream are independently associ-ated with prevalence of S haematobium infection while noIPTp-SP was associated with P falciparum infection Streamusage increased risk of coinfection while less water contactand SP usage decreased its risk The fact that light S haema-tobium infection was less common in P falciparum infectedwomen suggests that Plasmodium falciparum parasitaemiamay be associatedwith intensity of urogenital schistosomiasisin coinfected individuals Anaemia is a severe public healthproblem in pregnancy in Munyenge and coinfection withS haematobium and P falciparum exacerbates anaemiaLess water contact frequency and increase uptake of IPTp-SPdoses will significantly reduce risk of coinfection andconsequently anaemia severity in pregnancy in this setting
Abbreviations
IPTp-SP Intermittent preventive treatment in pregnancy(IPTp) with sulfadoxine-pyrimethamine (SP)
ITN Insecticide treated bed netsHIV Human immunodeficiency virusANC Antenatal care
Competing Interests
The authors declare that they do not have any competinginterests
Authorsrsquo Contributions
Judith K Anchang-Kimbi conceived and designed the studyanalyzed the data and wrote the manuscript Dillys MansohElad participated in the design of the study performedthe experiments and made inputs in manuscript write-upGemain Taiwe Sotoing and Eric Akum Achidi supervisedreviewed and provided inputs to the manuscript All authorsread and approved the final manuscript
Acknowledgments
The authors are grateful to all the pregnant women whogave their consent to participate in the study Special thanks
are due to the chief medical officer nurses and laboratorytechnician of the Munyenge Health Centre for their cooper-ation and contribution This study received financial supportfrom the Ministry of Higher Education University ResearchModernisation grant given to authors Judith K Anchang-Kimbi and Eric Akum Achidi
References
[1] T N Petney and R H Andrews ldquoMultiparasite communitiesin animals and humans frequency structure and pathogenicsignificancerdquo International Journal for Parasitology vol 28 no3 pp 377ndash393 1998
[2] F E G Cox ldquoConcomitant infections parasites and immuneresponsesrdquo Parasitology vol 122 supplement 1 pp S23ndashS382001
[3] M Nacher P Singhasivanon S Yimsamran et al ldquoIntestinalhelminth infections are associated with increased incidenceof Plasmodium falciparum malaria in Thailandrdquo Journal ofParasitology vol 88 no 1 pp 55ndash58 2002
[4] J-Y Le Hesran J Akiana E H M Ndiaye M Dia P Senghorand L Konate ldquoSevere malaria attack is associated with highprevalence of Ascaris lumbricoides infection among childrenin rural Senegalrdquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 98 no 7 pp 397ndash399 2004
[5] M Nacher F Gay P Singhasivanon et al ldquoAscaris lumbricoidesinfection is associated with protection from cerebral malariardquoParasite Immunology vol 22 no 3 pp 107ndash113 2000
[6] V Briand L Watier J-Y Le Hesran A Garcia and M CotldquoCoinfection with Plasmodium falciparum and Schistosomahaematobium protective effect of schistosomiasis on malariain Senegalese childrenrdquo American Journal of Tropical Medicineand Hygiene vol 72 no 6 pp 702ndash707 2005
[7] N Oslash Christensen P Furu J Kurtzhals and A OdaiboldquoHeterologous synergistic interactions in concurrent experi-mental infection in the mouse with Schistosoma mansoniEchinostoma revolution Plasmodium yoelii Babesia microtiand Trypanosoma bruceirdquo Parasitology Research vol 74 no 6pp 544ndash551 1988
[8] G Raso A Luginbuhl C A Adjoua et al ldquoMultiple parasiteinfections and their relationship to self-reported morbidity ina community of rural Cote drsquoIvoirerdquo International Journal ofEpidemiology vol 33 no 5 pp 1092ndash1102 2004
[9] S Brooker W Akhwale R Pullan et al ldquoEpidemiology ofPlasmodium-helminth co-infection in Africa populations atrisk potential impact on anemia and prospects for combiningcontrolrdquo American Journal of Tropical Medicine and Hygienevol 77 no 6 pp 88ndash98 2007
[10] C E Shulman and E K Dorman ldquoReducing childhood mor-tality in poor countries importance and prevention of malariain pregnancyrdquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 97 no 1 pp 30ndash35 2003
[11] WorldHealthOrganisation andAfrica Regional OfficeMalariaPrevention and Control during Pregnancy in the African RegionWHOAFRO Brazzaville Congo 2004
[12] D Engels L Chitsulo A Montresor and L Savioli ldquoTheglobal epidemiological situation of schistosomiasis and newapproaches to control and researchrdquo Acta Tropica vol 82 no2 pp 139ndash146 2002
[13] P J Hotez and A Kamath ldquoNeglected tropical diseases in sub-Saharan Africa review of their prevalence distribution and
[14] M J Van Der Werf S J De Vlas S Brooker et al ldquoQuantifica-tion of clinical morbidity associated with schistosome infectionin sub-Saharan Africardquo Acta Tropica vol 86 no 2-3 pp 125ndash139 2003
[15] M N Nour ldquoSchistosomias health effect on womenrdquo Reviewsin Obstetrics amp Gynecology vol 3 no 1 pp 28ndash32 2010
[16] J F Friedman P Mital H K Kanzaria G R Olds and J DKurtis ldquoSchistosomiasis and pregnancyrdquo Trends in Parasitologyvol 23 no 4 pp 159ndash164 2007
[17] httpwwwwhointschistosomiasisstrategyen[18] H N Ntonifor and J A Ajayi ldquoWater contact and Schistosoma
haematobium infection A case study of some communitiesin Toro Local Government council Area (TLGCA) of BauchiStaterdquoNigeria Journal of Natural and Applied Sciences vol 1 no1 pp 54ndash59 2005
[19] P Saotoing T Vroumsia A M Njan F N Tchuenguem andJ Messi ldquoEpidemiological survey of schistosomiasis due toSchistosoma haematobium in some primary schools in thetown of Maroua far north region Cameroonrdquo InternationalJournal of Tropical Medicine vol 6 no 2 pp 19ndash24 2011
[20] L A Tchuem Tchuente R I K Ngassam L Sumo et al ldquoMap-ping of schistosomiasis and soil- transmitted helminthiasis inthe regions of centre east and west cameroonrdquo PLoS NeglectedTropical Diseases vol 6 no 3 p e1553 2012
[21] L A Tchuem Tchuente N C Dongmo P Ngassam et alldquoMapping of schistosomiasis and soil- transmitted helminthi-asis in the regions of Littoral North-West South and South-West Cameroon and recommendations for treatmentrdquo BMCInfectious Disease vol 13 article 602 2013
[22] K J N Ndamukong M A Ayuk J S Dinga T N Akenji VA Ndiforchu and V P K Titanji ldquoPrevalence and intensity ofurinary schistosomiasis in primary school children of the KottoBarombi health area Cameroonrdquo East African Medical Journalvol 78 no 6 pp 287ndash289 2001
[23] H N Ntonifor G N Mbunkur and N W Ndaleh ldquoEpidemi-ological survey of urinary schistosomiasis in some primaryschools in a new focus behind Mount Cameroon (Munyenge)South West Region Cameroonrdquo East African Medical Journalvol 89 no 3 pp 82ndash88 2012
[24] J F Friedman H K Kanzaria and S T McGarvey ldquoHumanschistosomiasis and anemia the relationship and potentialmechanismsrdquo Trends in Parasitology vol 21 no 8 pp 386ndash3922005
[25] A Ajanga N J S Lwambo L Blair U Nyandindi A Fenwickand S Brooker ldquoSchistosoma mansoni in pregnancy andassociations with anaemia in northwest Tanzaniardquo Transactionsof the Royal Society of Tropical Medicine and Hygiene vol 100no 1 pp 59ndash63 2006
[26] G Helling-Giese E F Kjetland S G Gundersen et al ldquoSchis-tosomiasis in women manifestations in the upper reproductivetractrdquo Acta Tropica vol 62 no 4 pp 225ndash238 1996
[27] R W Steketee B L Nahlen M E Parise and C MenendezldquoTheburden ofmalaria in pregnancy inmalaria-endemic areasrdquoAmerican Journal of Tropical Medicine and Hygiene vol 64 no1-2 pp 28ndash35 2001
[28] V V Laxman B Adamson and T Mahmood ldquoRecurrentectopic pregnancy due to Schistosoma hematobiumrdquo Journal ofObstetrics and Gynaecology vol 28 no 4 pp 461ndash462 2008
[29] S Bahrami H Alatassi S P Slone and D M OrsquoConnorldquoTubal gestation and schistosomiasis a case reportrdquo Journal ofReproductiveMedicine for theObstetrician andGynecologist vol51 no 7 pp 595ndash598 2006
[30] P S Mbabazi O Andan D W Fitzgerald L Chitsulo DEngels and J A Downs ldquoExamining the relationship betweenurogenital schistosomiasis and HIV infectionrdquo PLoS NeglectedTropical Diseases vol 5 no 12 Article ID e1396 2011
[31] R Tweyongyere P A Mawa N O Emojong et al ldquoEffectof praziquantel treatment of Schistosomamansoni during preg-nancy on intensity of infection and antibody responses to schis-tosome antigens results of a randomised placebo-controlledtrialrdquo BMC Infectious Diseases vol 9 article 32 2009
[32] H N Ntonifor A E Green M O S Bopda et al ldquoEpi-demiology of urinary schistosomiasis and soil transmittedhelminthiasis in a recently established focus behind MountCameroonrdquo International Journal of Current Microbiology andApplied Sciences vol 4 no 3 pp 1056ndash1066 2015
[33] S Wanji A J Kengne-Ouafo E E Joan Eyong et al ldquoGeneticdiversity of Plasmodium falciparummerozoite surface protein-1 block 2 in sites of contrasting altitudes and malaria endemic-ities in the Mount Cameroon Regionrdquo American Journal ofTropical Medicine and Hygiene vol 86 no 5 pp 764ndash774 2012
[34] J K Anchang-Kimbi E A Achidi B Nkegoum E Sverremark-Ekstrom and M Troye-Blomberg ldquoDiagnostic comparisonof malaria infection in peripheral blood placental blood andplacental biopsies in Cameroonian parturient womenrdquoMalariaJournal vol 8 no 1 article 126 2009
[35] F J Bryan The Design and Analysis of Research Studies Uni-versity ofOtago Dunedin NewZealand CambridgeUniversityPress Cambridge UK 1992
[36] World Health Organisation Haemoglobin Concentrations forthe Diagnosis of Anaemia and Assessment of Severity Vitaminand mineral Nutrition Information System WHO GenevaSwitzerland 2011
[37] M CheesbroughDistrict Laboratory Practice in Tropical Coun-tries Cambridge University Press Cambridge UK 2006
[39] N O Christensen G Gotsche and F Frandsen ParasitologicalTechniques for Use in Routine Laboratory Maintainance of Schis-tosomes and Used in Studies on the Epidemiology of Human andBovine Schistosomiasis Danish Bilhaziasis Laboratory Manual1984
[40] World Health OrganizationmdashTropical Disease Research TDRstrategic direction Schistosomiasis WHO-TDR 2002
[41] World Health OrganizationGuidelines for the Evaluation of SoilTransmitted Helminthiasis and Schistosomiasis at CommunityLevel A Guide for Managers of Control Programme WHOGeneva Switzerland 1993
[42] J E Eyo G C Onyishi and F C Okafor ldquoUrinary schisto-somiasis among pregnant women in some endemic tropicalsemi-urban communities of Anambra State Nigeriardquo TropicalBiomedicine vol 29 no 4 pp 575ndash579 2012
[43] O T Salawu and A B Odaibo ldquoSchistosomiasis among preg-nant women in rural communities in Nigeriardquo InternationalJournal of Gynecology andObstetrics vol 122 no 1 pp 1ndash4 2013
[44] K R Tan B L Katalenich K E Mace et al ldquoEfficacyof sulphadoxine-pyrimethamine for intermittent preventivetreatment of malaria in pregnancy Mansa Zambiardquo MalariaJournal vol 13 no 1 article 227 2014
12 Journal of Parasitology Research
[45] J Bethony J T Williams H Kloos et al ldquoExposure toSchistosoma mansoni infection in a rural area in Brazil IIhousehold risk factorsrdquo Tropical Medicine and InternationalHealth vol 6 no 2 pp 136ndash145 2001
[46] J C Sousa-Figueiredo D Gamboa J M Pedro et al ldquoEpi-demiology of malaria schistosomiasis geohelminths anemiaand malnutrition in the context of a demographic surveillancesystem in northern Angolardquo PLoS ONE vol 7 no 4 Article IDe33189 2012
[47] F Anto V Asoala M Adjuik et al ldquoWater contact activitiesand prevalence of schistosomiasis infection among school-agechildren in communities along an irrigation scheme in RuralNorthern Ghanardquo Journal of Bacteriology amp Parasitology vol 4article 177 2013
[48] L-A Tchuem Tchuente J M Behnke F S Gilbert V RSouthgate and J Vercruysse ldquoPolyparasitism with Schistosomahaematobium and soil-transmitted helminth infections amongschool children in Loum Cameroonrdquo Tropical Medicine andInternational Health vol 8 no 11 pp 975ndash986 2003
[49] J-F Etard M Audibert and A Dabo ldquoAge-acquired resistanceand predisposition to reinfection with Schistosoma haemato-bium after treatment with praziquantel in Malirdquo The AmericanJournal of TropicalMedicine andHygiene vol 52 no 6 pp 549ndash558 1995
[50] A Gazzinelli G Velasquez-Melendez S B Crawford P TLoVerde R Correa-Oliveira and H Kloos ldquoSocioeconomicdeterminants of schistosomiasis in a poor rural area in BrazilrdquoActa Tropica vol 99 no 2-3 pp 260ndash271 2006
[51] A P Kapito-Tembo V Mwapasa S R Meshnick et al ldquoPreva-lence distribution and risk factors for Schistosoma hematobiuminfection among school children in Blantyre Malawirdquo PLoSNeglected Tropical Diseases vol 3 no 1 article e361 2009
[52] N J Yatich J Yi T Agbenyega et al ldquoMalaria and intestinalhelminth co-infection among pregnant women in Ghanaprevalence and risk factorsrdquo The American Journal of TropicalMedicine and Hygiene vol 80 no 6 pp 896ndash901 2009
[53] M Nacher ldquoInteractions between worms and malaria goodworms or bad wormsrdquoMalaria Journal vol 10 article no 2592011
[54] A A Adegnika and P G Kremsner ldquoEpidemiology of malariaand helminth interaction a review from 2001 to 2011rdquo CurrentOpinion in HIV and AIDS vol 7 no 3 pp 221ndash224 2012
[55] S Getie Y Wondimeneh G Getnet et al ldquoPrevalence andclinical correlates of Schistosoma mansoni co-infection amongmalaria infected patients Northwest Ethiopiardquo BMC ResearchNotes vol 8 no 1 article no 480 2015
[56] E Okafor and A Elenwo ldquoHaemoglobin status of children withmixed infection ofmalaria and urinary schistosomiasis inOdauCommunity Rivers state Nigeriardquo Journal of Agriculture andSocial Research vol 7 no 1 pp 56ndash62 2008
[57] M A McDevitt J Xie V Gordeuk and R Bucala ldquoThe anemiaof malaria infection role of inflammatory cytokinesrdquo CurrentHematology Reports vol 3 no 2 pp 97ndash106 2004
[58] J G Shaw and J F Friedman ldquoIron deficiency anemia focus oninfectious diseases in lesser developed countriesrdquo Anemia vol2011 Article ID 260380 10 pages 2011
[59] H K Green J C Sousa-Figueiredo M-G Basanez et alldquoAnaemia in Ugandan preschool-aged children the relativecontribution of intestinal parasites and malariardquo Parasitologyvol 138 no 12 pp 1534ndash1545 2011
[60] E Ivan N J Crowther E Mutimura L O Osuwat S Janssenand M P Grobusch ldquoHelminthic infections rates and malaria
in HIV-infected pregnant women on anti-retroviral therapy inRwandardquo PLoS Neglected Tropical Diseases vol 7 no 8 ArticleID e2380 2013
Figure 1 Map showing the location of Munyenge in Mount Cameroon Area
their consent were enrolled consecutively Pregnant womenwere interviewed by a field researcher using a questionnairewhich recorded demographic information (age residence)gynaecologicobstetric history (gravidity status gestationalage and pregnancy complications) socioeconomic indica-tors (educational level occupation) and questions relatedto malaria (IPTp-SP uptake ITN usage) and schistosomiasis(main household water source frequency of contact withopen water source and domestic activities carried out in thestream) In addition to the questionnaire interview womenwere asked to collect urine in supplied 20mL screw top plasticcontainers between 1000 am and 200 pmThe samples werestored in a cool box during transportation to the Universityof Buea Medical Research Laboratory and processed within24 hours of collection
31 Laboratory Analyses
311 Anaemia Status Determination Haemoglobin levelswere determined from finger-prick blood samples using aportable battery-operated photometer (HemoCue) (Hemo-Cue 201+ system HemoCue Angelholm Sweden) (URIT-12) Hb concentration was expressed in gdL Anaemia wasdefined as an Hb value lt 110 gdL [36] Anaemia severitywas defined as follows mild anaemia (Hb 10ndash109 gdL)moderate anaemia (Hb 7ndash99 gdL) and severe anaemia (Hblt 70 gdL) [36]
312 Parasitological Examination Malaria parasites wereidentified on thick and thin blood smears stained with 5Giemsa The smears were observed for 30 minutes underthe times100 (oil immersion) objective of a UNICO lightmicroscope [37] Malaria parasite density was estimated bycounting parasites against 200 leucocytes in thick smearsassuming a white cell count of 8000 leucocytes per 120583Lof blood [38] Malaria parasite density was classified into
lt500 501ndash5000 and gt5000 for low moderate and highparasitaemia respectively [38] S haematobium eggs wereidentified in urine samples using the filtration technique [39]In brief 10mls of urine was filtered using membrane filters(Sterlitech Polycarbonate (PCTE) membrane filters USA)and the egg count was recorded per 10mls of urine Theinfection intensity was classified as light (lt50 eggs10mL ofurine) or heavy (ge50 eggs10mL of urine) as defined by theWorld Health Organization (WHO) [40] Microhaematuriawas used as proxy-diagnosis of urogenital schistosomiasis anaccepted marker in the rapid diagnosis of S haematobiuminfection in urine [41] Samples were tested for microhaema-turia using urine reagent strips (Uripath Plasmatec Labo-ratory UK) (Combi-11) as per manufacturer instructionsResults were expressed as negative or in levels of positivity(+ ++ or +++) and not including traces A pregnant womanwas infected with S haematobium when she was diagnosedpositive by microscopic examination andor urine reagentstrip
32 Statistical Analysis The data was analyzed using SPSSversion 190 (SPSS Inc Chicago IL USA) Proportions ofS haematobium P falciparum and coinfection and anaemiastatus were compared between different groups (age groupsgravidity status educational level occupational status streamusage and activities and IPTp-SP uptake) using Pearson Chi-square test Crude odds ratios were estimated and factorsassociated with infections and anaemia to be included inthe multivariate logistic regression model were identifiedVariables that had a 119875 value lt 020 in bivariate analysiswere included in the multivariate logistic regression modelUsing the enter method variables that showed independentassociation with infections and anaemia status at a signifi-cance level of 119875 lt 005 were retained in the model MeanHb levels were compared between groups using Analysis ofVariance test (ANOVA) and Studentrsquos t-test Independent
4 Journal of Parasitology Research
factors associated with Hb levels were obtained using mul-tilinear regression analysis 119875 values lt 005 were consideredsignificant
33 Ethical Considerations The study protocol and designincluding the consent procedures were approved by the Insti-tutional Ethics ReviewBoard of the Faculty ofHealth ScienceUniversity of Buea and the Buea Regional Delegation ofPublic Health Prior to conducting the study the aim ofthe study and procedures to be used to collect data wereexplained to the pregnant women at the ANC clinic Written(from those who can read and write) or verbal (from thosewho cannot read and write) informed consent from all studyparticipants was obtained Each pregnant womanwho agreedto participate in the study was enrolled and given urinesample container to collect urine Participationwas voluntaryand study participants were assured of confidentiality andanonymity of data
4 Results
41 Characteristics of the Study Population In this cross-sectional study a total of 250 pregnant women reportingfor antenatal care was enrolled The mean age of the studyparticipants was 25 plusmn 521 years (range 14ndash40 years) Themajority (752) of the women were married All the studyparticipants had at least a primary education and about 50had obtained some form of secondary education Although ahigher proportion of the women had been enrolled for firstANC in the second trimester more than 40 had late clinicregistration About two-thirds of women reported taking atleast one dose of IPTp-SP and 46 reported having sleptunder a bed net the previous night The stream was the mainsource of water (99 stream usage) for domestic use andbathing The characteristics of the study sample are shown inTable 1
42 Prevalence and Intensity of Infection
421 S haematobium Infection Of the 250 volunteer preg-nant women enrolled 117 (468 95 CI 41ndash53) were pos-itive for S haematobium infection among whom 53 (453)had heavy (ge50 eggs10mL of urine) infection while 547(64) had light (lt50 eggs10mL of urine) infectionThe preva-lence of microhaematuria was 96 (24250) Using micro-scopic urine examination as gold standard the specificity andsensitivity ofmicrohaematuria in the diagnosis of S haemato-bium infection were 100 (95CI 972ndash100) and 205 (95CI 142ndash287) respectively Microhaematuria was stronglyrelated to egg density categories where microhaematuria wascommon (1205942 = 823 119875 = 0004) among women with heavyegg load (727) than in those with light infection (273)
422 P falciparum Infection The overall prevalence of Pfalciparum parasitaemia among the study participants was392 (98) (95 CI 334ndash454) Of the 98 pregnant womeninfected with P falciparum the proportions of low (lt500parasites120583L of blood) moderate (501ndash5000) and high
Table 1 Characteristics of the study participants
Characteristics Number examined (N) ()Age group (years)le20 56 22421ndash25 79 31626ndash30 71 284gt30 44 176
Activities in the streamDomestic contact and bathing 126 504Domestic contact only 124 496
Frequency to streamsday1 to 2 times 122 4883 to 4 times 57 2285+ times 71 284
IPTp-SP uptakeYes 169 676No 81 324
ITN useYes 115 460No 135 540
(gt5000) parasitaemia were 439 (43) 520 (61) and 41(4) respectively About 15 (38) (95 CI 113ndash202) ofthe pregnant women carried concurrent infections with Shaematobium and P falciparum Seventy-nine (316) andsixty (24) women had single infection with S haematobiumand P falciparum respectively
423 Factors Associated with Prevalence and Intensity ofS haematobium Infection S haematobium infection wasassociated with age gravidity status water contact frequency
Journal of Parasitology Research 5
Table 2 Risk factors associated with S haematobium infection among pregnant women in Munyenge
1205942 P value 417 00411205942 Pearson Chi-square test OR odd ratioOR adjusted using multivariate regression analysis
type of activity carried out in the stream and P falciparumparasitaemia in bivariate analysis (Table 2) The prevalenceof infection did not differ significantly with marital statuseducational level and occupational status In multivariate
analysis (controlling for age and gravidity status as con-founders) younger age groups le20 (aOR = 152 95 CI 17ndash1383) and 21ndash25 years (aOR = 73 95 CI 12ndash443) andbathing and domestic contact with stream (aOR = 335 95
6 Journal of Parasitology Research
CI 97ndash1159)were risk factors associatedwith S haematobiuminfection On the other hand less water contact frequency(1 to 2 times per day) (aOR = 28119864 minus 10 95 CI 94119864 minus11ndash85119864minus10) was associated with decreased risk of infectionSurprisingly primigravidity (OR = 02 95 CI 003ndash09)and secundigravidity (OR = 01 95 CI 002ndash04) wereless likely at risk Intensity of infection was associated withmalaria parasitaemia where light egg density infection wasless common (aOR = 04 95 CI 02ndash07 119875 = 0004)in malaria positive women (219 1464) than in malarianegative women (781 5064)
424 Factors Associated with Prevalence of P falciparumInfection The prevalence of P falciparum infection wasassociated (1205942 = 1782 119875 lt 001) with IPTp-SP uptake wheremalaria parasite infection was greater in women who had nottaken IPTp-SP (580) than in those who had at least one SPdose (302) The occurrence of P falciparum infection didnot differ significantly with maternal age gravidity status orITN usage
425 Factors Associated with Prevalence of Coinfection with Shaematobium and P falciparum Coinfection was associatedwith the type of activity carried out in the stream and watercontact frequency as well as IPTp-SP uptake Bathing anddomestic contact with stream (aOR = 133 95 CI 22ndash795) increased risk of coinfection among pregnant womenmeanwhile less water contact frequency (1 to 2 times per day(aOR = 01 95 CI 001ndash04) and 3 to 4 times per day (aOR =03 95 CI 01ndash09)) decreased risk of coinfection Womenwho had at least one SP dose were less likely (aOR= 006 95CI 002ndash02) to be coinfected (Table 3)
43 Haemoglobin Levels and Anaemia Themean (plusmnSD) hae-moglobin level of the pregnant women enrolled in the studywas 90 plusmn 16 gdL (range 61ndash137 gdL) Coinfection signif-icantly reduced Hb levels of pregnant women in the studyarea where levels in coinfected individuals were significantlylower (119875 lt 0001) when compared with levels seen withsingle infections (S haematobium and P falciparum) and noinfection (Table 4) In addition Hb levels were significantlylower among women coinfected with P falciparum and heavyS haematobium infections than in individuals coinfectedwith P falciparum and light S haematobium infection andthose with no infection (Table 5) Although age maritalstatus educational level occupational status infection statusand IPTp-SP uptake were identified as factors associatedwith Hb levels IPTp-SP was seen as the only independentpredictor of Hb levels taking into consideration all possibleconfounding variables (Table 4)
Anaemia prevalence was 888 (222250) with anaemiaseverity as follows mild (132 119899 = 33) moderate (628119899 = 157) and severe (128 119899 = 32) All cases diagnosedwithcoinfection were anaemic (Table 6) Coinfection accountedfor 938 (3032) of all severe anaemia cases with majority719 (2332) of the severe anaemic cases coinfected withP falciparum and heavy density S haematobium infections(Table 5) Uptake of IPTp-SP (438 1432) was associated
(1205942 = 1132 119875 = 001) with reduced percentage of severeanaemia compared with that observed among women withno SP (563 1832) Risk factors found to be associated withincreased odds of anaemia were P falciparum infection (OR=40 95 CI 10ndash145) and occupation (business) (OR = 20195 CI 40ndash101) (Table 6)
5 Discussion
To our knowledge this is the first study carried out on uro-genital schistosomiasis among pregnant women in Camer-oon This study determined the prevalence of S haemato-bium P falciparum and coinfection factors associated withthese infections and assessed their relative effect on anaemiaprevalence and severity among pregnant women in Mun-yenge S haematobium and P falciparum infections are com-mon among pregnant women living in Munyenge and theircoinfection exacerbates anaemia
The prevalence of S haematobium infection among preg-nant women in our study was 468 The high prevalencereflects high exposure to infection among pregnant womenliving in Munyenge due to absolute dependence on naturalwater sources for domestic activities and bathing Comparedto the level of infection in the present study lower prevalenceof urogenital schistosomiasis among pregnant women hasbeen reported inNigeria by Eyo et al [42] (238) and Salawuand Odaibo [43] (208) Differences in the method usedfor the detection of S haematobium infection may partlyexplain the observed differences in rates Although thesestudies attributed the lower prevalence levels of urinary schis-tosomiasis among pregnant women to a taboo restrictingpregnant women from visiting natural water bodies [42]compared with urine filtration method used in our study thelower sensitive centrifugation method use in the diagnosisof S haematobium infection in the Nigerian studies mayhave underestimated true infection levelsMalaria is commonamong pregnant women in the study area with a prevalenceof 392 The only factor seen to be associated with malariaparasite infection in this study site was IPTp uptake Theeffectiveness of IPTp-SP in the prevention of malaria inpregnancy is well established [34 44]
For transmission of schistosomiasis to take place theschistosomes parasite requires an avenue where it is indirect contact with the human host [9] Pregnant womenliving in Munyenge get in contact with infection duringactivities such as laundry plate washing and water fetchingfor domestic use In addition to domestic activities bathingin streams poses a greater risk of infection among pregnantwomen in this area Analyses from other studies have shownthat regularly bathing in water sources contaminated withthe developmental stages of the schistosomes parasite wasassociated with prevalence and intensity of schistosomiasis[45ndash47]Moreover increased risk of infection associatedwiththe number and duration of water contact with infestedwaters per day has also been reported [47] Women whoreported surface-water contact at least 3 to 5 times perday were at greater risk of infection due to longer periodof contact with contaminated water Health education toinstruct pregnant women to make less surface-water contact
Journal of Parasitology Research 7
Table 3 Risk factors associated with coinfection with S haematobium and P falciparum among pregnant women in Munyenge
1205942 119875 value 1329 lt00011205942 Pearson Chi-square test OR odd ratioAdjusted OR using multivariate regression analysis
frequency and the implication of voiding their bladder inwater bodies is paramount These behavioural changes willsignificantly reduce the risk of S haematobium infectionamong pregnant women and contamination of water sourcesin this setting Ultimately provision of portable water andimproved sanitation system will play a major role in decreas-ing disease transmission and incidence
Age as observed in most schistosomiasis surveys was amajor determinant of schistosomes infection among preg-nant women in our study area The highest prevalence val-ues of urogenital schistosomiasis were recorded in youngerwomen (le25 years) Individuals within le20 age group werefound to be at a greater risk of S haematobium infection withprevalence of 554 This is in agreement with trends estab-lished in schistosomiasis surveys carried out in Cameroon
[32 48] and other parts of Africa [42 43] Alternativelythe decrease risk of infection observed in older age groups(gt25 years) conformed to earlier reports [32 42] Studieshave reported that age-acquired immunity to reinfection andchanges in water contact patterns contribute to the decliningtrend in prevalence with increasing age [49] Older womenare less likely to be engaged in water contact behaviourscompared to younger women Age dependent immunity toS haematobium has been shown to affect mean egg outputof infected persons [49] Socioeconomic status of the womenwas not an independent factor associated with S haema-tobium prevalence in this high-risk community Similarlyreports from other rural settings endemic for schistosomi-asis failed to identify any socioeconomic variables that arestrongly associated with schistosomiasis prevalence [50 51]
8 Journal of Parasitology Research
Table 4 Factors associated with mean (plusmnSD) haemoglobin levels among pregnant women in Munyenge Health Area
Factors Category Mean (plusmnSD) Hblevels Test-value Unadjusted
lowastAnalysis of variance test (ANOVA)$Studentrsquos 119905-testampAdjusted 119875 values using multilinear regression analysisNA not applicable variables with 119875 gt 02 in bivariate analysis were not included in regression analysis
Table 5 Association between S haematobium intensity P falciparum infection and mean (plusmnSD) haemoglobin levels and anaemia severity
lowastSignificance level 119865 = 1240 119875 lt 0001lowastAnalysis of variance test (ANOVA)ampPearson Chi-Square test
The absence of association between socioeconomic variablesand infection prevalencemay be attributed to general povertyand uniformity in high exposure risk in the population [50]
The overall prevalence of coinfection with S haema-tobium and P falciparum infection was 152 suggestingcoendemicity of both infections in the study area SimilarlyYatich et al [52] reported a helminth andmalaria coinfectionprevalence of 166 among pregnant women in Ghana Theimpact of helminth infections on malaria parasitaemia and
disease during coinfection is an established phenomenonalthough much is still unknown and contradictions persist[53 54]We observed that light S haematobium infectionwasless common (aOR= 04) among pregnant women coinfectedwith P falciparum suggesting a negative interaction betweenboth parasites [4] In accordance with findings of Getie etal [55] schistosomiasis coinfection could affect Plasmodiumparasitemia and vice versa depending on the intensity of theova in coinfected persons Nonetheless a further study is
Journal of Parasitology Research 9
Table 6 Risk factors associated with anaemia among pregnant women in Munyenge Health Area
Factors Category Anaemia prevalence Adjusted OR (95 CI) 119875 value
Adjusted OR using multivariate regression analysisNA not applicable variables with 119875 gt 02 in bivariate analysis were not included in multivariate analysis
needed to explore the underlying mechanisms of interactionbetween malaria parasitaemia and S haematobium
Schistosomiasis causes long term morbidity such asanaemia Our study showed that the magnitude of S haema-tobium egg counts is significantly related to haemoglobinconcentration confirming that urogenital schistosomiasiscontributes to anaemia [24 25] In this study anaemiawas more pronounced in women with heavy infectionintensity than in those with light infection Coinfection ofhelminth infections and P falciparum increases anaemiaseverity [8 9] Coinfection among pregnant women lowersHb concentration compared with single infection This is inagreement with findings of Okafor and Elenwo [56] Moreso coinfected women with heavy intensity S haematobiuminfection had the lowest mean Hb levels (66 gdL) andthis subpopulation of women contributed to about 72of all severe anaemic cases The combined presence and
interaction of S haematobium and P falciparum infectionsis partly responsible for the low haemoglobin concentrationin women with concurrent infectionMalaria causes anaemiaby destruction and removal of parasitized red blood cellsand shortening of the life span of nonparasitized red cellsas well as decreasing the rate of erythrocyte production inbone marrow [57]Themechanism by which schistosomiasiscauses anaemia is not fully understood but it is suggested thathelminth infections could contribute to increase in the preva-lence of inflammatory syndromes impairing erythropoiesisand interfering with mobilization of reticuloendothelial ironstorages and shortening erythrocyte survival [58] Similar toprevious reports of a study in Uganda [59] malaria parasiteinfection was an independent factor associated with increaseanaemia risk
The risk of coinfection was associated with streamusage (bathing and domestic contact with stream) while
10 Journal of Parasitology Research
less water contact and SP usage decreased risk of infectionThis finding suggests that intervention strategies focusingon combating malaria and schistosomiasis respectively byincreasing the uptake of IPTp-SPdoses and less water contactamong pregnant women living in Munyenge represents themost appropriate prevention of coinfection with consequentincrease in Hb levels
This study had one limitation We did not investigate theprevalence of HIV infection among the study participants Ithas been shown that coinfections with helminths andmalariacause considerable morbidity in the host particularly in thepresence of HIV infection [60]
To conclude the study has indicated that S haematobiumand P falciparum infections are common among pregnantwomen living in Munyenge and their coinfection is influ-enced by high frequencies of these parasites in the same pop-ulationThe study also revealed that younger age and bathingand domestic contact with stream are independently associ-ated with prevalence of S haematobium infection while noIPTp-SP was associated with P falciparum infection Streamusage increased risk of coinfection while less water contactand SP usage decreased its risk The fact that light S haema-tobium infection was less common in P falciparum infectedwomen suggests that Plasmodium falciparum parasitaemiamay be associatedwith intensity of urogenital schistosomiasisin coinfected individuals Anaemia is a severe public healthproblem in pregnancy in Munyenge and coinfection withS haematobium and P falciparum exacerbates anaemiaLess water contact frequency and increase uptake of IPTp-SPdoses will significantly reduce risk of coinfection andconsequently anaemia severity in pregnancy in this setting
Abbreviations
IPTp-SP Intermittent preventive treatment in pregnancy(IPTp) with sulfadoxine-pyrimethamine (SP)
ITN Insecticide treated bed netsHIV Human immunodeficiency virusANC Antenatal care
Competing Interests
The authors declare that they do not have any competinginterests
Authorsrsquo Contributions
Judith K Anchang-Kimbi conceived and designed the studyanalyzed the data and wrote the manuscript Dillys MansohElad participated in the design of the study performedthe experiments and made inputs in manuscript write-upGemain Taiwe Sotoing and Eric Akum Achidi supervisedreviewed and provided inputs to the manuscript All authorsread and approved the final manuscript
Acknowledgments
The authors are grateful to all the pregnant women whogave their consent to participate in the study Special thanks
are due to the chief medical officer nurses and laboratorytechnician of the Munyenge Health Centre for their cooper-ation and contribution This study received financial supportfrom the Ministry of Higher Education University ResearchModernisation grant given to authors Judith K Anchang-Kimbi and Eric Akum Achidi
References
[1] T N Petney and R H Andrews ldquoMultiparasite communitiesin animals and humans frequency structure and pathogenicsignificancerdquo International Journal for Parasitology vol 28 no3 pp 377ndash393 1998
[2] F E G Cox ldquoConcomitant infections parasites and immuneresponsesrdquo Parasitology vol 122 supplement 1 pp S23ndashS382001
[3] M Nacher P Singhasivanon S Yimsamran et al ldquoIntestinalhelminth infections are associated with increased incidenceof Plasmodium falciparum malaria in Thailandrdquo Journal ofParasitology vol 88 no 1 pp 55ndash58 2002
[4] J-Y Le Hesran J Akiana E H M Ndiaye M Dia P Senghorand L Konate ldquoSevere malaria attack is associated with highprevalence of Ascaris lumbricoides infection among childrenin rural Senegalrdquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 98 no 7 pp 397ndash399 2004
[5] M Nacher F Gay P Singhasivanon et al ldquoAscaris lumbricoidesinfection is associated with protection from cerebral malariardquoParasite Immunology vol 22 no 3 pp 107ndash113 2000
[6] V Briand L Watier J-Y Le Hesran A Garcia and M CotldquoCoinfection with Plasmodium falciparum and Schistosomahaematobium protective effect of schistosomiasis on malariain Senegalese childrenrdquo American Journal of Tropical Medicineand Hygiene vol 72 no 6 pp 702ndash707 2005
[7] N Oslash Christensen P Furu J Kurtzhals and A OdaiboldquoHeterologous synergistic interactions in concurrent experi-mental infection in the mouse with Schistosoma mansoniEchinostoma revolution Plasmodium yoelii Babesia microtiand Trypanosoma bruceirdquo Parasitology Research vol 74 no 6pp 544ndash551 1988
[8] G Raso A Luginbuhl C A Adjoua et al ldquoMultiple parasiteinfections and their relationship to self-reported morbidity ina community of rural Cote drsquoIvoirerdquo International Journal ofEpidemiology vol 33 no 5 pp 1092ndash1102 2004
[9] S Brooker W Akhwale R Pullan et al ldquoEpidemiology ofPlasmodium-helminth co-infection in Africa populations atrisk potential impact on anemia and prospects for combiningcontrolrdquo American Journal of Tropical Medicine and Hygienevol 77 no 6 pp 88ndash98 2007
[10] C E Shulman and E K Dorman ldquoReducing childhood mor-tality in poor countries importance and prevention of malariain pregnancyrdquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 97 no 1 pp 30ndash35 2003
[11] WorldHealthOrganisation andAfrica Regional OfficeMalariaPrevention and Control during Pregnancy in the African RegionWHOAFRO Brazzaville Congo 2004
[12] D Engels L Chitsulo A Montresor and L Savioli ldquoTheglobal epidemiological situation of schistosomiasis and newapproaches to control and researchrdquo Acta Tropica vol 82 no2 pp 139ndash146 2002
[13] P J Hotez and A Kamath ldquoNeglected tropical diseases in sub-Saharan Africa review of their prevalence distribution and
[14] M J Van Der Werf S J De Vlas S Brooker et al ldquoQuantifica-tion of clinical morbidity associated with schistosome infectionin sub-Saharan Africardquo Acta Tropica vol 86 no 2-3 pp 125ndash139 2003
[15] M N Nour ldquoSchistosomias health effect on womenrdquo Reviewsin Obstetrics amp Gynecology vol 3 no 1 pp 28ndash32 2010
[16] J F Friedman P Mital H K Kanzaria G R Olds and J DKurtis ldquoSchistosomiasis and pregnancyrdquo Trends in Parasitologyvol 23 no 4 pp 159ndash164 2007
[17] httpwwwwhointschistosomiasisstrategyen[18] H N Ntonifor and J A Ajayi ldquoWater contact and Schistosoma
haematobium infection A case study of some communitiesin Toro Local Government council Area (TLGCA) of BauchiStaterdquoNigeria Journal of Natural and Applied Sciences vol 1 no1 pp 54ndash59 2005
[19] P Saotoing T Vroumsia A M Njan F N Tchuenguem andJ Messi ldquoEpidemiological survey of schistosomiasis due toSchistosoma haematobium in some primary schools in thetown of Maroua far north region Cameroonrdquo InternationalJournal of Tropical Medicine vol 6 no 2 pp 19ndash24 2011
[20] L A Tchuem Tchuente R I K Ngassam L Sumo et al ldquoMap-ping of schistosomiasis and soil- transmitted helminthiasis inthe regions of centre east and west cameroonrdquo PLoS NeglectedTropical Diseases vol 6 no 3 p e1553 2012
[21] L A Tchuem Tchuente N C Dongmo P Ngassam et alldquoMapping of schistosomiasis and soil- transmitted helminthi-asis in the regions of Littoral North-West South and South-West Cameroon and recommendations for treatmentrdquo BMCInfectious Disease vol 13 article 602 2013
[22] K J N Ndamukong M A Ayuk J S Dinga T N Akenji VA Ndiforchu and V P K Titanji ldquoPrevalence and intensity ofurinary schistosomiasis in primary school children of the KottoBarombi health area Cameroonrdquo East African Medical Journalvol 78 no 6 pp 287ndash289 2001
[23] H N Ntonifor G N Mbunkur and N W Ndaleh ldquoEpidemi-ological survey of urinary schistosomiasis in some primaryschools in a new focus behind Mount Cameroon (Munyenge)South West Region Cameroonrdquo East African Medical Journalvol 89 no 3 pp 82ndash88 2012
[24] J F Friedman H K Kanzaria and S T McGarvey ldquoHumanschistosomiasis and anemia the relationship and potentialmechanismsrdquo Trends in Parasitology vol 21 no 8 pp 386ndash3922005
[25] A Ajanga N J S Lwambo L Blair U Nyandindi A Fenwickand S Brooker ldquoSchistosoma mansoni in pregnancy andassociations with anaemia in northwest Tanzaniardquo Transactionsof the Royal Society of Tropical Medicine and Hygiene vol 100no 1 pp 59ndash63 2006
[26] G Helling-Giese E F Kjetland S G Gundersen et al ldquoSchis-tosomiasis in women manifestations in the upper reproductivetractrdquo Acta Tropica vol 62 no 4 pp 225ndash238 1996
[27] R W Steketee B L Nahlen M E Parise and C MenendezldquoTheburden ofmalaria in pregnancy inmalaria-endemic areasrdquoAmerican Journal of Tropical Medicine and Hygiene vol 64 no1-2 pp 28ndash35 2001
[28] V V Laxman B Adamson and T Mahmood ldquoRecurrentectopic pregnancy due to Schistosoma hematobiumrdquo Journal ofObstetrics and Gynaecology vol 28 no 4 pp 461ndash462 2008
[29] S Bahrami H Alatassi S P Slone and D M OrsquoConnorldquoTubal gestation and schistosomiasis a case reportrdquo Journal ofReproductiveMedicine for theObstetrician andGynecologist vol51 no 7 pp 595ndash598 2006
[30] P S Mbabazi O Andan D W Fitzgerald L Chitsulo DEngels and J A Downs ldquoExamining the relationship betweenurogenital schistosomiasis and HIV infectionrdquo PLoS NeglectedTropical Diseases vol 5 no 12 Article ID e1396 2011
[31] R Tweyongyere P A Mawa N O Emojong et al ldquoEffectof praziquantel treatment of Schistosomamansoni during preg-nancy on intensity of infection and antibody responses to schis-tosome antigens results of a randomised placebo-controlledtrialrdquo BMC Infectious Diseases vol 9 article 32 2009
[32] H N Ntonifor A E Green M O S Bopda et al ldquoEpi-demiology of urinary schistosomiasis and soil transmittedhelminthiasis in a recently established focus behind MountCameroonrdquo International Journal of Current Microbiology andApplied Sciences vol 4 no 3 pp 1056ndash1066 2015
[33] S Wanji A J Kengne-Ouafo E E Joan Eyong et al ldquoGeneticdiversity of Plasmodium falciparummerozoite surface protein-1 block 2 in sites of contrasting altitudes and malaria endemic-ities in the Mount Cameroon Regionrdquo American Journal ofTropical Medicine and Hygiene vol 86 no 5 pp 764ndash774 2012
[34] J K Anchang-Kimbi E A Achidi B Nkegoum E Sverremark-Ekstrom and M Troye-Blomberg ldquoDiagnostic comparisonof malaria infection in peripheral blood placental blood andplacental biopsies in Cameroonian parturient womenrdquoMalariaJournal vol 8 no 1 article 126 2009
[35] F J Bryan The Design and Analysis of Research Studies Uni-versity ofOtago Dunedin NewZealand CambridgeUniversityPress Cambridge UK 1992
[36] World Health Organisation Haemoglobin Concentrations forthe Diagnosis of Anaemia and Assessment of Severity Vitaminand mineral Nutrition Information System WHO GenevaSwitzerland 2011
[37] M CheesbroughDistrict Laboratory Practice in Tropical Coun-tries Cambridge University Press Cambridge UK 2006
[39] N O Christensen G Gotsche and F Frandsen ParasitologicalTechniques for Use in Routine Laboratory Maintainance of Schis-tosomes and Used in Studies on the Epidemiology of Human andBovine Schistosomiasis Danish Bilhaziasis Laboratory Manual1984
[40] World Health OrganizationmdashTropical Disease Research TDRstrategic direction Schistosomiasis WHO-TDR 2002
[41] World Health OrganizationGuidelines for the Evaluation of SoilTransmitted Helminthiasis and Schistosomiasis at CommunityLevel A Guide for Managers of Control Programme WHOGeneva Switzerland 1993
[42] J E Eyo G C Onyishi and F C Okafor ldquoUrinary schisto-somiasis among pregnant women in some endemic tropicalsemi-urban communities of Anambra State Nigeriardquo TropicalBiomedicine vol 29 no 4 pp 575ndash579 2012
[43] O T Salawu and A B Odaibo ldquoSchistosomiasis among preg-nant women in rural communities in Nigeriardquo InternationalJournal of Gynecology andObstetrics vol 122 no 1 pp 1ndash4 2013
[44] K R Tan B L Katalenich K E Mace et al ldquoEfficacyof sulphadoxine-pyrimethamine for intermittent preventivetreatment of malaria in pregnancy Mansa Zambiardquo MalariaJournal vol 13 no 1 article 227 2014
12 Journal of Parasitology Research
[45] J Bethony J T Williams H Kloos et al ldquoExposure toSchistosoma mansoni infection in a rural area in Brazil IIhousehold risk factorsrdquo Tropical Medicine and InternationalHealth vol 6 no 2 pp 136ndash145 2001
[46] J C Sousa-Figueiredo D Gamboa J M Pedro et al ldquoEpi-demiology of malaria schistosomiasis geohelminths anemiaand malnutrition in the context of a demographic surveillancesystem in northern Angolardquo PLoS ONE vol 7 no 4 Article IDe33189 2012
[47] F Anto V Asoala M Adjuik et al ldquoWater contact activitiesand prevalence of schistosomiasis infection among school-agechildren in communities along an irrigation scheme in RuralNorthern Ghanardquo Journal of Bacteriology amp Parasitology vol 4article 177 2013
[48] L-A Tchuem Tchuente J M Behnke F S Gilbert V RSouthgate and J Vercruysse ldquoPolyparasitism with Schistosomahaematobium and soil-transmitted helminth infections amongschool children in Loum Cameroonrdquo Tropical Medicine andInternational Health vol 8 no 11 pp 975ndash986 2003
[49] J-F Etard M Audibert and A Dabo ldquoAge-acquired resistanceand predisposition to reinfection with Schistosoma haemato-bium after treatment with praziquantel in Malirdquo The AmericanJournal of TropicalMedicine andHygiene vol 52 no 6 pp 549ndash558 1995
[50] A Gazzinelli G Velasquez-Melendez S B Crawford P TLoVerde R Correa-Oliveira and H Kloos ldquoSocioeconomicdeterminants of schistosomiasis in a poor rural area in BrazilrdquoActa Tropica vol 99 no 2-3 pp 260ndash271 2006
[51] A P Kapito-Tembo V Mwapasa S R Meshnick et al ldquoPreva-lence distribution and risk factors for Schistosoma hematobiuminfection among school children in Blantyre Malawirdquo PLoSNeglected Tropical Diseases vol 3 no 1 article e361 2009
[52] N J Yatich J Yi T Agbenyega et al ldquoMalaria and intestinalhelminth co-infection among pregnant women in Ghanaprevalence and risk factorsrdquo The American Journal of TropicalMedicine and Hygiene vol 80 no 6 pp 896ndash901 2009
[53] M Nacher ldquoInteractions between worms and malaria goodworms or bad wormsrdquoMalaria Journal vol 10 article no 2592011
[54] A A Adegnika and P G Kremsner ldquoEpidemiology of malariaand helminth interaction a review from 2001 to 2011rdquo CurrentOpinion in HIV and AIDS vol 7 no 3 pp 221ndash224 2012
[55] S Getie Y Wondimeneh G Getnet et al ldquoPrevalence andclinical correlates of Schistosoma mansoni co-infection amongmalaria infected patients Northwest Ethiopiardquo BMC ResearchNotes vol 8 no 1 article no 480 2015
[56] E Okafor and A Elenwo ldquoHaemoglobin status of children withmixed infection ofmalaria and urinary schistosomiasis inOdauCommunity Rivers state Nigeriardquo Journal of Agriculture andSocial Research vol 7 no 1 pp 56ndash62 2008
[57] M A McDevitt J Xie V Gordeuk and R Bucala ldquoThe anemiaof malaria infection role of inflammatory cytokinesrdquo CurrentHematology Reports vol 3 no 2 pp 97ndash106 2004
[58] J G Shaw and J F Friedman ldquoIron deficiency anemia focus oninfectious diseases in lesser developed countriesrdquo Anemia vol2011 Article ID 260380 10 pages 2011
[59] H K Green J C Sousa-Figueiredo M-G Basanez et alldquoAnaemia in Ugandan preschool-aged children the relativecontribution of intestinal parasites and malariardquo Parasitologyvol 138 no 12 pp 1534ndash1545 2011
[60] E Ivan N J Crowther E Mutimura L O Osuwat S Janssenand M P Grobusch ldquoHelminthic infections rates and malaria
in HIV-infected pregnant women on anti-retroviral therapy inRwandardquo PLoS Neglected Tropical Diseases vol 7 no 8 ArticleID e2380 2013
factors associated with Hb levels were obtained using mul-tilinear regression analysis 119875 values lt 005 were consideredsignificant
33 Ethical Considerations The study protocol and designincluding the consent procedures were approved by the Insti-tutional Ethics ReviewBoard of the Faculty ofHealth ScienceUniversity of Buea and the Buea Regional Delegation ofPublic Health Prior to conducting the study the aim ofthe study and procedures to be used to collect data wereexplained to the pregnant women at the ANC clinic Written(from those who can read and write) or verbal (from thosewho cannot read and write) informed consent from all studyparticipants was obtained Each pregnant womanwho agreedto participate in the study was enrolled and given urinesample container to collect urine Participationwas voluntaryand study participants were assured of confidentiality andanonymity of data
4 Results
41 Characteristics of the Study Population In this cross-sectional study a total of 250 pregnant women reportingfor antenatal care was enrolled The mean age of the studyparticipants was 25 plusmn 521 years (range 14ndash40 years) Themajority (752) of the women were married All the studyparticipants had at least a primary education and about 50had obtained some form of secondary education Although ahigher proportion of the women had been enrolled for firstANC in the second trimester more than 40 had late clinicregistration About two-thirds of women reported taking atleast one dose of IPTp-SP and 46 reported having sleptunder a bed net the previous night The stream was the mainsource of water (99 stream usage) for domestic use andbathing The characteristics of the study sample are shown inTable 1
42 Prevalence and Intensity of Infection
421 S haematobium Infection Of the 250 volunteer preg-nant women enrolled 117 (468 95 CI 41ndash53) were pos-itive for S haematobium infection among whom 53 (453)had heavy (ge50 eggs10mL of urine) infection while 547(64) had light (lt50 eggs10mL of urine) infectionThe preva-lence of microhaematuria was 96 (24250) Using micro-scopic urine examination as gold standard the specificity andsensitivity ofmicrohaematuria in the diagnosis of S haemato-bium infection were 100 (95CI 972ndash100) and 205 (95CI 142ndash287) respectively Microhaematuria was stronglyrelated to egg density categories where microhaematuria wascommon (1205942 = 823 119875 = 0004) among women with heavyegg load (727) than in those with light infection (273)
422 P falciparum Infection The overall prevalence of Pfalciparum parasitaemia among the study participants was392 (98) (95 CI 334ndash454) Of the 98 pregnant womeninfected with P falciparum the proportions of low (lt500parasites120583L of blood) moderate (501ndash5000) and high
Table 1 Characteristics of the study participants
Characteristics Number examined (N) ()Age group (years)le20 56 22421ndash25 79 31626ndash30 71 284gt30 44 176
Activities in the streamDomestic contact and bathing 126 504Domestic contact only 124 496
Frequency to streamsday1 to 2 times 122 4883 to 4 times 57 2285+ times 71 284
IPTp-SP uptakeYes 169 676No 81 324
ITN useYes 115 460No 135 540
(gt5000) parasitaemia were 439 (43) 520 (61) and 41(4) respectively About 15 (38) (95 CI 113ndash202) ofthe pregnant women carried concurrent infections with Shaematobium and P falciparum Seventy-nine (316) andsixty (24) women had single infection with S haematobiumand P falciparum respectively
423 Factors Associated with Prevalence and Intensity ofS haematobium Infection S haematobium infection wasassociated with age gravidity status water contact frequency
Journal of Parasitology Research 5
Table 2 Risk factors associated with S haematobium infection among pregnant women in Munyenge
1205942 P value 417 00411205942 Pearson Chi-square test OR odd ratioOR adjusted using multivariate regression analysis
type of activity carried out in the stream and P falciparumparasitaemia in bivariate analysis (Table 2) The prevalenceof infection did not differ significantly with marital statuseducational level and occupational status In multivariate
analysis (controlling for age and gravidity status as con-founders) younger age groups le20 (aOR = 152 95 CI 17ndash1383) and 21ndash25 years (aOR = 73 95 CI 12ndash443) andbathing and domestic contact with stream (aOR = 335 95
6 Journal of Parasitology Research
CI 97ndash1159)were risk factors associatedwith S haematobiuminfection On the other hand less water contact frequency(1 to 2 times per day) (aOR = 28119864 minus 10 95 CI 94119864 minus11ndash85119864minus10) was associated with decreased risk of infectionSurprisingly primigravidity (OR = 02 95 CI 003ndash09)and secundigravidity (OR = 01 95 CI 002ndash04) wereless likely at risk Intensity of infection was associated withmalaria parasitaemia where light egg density infection wasless common (aOR = 04 95 CI 02ndash07 119875 = 0004)in malaria positive women (219 1464) than in malarianegative women (781 5064)
424 Factors Associated with Prevalence of P falciparumInfection The prevalence of P falciparum infection wasassociated (1205942 = 1782 119875 lt 001) with IPTp-SP uptake wheremalaria parasite infection was greater in women who had nottaken IPTp-SP (580) than in those who had at least one SPdose (302) The occurrence of P falciparum infection didnot differ significantly with maternal age gravidity status orITN usage
425 Factors Associated with Prevalence of Coinfection with Shaematobium and P falciparum Coinfection was associatedwith the type of activity carried out in the stream and watercontact frequency as well as IPTp-SP uptake Bathing anddomestic contact with stream (aOR = 133 95 CI 22ndash795) increased risk of coinfection among pregnant womenmeanwhile less water contact frequency (1 to 2 times per day(aOR = 01 95 CI 001ndash04) and 3 to 4 times per day (aOR =03 95 CI 01ndash09)) decreased risk of coinfection Womenwho had at least one SP dose were less likely (aOR= 006 95CI 002ndash02) to be coinfected (Table 3)
43 Haemoglobin Levels and Anaemia Themean (plusmnSD) hae-moglobin level of the pregnant women enrolled in the studywas 90 plusmn 16 gdL (range 61ndash137 gdL) Coinfection signif-icantly reduced Hb levels of pregnant women in the studyarea where levels in coinfected individuals were significantlylower (119875 lt 0001) when compared with levels seen withsingle infections (S haematobium and P falciparum) and noinfection (Table 4) In addition Hb levels were significantlylower among women coinfected with P falciparum and heavyS haematobium infections than in individuals coinfectedwith P falciparum and light S haematobium infection andthose with no infection (Table 5) Although age maritalstatus educational level occupational status infection statusand IPTp-SP uptake were identified as factors associatedwith Hb levels IPTp-SP was seen as the only independentpredictor of Hb levels taking into consideration all possibleconfounding variables (Table 4)
Anaemia prevalence was 888 (222250) with anaemiaseverity as follows mild (132 119899 = 33) moderate (628119899 = 157) and severe (128 119899 = 32) All cases diagnosedwithcoinfection were anaemic (Table 6) Coinfection accountedfor 938 (3032) of all severe anaemia cases with majority719 (2332) of the severe anaemic cases coinfected withP falciparum and heavy density S haematobium infections(Table 5) Uptake of IPTp-SP (438 1432) was associated
(1205942 = 1132 119875 = 001) with reduced percentage of severeanaemia compared with that observed among women withno SP (563 1832) Risk factors found to be associated withincreased odds of anaemia were P falciparum infection (OR=40 95 CI 10ndash145) and occupation (business) (OR = 20195 CI 40ndash101) (Table 6)
5 Discussion
To our knowledge this is the first study carried out on uro-genital schistosomiasis among pregnant women in Camer-oon This study determined the prevalence of S haemato-bium P falciparum and coinfection factors associated withthese infections and assessed their relative effect on anaemiaprevalence and severity among pregnant women in Mun-yenge S haematobium and P falciparum infections are com-mon among pregnant women living in Munyenge and theircoinfection exacerbates anaemia
The prevalence of S haematobium infection among preg-nant women in our study was 468 The high prevalencereflects high exposure to infection among pregnant womenliving in Munyenge due to absolute dependence on naturalwater sources for domestic activities and bathing Comparedto the level of infection in the present study lower prevalenceof urogenital schistosomiasis among pregnant women hasbeen reported inNigeria by Eyo et al [42] (238) and Salawuand Odaibo [43] (208) Differences in the method usedfor the detection of S haematobium infection may partlyexplain the observed differences in rates Although thesestudies attributed the lower prevalence levels of urinary schis-tosomiasis among pregnant women to a taboo restrictingpregnant women from visiting natural water bodies [42]compared with urine filtration method used in our study thelower sensitive centrifugation method use in the diagnosisof S haematobium infection in the Nigerian studies mayhave underestimated true infection levelsMalaria is commonamong pregnant women in the study area with a prevalenceof 392 The only factor seen to be associated with malariaparasite infection in this study site was IPTp uptake Theeffectiveness of IPTp-SP in the prevention of malaria inpregnancy is well established [34 44]
For transmission of schistosomiasis to take place theschistosomes parasite requires an avenue where it is indirect contact with the human host [9] Pregnant womenliving in Munyenge get in contact with infection duringactivities such as laundry plate washing and water fetchingfor domestic use In addition to domestic activities bathingin streams poses a greater risk of infection among pregnantwomen in this area Analyses from other studies have shownthat regularly bathing in water sources contaminated withthe developmental stages of the schistosomes parasite wasassociated with prevalence and intensity of schistosomiasis[45ndash47]Moreover increased risk of infection associatedwiththe number and duration of water contact with infestedwaters per day has also been reported [47] Women whoreported surface-water contact at least 3 to 5 times perday were at greater risk of infection due to longer periodof contact with contaminated water Health education toinstruct pregnant women to make less surface-water contact
Journal of Parasitology Research 7
Table 3 Risk factors associated with coinfection with S haematobium and P falciparum among pregnant women in Munyenge
1205942 119875 value 1329 lt00011205942 Pearson Chi-square test OR odd ratioAdjusted OR using multivariate regression analysis
frequency and the implication of voiding their bladder inwater bodies is paramount These behavioural changes willsignificantly reduce the risk of S haematobium infectionamong pregnant women and contamination of water sourcesin this setting Ultimately provision of portable water andimproved sanitation system will play a major role in decreas-ing disease transmission and incidence
Age as observed in most schistosomiasis surveys was amajor determinant of schistosomes infection among preg-nant women in our study area The highest prevalence val-ues of urogenital schistosomiasis were recorded in youngerwomen (le25 years) Individuals within le20 age group werefound to be at a greater risk of S haematobium infection withprevalence of 554 This is in agreement with trends estab-lished in schistosomiasis surveys carried out in Cameroon
[32 48] and other parts of Africa [42 43] Alternativelythe decrease risk of infection observed in older age groups(gt25 years) conformed to earlier reports [32 42] Studieshave reported that age-acquired immunity to reinfection andchanges in water contact patterns contribute to the decliningtrend in prevalence with increasing age [49] Older womenare less likely to be engaged in water contact behaviourscompared to younger women Age dependent immunity toS haematobium has been shown to affect mean egg outputof infected persons [49] Socioeconomic status of the womenwas not an independent factor associated with S haema-tobium prevalence in this high-risk community Similarlyreports from other rural settings endemic for schistosomi-asis failed to identify any socioeconomic variables that arestrongly associated with schistosomiasis prevalence [50 51]
8 Journal of Parasitology Research
Table 4 Factors associated with mean (plusmnSD) haemoglobin levels among pregnant women in Munyenge Health Area
Factors Category Mean (plusmnSD) Hblevels Test-value Unadjusted
lowastAnalysis of variance test (ANOVA)$Studentrsquos 119905-testampAdjusted 119875 values using multilinear regression analysisNA not applicable variables with 119875 gt 02 in bivariate analysis were not included in regression analysis
Table 5 Association between S haematobium intensity P falciparum infection and mean (plusmnSD) haemoglobin levels and anaemia severity
lowastSignificance level 119865 = 1240 119875 lt 0001lowastAnalysis of variance test (ANOVA)ampPearson Chi-Square test
The absence of association between socioeconomic variablesand infection prevalencemay be attributed to general povertyand uniformity in high exposure risk in the population [50]
The overall prevalence of coinfection with S haema-tobium and P falciparum infection was 152 suggestingcoendemicity of both infections in the study area SimilarlyYatich et al [52] reported a helminth andmalaria coinfectionprevalence of 166 among pregnant women in Ghana Theimpact of helminth infections on malaria parasitaemia and
disease during coinfection is an established phenomenonalthough much is still unknown and contradictions persist[53 54]We observed that light S haematobium infectionwasless common (aOR= 04) among pregnant women coinfectedwith P falciparum suggesting a negative interaction betweenboth parasites [4] In accordance with findings of Getie etal [55] schistosomiasis coinfection could affect Plasmodiumparasitemia and vice versa depending on the intensity of theova in coinfected persons Nonetheless a further study is
Journal of Parasitology Research 9
Table 6 Risk factors associated with anaemia among pregnant women in Munyenge Health Area
Factors Category Anaemia prevalence Adjusted OR (95 CI) 119875 value
Adjusted OR using multivariate regression analysisNA not applicable variables with 119875 gt 02 in bivariate analysis were not included in multivariate analysis
needed to explore the underlying mechanisms of interactionbetween malaria parasitaemia and S haematobium
Schistosomiasis causes long term morbidity such asanaemia Our study showed that the magnitude of S haema-tobium egg counts is significantly related to haemoglobinconcentration confirming that urogenital schistosomiasiscontributes to anaemia [24 25] In this study anaemiawas more pronounced in women with heavy infectionintensity than in those with light infection Coinfection ofhelminth infections and P falciparum increases anaemiaseverity [8 9] Coinfection among pregnant women lowersHb concentration compared with single infection This is inagreement with findings of Okafor and Elenwo [56] Moreso coinfected women with heavy intensity S haematobiuminfection had the lowest mean Hb levels (66 gdL) andthis subpopulation of women contributed to about 72of all severe anaemic cases The combined presence and
interaction of S haematobium and P falciparum infectionsis partly responsible for the low haemoglobin concentrationin women with concurrent infectionMalaria causes anaemiaby destruction and removal of parasitized red blood cellsand shortening of the life span of nonparasitized red cellsas well as decreasing the rate of erythrocyte production inbone marrow [57]Themechanism by which schistosomiasiscauses anaemia is not fully understood but it is suggested thathelminth infections could contribute to increase in the preva-lence of inflammatory syndromes impairing erythropoiesisand interfering with mobilization of reticuloendothelial ironstorages and shortening erythrocyte survival [58] Similar toprevious reports of a study in Uganda [59] malaria parasiteinfection was an independent factor associated with increaseanaemia risk
The risk of coinfection was associated with streamusage (bathing and domestic contact with stream) while
10 Journal of Parasitology Research
less water contact and SP usage decreased risk of infectionThis finding suggests that intervention strategies focusingon combating malaria and schistosomiasis respectively byincreasing the uptake of IPTp-SPdoses and less water contactamong pregnant women living in Munyenge represents themost appropriate prevention of coinfection with consequentincrease in Hb levels
This study had one limitation We did not investigate theprevalence of HIV infection among the study participants Ithas been shown that coinfections with helminths andmalariacause considerable morbidity in the host particularly in thepresence of HIV infection [60]
To conclude the study has indicated that S haematobiumand P falciparum infections are common among pregnantwomen living in Munyenge and their coinfection is influ-enced by high frequencies of these parasites in the same pop-ulationThe study also revealed that younger age and bathingand domestic contact with stream are independently associ-ated with prevalence of S haematobium infection while noIPTp-SP was associated with P falciparum infection Streamusage increased risk of coinfection while less water contactand SP usage decreased its risk The fact that light S haema-tobium infection was less common in P falciparum infectedwomen suggests that Plasmodium falciparum parasitaemiamay be associatedwith intensity of urogenital schistosomiasisin coinfected individuals Anaemia is a severe public healthproblem in pregnancy in Munyenge and coinfection withS haematobium and P falciparum exacerbates anaemiaLess water contact frequency and increase uptake of IPTp-SPdoses will significantly reduce risk of coinfection andconsequently anaemia severity in pregnancy in this setting
Abbreviations
IPTp-SP Intermittent preventive treatment in pregnancy(IPTp) with sulfadoxine-pyrimethamine (SP)
ITN Insecticide treated bed netsHIV Human immunodeficiency virusANC Antenatal care
Competing Interests
The authors declare that they do not have any competinginterests
Authorsrsquo Contributions
Judith K Anchang-Kimbi conceived and designed the studyanalyzed the data and wrote the manuscript Dillys MansohElad participated in the design of the study performedthe experiments and made inputs in manuscript write-upGemain Taiwe Sotoing and Eric Akum Achidi supervisedreviewed and provided inputs to the manuscript All authorsread and approved the final manuscript
Acknowledgments
The authors are grateful to all the pregnant women whogave their consent to participate in the study Special thanks
are due to the chief medical officer nurses and laboratorytechnician of the Munyenge Health Centre for their cooper-ation and contribution This study received financial supportfrom the Ministry of Higher Education University ResearchModernisation grant given to authors Judith K Anchang-Kimbi and Eric Akum Achidi
References
[1] T N Petney and R H Andrews ldquoMultiparasite communitiesin animals and humans frequency structure and pathogenicsignificancerdquo International Journal for Parasitology vol 28 no3 pp 377ndash393 1998
[2] F E G Cox ldquoConcomitant infections parasites and immuneresponsesrdquo Parasitology vol 122 supplement 1 pp S23ndashS382001
[3] M Nacher P Singhasivanon S Yimsamran et al ldquoIntestinalhelminth infections are associated with increased incidenceof Plasmodium falciparum malaria in Thailandrdquo Journal ofParasitology vol 88 no 1 pp 55ndash58 2002
[4] J-Y Le Hesran J Akiana E H M Ndiaye M Dia P Senghorand L Konate ldquoSevere malaria attack is associated with highprevalence of Ascaris lumbricoides infection among childrenin rural Senegalrdquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 98 no 7 pp 397ndash399 2004
[5] M Nacher F Gay P Singhasivanon et al ldquoAscaris lumbricoidesinfection is associated with protection from cerebral malariardquoParasite Immunology vol 22 no 3 pp 107ndash113 2000
[6] V Briand L Watier J-Y Le Hesran A Garcia and M CotldquoCoinfection with Plasmodium falciparum and Schistosomahaematobium protective effect of schistosomiasis on malariain Senegalese childrenrdquo American Journal of Tropical Medicineand Hygiene vol 72 no 6 pp 702ndash707 2005
[7] N Oslash Christensen P Furu J Kurtzhals and A OdaiboldquoHeterologous synergistic interactions in concurrent experi-mental infection in the mouse with Schistosoma mansoniEchinostoma revolution Plasmodium yoelii Babesia microtiand Trypanosoma bruceirdquo Parasitology Research vol 74 no 6pp 544ndash551 1988
[8] G Raso A Luginbuhl C A Adjoua et al ldquoMultiple parasiteinfections and their relationship to self-reported morbidity ina community of rural Cote drsquoIvoirerdquo International Journal ofEpidemiology vol 33 no 5 pp 1092ndash1102 2004
[9] S Brooker W Akhwale R Pullan et al ldquoEpidemiology ofPlasmodium-helminth co-infection in Africa populations atrisk potential impact on anemia and prospects for combiningcontrolrdquo American Journal of Tropical Medicine and Hygienevol 77 no 6 pp 88ndash98 2007
[10] C E Shulman and E K Dorman ldquoReducing childhood mor-tality in poor countries importance and prevention of malariain pregnancyrdquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 97 no 1 pp 30ndash35 2003
[11] WorldHealthOrganisation andAfrica Regional OfficeMalariaPrevention and Control during Pregnancy in the African RegionWHOAFRO Brazzaville Congo 2004
[12] D Engels L Chitsulo A Montresor and L Savioli ldquoTheglobal epidemiological situation of schistosomiasis and newapproaches to control and researchrdquo Acta Tropica vol 82 no2 pp 139ndash146 2002
[13] P J Hotez and A Kamath ldquoNeglected tropical diseases in sub-Saharan Africa review of their prevalence distribution and
[14] M J Van Der Werf S J De Vlas S Brooker et al ldquoQuantifica-tion of clinical morbidity associated with schistosome infectionin sub-Saharan Africardquo Acta Tropica vol 86 no 2-3 pp 125ndash139 2003
[15] M N Nour ldquoSchistosomias health effect on womenrdquo Reviewsin Obstetrics amp Gynecology vol 3 no 1 pp 28ndash32 2010
[16] J F Friedman P Mital H K Kanzaria G R Olds and J DKurtis ldquoSchistosomiasis and pregnancyrdquo Trends in Parasitologyvol 23 no 4 pp 159ndash164 2007
[17] httpwwwwhointschistosomiasisstrategyen[18] H N Ntonifor and J A Ajayi ldquoWater contact and Schistosoma
haematobium infection A case study of some communitiesin Toro Local Government council Area (TLGCA) of BauchiStaterdquoNigeria Journal of Natural and Applied Sciences vol 1 no1 pp 54ndash59 2005
[19] P Saotoing T Vroumsia A M Njan F N Tchuenguem andJ Messi ldquoEpidemiological survey of schistosomiasis due toSchistosoma haematobium in some primary schools in thetown of Maroua far north region Cameroonrdquo InternationalJournal of Tropical Medicine vol 6 no 2 pp 19ndash24 2011
[20] L A Tchuem Tchuente R I K Ngassam L Sumo et al ldquoMap-ping of schistosomiasis and soil- transmitted helminthiasis inthe regions of centre east and west cameroonrdquo PLoS NeglectedTropical Diseases vol 6 no 3 p e1553 2012
[21] L A Tchuem Tchuente N C Dongmo P Ngassam et alldquoMapping of schistosomiasis and soil- transmitted helminthi-asis in the regions of Littoral North-West South and South-West Cameroon and recommendations for treatmentrdquo BMCInfectious Disease vol 13 article 602 2013
[22] K J N Ndamukong M A Ayuk J S Dinga T N Akenji VA Ndiforchu and V P K Titanji ldquoPrevalence and intensity ofurinary schistosomiasis in primary school children of the KottoBarombi health area Cameroonrdquo East African Medical Journalvol 78 no 6 pp 287ndash289 2001
[23] H N Ntonifor G N Mbunkur and N W Ndaleh ldquoEpidemi-ological survey of urinary schistosomiasis in some primaryschools in a new focus behind Mount Cameroon (Munyenge)South West Region Cameroonrdquo East African Medical Journalvol 89 no 3 pp 82ndash88 2012
[24] J F Friedman H K Kanzaria and S T McGarvey ldquoHumanschistosomiasis and anemia the relationship and potentialmechanismsrdquo Trends in Parasitology vol 21 no 8 pp 386ndash3922005
[25] A Ajanga N J S Lwambo L Blair U Nyandindi A Fenwickand S Brooker ldquoSchistosoma mansoni in pregnancy andassociations with anaemia in northwest Tanzaniardquo Transactionsof the Royal Society of Tropical Medicine and Hygiene vol 100no 1 pp 59ndash63 2006
[26] G Helling-Giese E F Kjetland S G Gundersen et al ldquoSchis-tosomiasis in women manifestations in the upper reproductivetractrdquo Acta Tropica vol 62 no 4 pp 225ndash238 1996
[27] R W Steketee B L Nahlen M E Parise and C MenendezldquoTheburden ofmalaria in pregnancy inmalaria-endemic areasrdquoAmerican Journal of Tropical Medicine and Hygiene vol 64 no1-2 pp 28ndash35 2001
[28] V V Laxman B Adamson and T Mahmood ldquoRecurrentectopic pregnancy due to Schistosoma hematobiumrdquo Journal ofObstetrics and Gynaecology vol 28 no 4 pp 461ndash462 2008
[29] S Bahrami H Alatassi S P Slone and D M OrsquoConnorldquoTubal gestation and schistosomiasis a case reportrdquo Journal ofReproductiveMedicine for theObstetrician andGynecologist vol51 no 7 pp 595ndash598 2006
[30] P S Mbabazi O Andan D W Fitzgerald L Chitsulo DEngels and J A Downs ldquoExamining the relationship betweenurogenital schistosomiasis and HIV infectionrdquo PLoS NeglectedTropical Diseases vol 5 no 12 Article ID e1396 2011
[31] R Tweyongyere P A Mawa N O Emojong et al ldquoEffectof praziquantel treatment of Schistosomamansoni during preg-nancy on intensity of infection and antibody responses to schis-tosome antigens results of a randomised placebo-controlledtrialrdquo BMC Infectious Diseases vol 9 article 32 2009
[32] H N Ntonifor A E Green M O S Bopda et al ldquoEpi-demiology of urinary schistosomiasis and soil transmittedhelminthiasis in a recently established focus behind MountCameroonrdquo International Journal of Current Microbiology andApplied Sciences vol 4 no 3 pp 1056ndash1066 2015
[33] S Wanji A J Kengne-Ouafo E E Joan Eyong et al ldquoGeneticdiversity of Plasmodium falciparummerozoite surface protein-1 block 2 in sites of contrasting altitudes and malaria endemic-ities in the Mount Cameroon Regionrdquo American Journal ofTropical Medicine and Hygiene vol 86 no 5 pp 764ndash774 2012
[34] J K Anchang-Kimbi E A Achidi B Nkegoum E Sverremark-Ekstrom and M Troye-Blomberg ldquoDiagnostic comparisonof malaria infection in peripheral blood placental blood andplacental biopsies in Cameroonian parturient womenrdquoMalariaJournal vol 8 no 1 article 126 2009
[35] F J Bryan The Design and Analysis of Research Studies Uni-versity ofOtago Dunedin NewZealand CambridgeUniversityPress Cambridge UK 1992
[36] World Health Organisation Haemoglobin Concentrations forthe Diagnosis of Anaemia and Assessment of Severity Vitaminand mineral Nutrition Information System WHO GenevaSwitzerland 2011
[37] M CheesbroughDistrict Laboratory Practice in Tropical Coun-tries Cambridge University Press Cambridge UK 2006
[39] N O Christensen G Gotsche and F Frandsen ParasitologicalTechniques for Use in Routine Laboratory Maintainance of Schis-tosomes and Used in Studies on the Epidemiology of Human andBovine Schistosomiasis Danish Bilhaziasis Laboratory Manual1984
[40] World Health OrganizationmdashTropical Disease Research TDRstrategic direction Schistosomiasis WHO-TDR 2002
[41] World Health OrganizationGuidelines for the Evaluation of SoilTransmitted Helminthiasis and Schistosomiasis at CommunityLevel A Guide for Managers of Control Programme WHOGeneva Switzerland 1993
[42] J E Eyo G C Onyishi and F C Okafor ldquoUrinary schisto-somiasis among pregnant women in some endemic tropicalsemi-urban communities of Anambra State Nigeriardquo TropicalBiomedicine vol 29 no 4 pp 575ndash579 2012
[43] O T Salawu and A B Odaibo ldquoSchistosomiasis among preg-nant women in rural communities in Nigeriardquo InternationalJournal of Gynecology andObstetrics vol 122 no 1 pp 1ndash4 2013
[44] K R Tan B L Katalenich K E Mace et al ldquoEfficacyof sulphadoxine-pyrimethamine for intermittent preventivetreatment of malaria in pregnancy Mansa Zambiardquo MalariaJournal vol 13 no 1 article 227 2014
12 Journal of Parasitology Research
[45] J Bethony J T Williams H Kloos et al ldquoExposure toSchistosoma mansoni infection in a rural area in Brazil IIhousehold risk factorsrdquo Tropical Medicine and InternationalHealth vol 6 no 2 pp 136ndash145 2001
[46] J C Sousa-Figueiredo D Gamboa J M Pedro et al ldquoEpi-demiology of malaria schistosomiasis geohelminths anemiaand malnutrition in the context of a demographic surveillancesystem in northern Angolardquo PLoS ONE vol 7 no 4 Article IDe33189 2012
[47] F Anto V Asoala M Adjuik et al ldquoWater contact activitiesand prevalence of schistosomiasis infection among school-agechildren in communities along an irrigation scheme in RuralNorthern Ghanardquo Journal of Bacteriology amp Parasitology vol 4article 177 2013
[48] L-A Tchuem Tchuente J M Behnke F S Gilbert V RSouthgate and J Vercruysse ldquoPolyparasitism with Schistosomahaematobium and soil-transmitted helminth infections amongschool children in Loum Cameroonrdquo Tropical Medicine andInternational Health vol 8 no 11 pp 975ndash986 2003
[49] J-F Etard M Audibert and A Dabo ldquoAge-acquired resistanceand predisposition to reinfection with Schistosoma haemato-bium after treatment with praziquantel in Malirdquo The AmericanJournal of TropicalMedicine andHygiene vol 52 no 6 pp 549ndash558 1995
[50] A Gazzinelli G Velasquez-Melendez S B Crawford P TLoVerde R Correa-Oliveira and H Kloos ldquoSocioeconomicdeterminants of schistosomiasis in a poor rural area in BrazilrdquoActa Tropica vol 99 no 2-3 pp 260ndash271 2006
[51] A P Kapito-Tembo V Mwapasa S R Meshnick et al ldquoPreva-lence distribution and risk factors for Schistosoma hematobiuminfection among school children in Blantyre Malawirdquo PLoSNeglected Tropical Diseases vol 3 no 1 article e361 2009
[52] N J Yatich J Yi T Agbenyega et al ldquoMalaria and intestinalhelminth co-infection among pregnant women in Ghanaprevalence and risk factorsrdquo The American Journal of TropicalMedicine and Hygiene vol 80 no 6 pp 896ndash901 2009
[53] M Nacher ldquoInteractions between worms and malaria goodworms or bad wormsrdquoMalaria Journal vol 10 article no 2592011
[54] A A Adegnika and P G Kremsner ldquoEpidemiology of malariaand helminth interaction a review from 2001 to 2011rdquo CurrentOpinion in HIV and AIDS vol 7 no 3 pp 221ndash224 2012
[55] S Getie Y Wondimeneh G Getnet et al ldquoPrevalence andclinical correlates of Schistosoma mansoni co-infection amongmalaria infected patients Northwest Ethiopiardquo BMC ResearchNotes vol 8 no 1 article no 480 2015
[56] E Okafor and A Elenwo ldquoHaemoglobin status of children withmixed infection ofmalaria and urinary schistosomiasis inOdauCommunity Rivers state Nigeriardquo Journal of Agriculture andSocial Research vol 7 no 1 pp 56ndash62 2008
[57] M A McDevitt J Xie V Gordeuk and R Bucala ldquoThe anemiaof malaria infection role of inflammatory cytokinesrdquo CurrentHematology Reports vol 3 no 2 pp 97ndash106 2004
[58] J G Shaw and J F Friedman ldquoIron deficiency anemia focus oninfectious diseases in lesser developed countriesrdquo Anemia vol2011 Article ID 260380 10 pages 2011
[59] H K Green J C Sousa-Figueiredo M-G Basanez et alldquoAnaemia in Ugandan preschool-aged children the relativecontribution of intestinal parasites and malariardquo Parasitologyvol 138 no 12 pp 1534ndash1545 2011
[60] E Ivan N J Crowther E Mutimura L O Osuwat S Janssenand M P Grobusch ldquoHelminthic infections rates and malaria
in HIV-infected pregnant women on anti-retroviral therapy inRwandardquo PLoS Neglected Tropical Diseases vol 7 no 8 ArticleID e2380 2013
1205942 P value 417 00411205942 Pearson Chi-square test OR odd ratioOR adjusted using multivariate regression analysis
type of activity carried out in the stream and P falciparumparasitaemia in bivariate analysis (Table 2) The prevalenceof infection did not differ significantly with marital statuseducational level and occupational status In multivariate
analysis (controlling for age and gravidity status as con-founders) younger age groups le20 (aOR = 152 95 CI 17ndash1383) and 21ndash25 years (aOR = 73 95 CI 12ndash443) andbathing and domestic contact with stream (aOR = 335 95
6 Journal of Parasitology Research
CI 97ndash1159)were risk factors associatedwith S haematobiuminfection On the other hand less water contact frequency(1 to 2 times per day) (aOR = 28119864 minus 10 95 CI 94119864 minus11ndash85119864minus10) was associated with decreased risk of infectionSurprisingly primigravidity (OR = 02 95 CI 003ndash09)and secundigravidity (OR = 01 95 CI 002ndash04) wereless likely at risk Intensity of infection was associated withmalaria parasitaemia where light egg density infection wasless common (aOR = 04 95 CI 02ndash07 119875 = 0004)in malaria positive women (219 1464) than in malarianegative women (781 5064)
424 Factors Associated with Prevalence of P falciparumInfection The prevalence of P falciparum infection wasassociated (1205942 = 1782 119875 lt 001) with IPTp-SP uptake wheremalaria parasite infection was greater in women who had nottaken IPTp-SP (580) than in those who had at least one SPdose (302) The occurrence of P falciparum infection didnot differ significantly with maternal age gravidity status orITN usage
425 Factors Associated with Prevalence of Coinfection with Shaematobium and P falciparum Coinfection was associatedwith the type of activity carried out in the stream and watercontact frequency as well as IPTp-SP uptake Bathing anddomestic contact with stream (aOR = 133 95 CI 22ndash795) increased risk of coinfection among pregnant womenmeanwhile less water contact frequency (1 to 2 times per day(aOR = 01 95 CI 001ndash04) and 3 to 4 times per day (aOR =03 95 CI 01ndash09)) decreased risk of coinfection Womenwho had at least one SP dose were less likely (aOR= 006 95CI 002ndash02) to be coinfected (Table 3)
43 Haemoglobin Levels and Anaemia Themean (plusmnSD) hae-moglobin level of the pregnant women enrolled in the studywas 90 plusmn 16 gdL (range 61ndash137 gdL) Coinfection signif-icantly reduced Hb levels of pregnant women in the studyarea where levels in coinfected individuals were significantlylower (119875 lt 0001) when compared with levels seen withsingle infections (S haematobium and P falciparum) and noinfection (Table 4) In addition Hb levels were significantlylower among women coinfected with P falciparum and heavyS haematobium infections than in individuals coinfectedwith P falciparum and light S haematobium infection andthose with no infection (Table 5) Although age maritalstatus educational level occupational status infection statusand IPTp-SP uptake were identified as factors associatedwith Hb levels IPTp-SP was seen as the only independentpredictor of Hb levels taking into consideration all possibleconfounding variables (Table 4)
Anaemia prevalence was 888 (222250) with anaemiaseverity as follows mild (132 119899 = 33) moderate (628119899 = 157) and severe (128 119899 = 32) All cases diagnosedwithcoinfection were anaemic (Table 6) Coinfection accountedfor 938 (3032) of all severe anaemia cases with majority719 (2332) of the severe anaemic cases coinfected withP falciparum and heavy density S haematobium infections(Table 5) Uptake of IPTp-SP (438 1432) was associated
(1205942 = 1132 119875 = 001) with reduced percentage of severeanaemia compared with that observed among women withno SP (563 1832) Risk factors found to be associated withincreased odds of anaemia were P falciparum infection (OR=40 95 CI 10ndash145) and occupation (business) (OR = 20195 CI 40ndash101) (Table 6)
5 Discussion
To our knowledge this is the first study carried out on uro-genital schistosomiasis among pregnant women in Camer-oon This study determined the prevalence of S haemato-bium P falciparum and coinfection factors associated withthese infections and assessed their relative effect on anaemiaprevalence and severity among pregnant women in Mun-yenge S haematobium and P falciparum infections are com-mon among pregnant women living in Munyenge and theircoinfection exacerbates anaemia
The prevalence of S haematobium infection among preg-nant women in our study was 468 The high prevalencereflects high exposure to infection among pregnant womenliving in Munyenge due to absolute dependence on naturalwater sources for domestic activities and bathing Comparedto the level of infection in the present study lower prevalenceof urogenital schistosomiasis among pregnant women hasbeen reported inNigeria by Eyo et al [42] (238) and Salawuand Odaibo [43] (208) Differences in the method usedfor the detection of S haematobium infection may partlyexplain the observed differences in rates Although thesestudies attributed the lower prevalence levels of urinary schis-tosomiasis among pregnant women to a taboo restrictingpregnant women from visiting natural water bodies [42]compared with urine filtration method used in our study thelower sensitive centrifugation method use in the diagnosisof S haematobium infection in the Nigerian studies mayhave underestimated true infection levelsMalaria is commonamong pregnant women in the study area with a prevalenceof 392 The only factor seen to be associated with malariaparasite infection in this study site was IPTp uptake Theeffectiveness of IPTp-SP in the prevention of malaria inpregnancy is well established [34 44]
For transmission of schistosomiasis to take place theschistosomes parasite requires an avenue where it is indirect contact with the human host [9] Pregnant womenliving in Munyenge get in contact with infection duringactivities such as laundry plate washing and water fetchingfor domestic use In addition to domestic activities bathingin streams poses a greater risk of infection among pregnantwomen in this area Analyses from other studies have shownthat regularly bathing in water sources contaminated withthe developmental stages of the schistosomes parasite wasassociated with prevalence and intensity of schistosomiasis[45ndash47]Moreover increased risk of infection associatedwiththe number and duration of water contact with infestedwaters per day has also been reported [47] Women whoreported surface-water contact at least 3 to 5 times perday were at greater risk of infection due to longer periodof contact with contaminated water Health education toinstruct pregnant women to make less surface-water contact
Journal of Parasitology Research 7
Table 3 Risk factors associated with coinfection with S haematobium and P falciparum among pregnant women in Munyenge
1205942 119875 value 1329 lt00011205942 Pearson Chi-square test OR odd ratioAdjusted OR using multivariate regression analysis
frequency and the implication of voiding their bladder inwater bodies is paramount These behavioural changes willsignificantly reduce the risk of S haematobium infectionamong pregnant women and contamination of water sourcesin this setting Ultimately provision of portable water andimproved sanitation system will play a major role in decreas-ing disease transmission and incidence
Age as observed in most schistosomiasis surveys was amajor determinant of schistosomes infection among preg-nant women in our study area The highest prevalence val-ues of urogenital schistosomiasis were recorded in youngerwomen (le25 years) Individuals within le20 age group werefound to be at a greater risk of S haematobium infection withprevalence of 554 This is in agreement with trends estab-lished in schistosomiasis surveys carried out in Cameroon
[32 48] and other parts of Africa [42 43] Alternativelythe decrease risk of infection observed in older age groups(gt25 years) conformed to earlier reports [32 42] Studieshave reported that age-acquired immunity to reinfection andchanges in water contact patterns contribute to the decliningtrend in prevalence with increasing age [49] Older womenare less likely to be engaged in water contact behaviourscompared to younger women Age dependent immunity toS haematobium has been shown to affect mean egg outputof infected persons [49] Socioeconomic status of the womenwas not an independent factor associated with S haema-tobium prevalence in this high-risk community Similarlyreports from other rural settings endemic for schistosomi-asis failed to identify any socioeconomic variables that arestrongly associated with schistosomiasis prevalence [50 51]
8 Journal of Parasitology Research
Table 4 Factors associated with mean (plusmnSD) haemoglobin levels among pregnant women in Munyenge Health Area
Factors Category Mean (plusmnSD) Hblevels Test-value Unadjusted
lowastAnalysis of variance test (ANOVA)$Studentrsquos 119905-testampAdjusted 119875 values using multilinear regression analysisNA not applicable variables with 119875 gt 02 in bivariate analysis were not included in regression analysis
Table 5 Association between S haematobium intensity P falciparum infection and mean (plusmnSD) haemoglobin levels and anaemia severity
lowastSignificance level 119865 = 1240 119875 lt 0001lowastAnalysis of variance test (ANOVA)ampPearson Chi-Square test
The absence of association between socioeconomic variablesand infection prevalencemay be attributed to general povertyand uniformity in high exposure risk in the population [50]
The overall prevalence of coinfection with S haema-tobium and P falciparum infection was 152 suggestingcoendemicity of both infections in the study area SimilarlyYatich et al [52] reported a helminth andmalaria coinfectionprevalence of 166 among pregnant women in Ghana Theimpact of helminth infections on malaria parasitaemia and
disease during coinfection is an established phenomenonalthough much is still unknown and contradictions persist[53 54]We observed that light S haematobium infectionwasless common (aOR= 04) among pregnant women coinfectedwith P falciparum suggesting a negative interaction betweenboth parasites [4] In accordance with findings of Getie etal [55] schistosomiasis coinfection could affect Plasmodiumparasitemia and vice versa depending on the intensity of theova in coinfected persons Nonetheless a further study is
Journal of Parasitology Research 9
Table 6 Risk factors associated with anaemia among pregnant women in Munyenge Health Area
Factors Category Anaemia prevalence Adjusted OR (95 CI) 119875 value
Adjusted OR using multivariate regression analysisNA not applicable variables with 119875 gt 02 in bivariate analysis were not included in multivariate analysis
needed to explore the underlying mechanisms of interactionbetween malaria parasitaemia and S haematobium
Schistosomiasis causes long term morbidity such asanaemia Our study showed that the magnitude of S haema-tobium egg counts is significantly related to haemoglobinconcentration confirming that urogenital schistosomiasiscontributes to anaemia [24 25] In this study anaemiawas more pronounced in women with heavy infectionintensity than in those with light infection Coinfection ofhelminth infections and P falciparum increases anaemiaseverity [8 9] Coinfection among pregnant women lowersHb concentration compared with single infection This is inagreement with findings of Okafor and Elenwo [56] Moreso coinfected women with heavy intensity S haematobiuminfection had the lowest mean Hb levels (66 gdL) andthis subpopulation of women contributed to about 72of all severe anaemic cases The combined presence and
interaction of S haematobium and P falciparum infectionsis partly responsible for the low haemoglobin concentrationin women with concurrent infectionMalaria causes anaemiaby destruction and removal of parasitized red blood cellsand shortening of the life span of nonparasitized red cellsas well as decreasing the rate of erythrocyte production inbone marrow [57]Themechanism by which schistosomiasiscauses anaemia is not fully understood but it is suggested thathelminth infections could contribute to increase in the preva-lence of inflammatory syndromes impairing erythropoiesisand interfering with mobilization of reticuloendothelial ironstorages and shortening erythrocyte survival [58] Similar toprevious reports of a study in Uganda [59] malaria parasiteinfection was an independent factor associated with increaseanaemia risk
The risk of coinfection was associated with streamusage (bathing and domestic contact with stream) while
10 Journal of Parasitology Research
less water contact and SP usage decreased risk of infectionThis finding suggests that intervention strategies focusingon combating malaria and schistosomiasis respectively byincreasing the uptake of IPTp-SPdoses and less water contactamong pregnant women living in Munyenge represents themost appropriate prevention of coinfection with consequentincrease in Hb levels
This study had one limitation We did not investigate theprevalence of HIV infection among the study participants Ithas been shown that coinfections with helminths andmalariacause considerable morbidity in the host particularly in thepresence of HIV infection [60]
To conclude the study has indicated that S haematobiumand P falciparum infections are common among pregnantwomen living in Munyenge and their coinfection is influ-enced by high frequencies of these parasites in the same pop-ulationThe study also revealed that younger age and bathingand domestic contact with stream are independently associ-ated with prevalence of S haematobium infection while noIPTp-SP was associated with P falciparum infection Streamusage increased risk of coinfection while less water contactand SP usage decreased its risk The fact that light S haema-tobium infection was less common in P falciparum infectedwomen suggests that Plasmodium falciparum parasitaemiamay be associatedwith intensity of urogenital schistosomiasisin coinfected individuals Anaemia is a severe public healthproblem in pregnancy in Munyenge and coinfection withS haematobium and P falciparum exacerbates anaemiaLess water contact frequency and increase uptake of IPTp-SPdoses will significantly reduce risk of coinfection andconsequently anaemia severity in pregnancy in this setting
Abbreviations
IPTp-SP Intermittent preventive treatment in pregnancy(IPTp) with sulfadoxine-pyrimethamine (SP)
ITN Insecticide treated bed netsHIV Human immunodeficiency virusANC Antenatal care
Competing Interests
The authors declare that they do not have any competinginterests
Authorsrsquo Contributions
Judith K Anchang-Kimbi conceived and designed the studyanalyzed the data and wrote the manuscript Dillys MansohElad participated in the design of the study performedthe experiments and made inputs in manuscript write-upGemain Taiwe Sotoing and Eric Akum Achidi supervisedreviewed and provided inputs to the manuscript All authorsread and approved the final manuscript
Acknowledgments
The authors are grateful to all the pregnant women whogave their consent to participate in the study Special thanks
are due to the chief medical officer nurses and laboratorytechnician of the Munyenge Health Centre for their cooper-ation and contribution This study received financial supportfrom the Ministry of Higher Education University ResearchModernisation grant given to authors Judith K Anchang-Kimbi and Eric Akum Achidi
References
[1] T N Petney and R H Andrews ldquoMultiparasite communitiesin animals and humans frequency structure and pathogenicsignificancerdquo International Journal for Parasitology vol 28 no3 pp 377ndash393 1998
[2] F E G Cox ldquoConcomitant infections parasites and immuneresponsesrdquo Parasitology vol 122 supplement 1 pp S23ndashS382001
[3] M Nacher P Singhasivanon S Yimsamran et al ldquoIntestinalhelminth infections are associated with increased incidenceof Plasmodium falciparum malaria in Thailandrdquo Journal ofParasitology vol 88 no 1 pp 55ndash58 2002
[4] J-Y Le Hesran J Akiana E H M Ndiaye M Dia P Senghorand L Konate ldquoSevere malaria attack is associated with highprevalence of Ascaris lumbricoides infection among childrenin rural Senegalrdquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 98 no 7 pp 397ndash399 2004
[5] M Nacher F Gay P Singhasivanon et al ldquoAscaris lumbricoidesinfection is associated with protection from cerebral malariardquoParasite Immunology vol 22 no 3 pp 107ndash113 2000
[6] V Briand L Watier J-Y Le Hesran A Garcia and M CotldquoCoinfection with Plasmodium falciparum and Schistosomahaematobium protective effect of schistosomiasis on malariain Senegalese childrenrdquo American Journal of Tropical Medicineand Hygiene vol 72 no 6 pp 702ndash707 2005
[7] N Oslash Christensen P Furu J Kurtzhals and A OdaiboldquoHeterologous synergistic interactions in concurrent experi-mental infection in the mouse with Schistosoma mansoniEchinostoma revolution Plasmodium yoelii Babesia microtiand Trypanosoma bruceirdquo Parasitology Research vol 74 no 6pp 544ndash551 1988
[8] G Raso A Luginbuhl C A Adjoua et al ldquoMultiple parasiteinfections and their relationship to self-reported morbidity ina community of rural Cote drsquoIvoirerdquo International Journal ofEpidemiology vol 33 no 5 pp 1092ndash1102 2004
[9] S Brooker W Akhwale R Pullan et al ldquoEpidemiology ofPlasmodium-helminth co-infection in Africa populations atrisk potential impact on anemia and prospects for combiningcontrolrdquo American Journal of Tropical Medicine and Hygienevol 77 no 6 pp 88ndash98 2007
[10] C E Shulman and E K Dorman ldquoReducing childhood mor-tality in poor countries importance and prevention of malariain pregnancyrdquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 97 no 1 pp 30ndash35 2003
[11] WorldHealthOrganisation andAfrica Regional OfficeMalariaPrevention and Control during Pregnancy in the African RegionWHOAFRO Brazzaville Congo 2004
[12] D Engels L Chitsulo A Montresor and L Savioli ldquoTheglobal epidemiological situation of schistosomiasis and newapproaches to control and researchrdquo Acta Tropica vol 82 no2 pp 139ndash146 2002
[13] P J Hotez and A Kamath ldquoNeglected tropical diseases in sub-Saharan Africa review of their prevalence distribution and
[14] M J Van Der Werf S J De Vlas S Brooker et al ldquoQuantifica-tion of clinical morbidity associated with schistosome infectionin sub-Saharan Africardquo Acta Tropica vol 86 no 2-3 pp 125ndash139 2003
[15] M N Nour ldquoSchistosomias health effect on womenrdquo Reviewsin Obstetrics amp Gynecology vol 3 no 1 pp 28ndash32 2010
[16] J F Friedman P Mital H K Kanzaria G R Olds and J DKurtis ldquoSchistosomiasis and pregnancyrdquo Trends in Parasitologyvol 23 no 4 pp 159ndash164 2007
[17] httpwwwwhointschistosomiasisstrategyen[18] H N Ntonifor and J A Ajayi ldquoWater contact and Schistosoma
haematobium infection A case study of some communitiesin Toro Local Government council Area (TLGCA) of BauchiStaterdquoNigeria Journal of Natural and Applied Sciences vol 1 no1 pp 54ndash59 2005
[19] P Saotoing T Vroumsia A M Njan F N Tchuenguem andJ Messi ldquoEpidemiological survey of schistosomiasis due toSchistosoma haematobium in some primary schools in thetown of Maroua far north region Cameroonrdquo InternationalJournal of Tropical Medicine vol 6 no 2 pp 19ndash24 2011
[20] L A Tchuem Tchuente R I K Ngassam L Sumo et al ldquoMap-ping of schistosomiasis and soil- transmitted helminthiasis inthe regions of centre east and west cameroonrdquo PLoS NeglectedTropical Diseases vol 6 no 3 p e1553 2012
[21] L A Tchuem Tchuente N C Dongmo P Ngassam et alldquoMapping of schistosomiasis and soil- transmitted helminthi-asis in the regions of Littoral North-West South and South-West Cameroon and recommendations for treatmentrdquo BMCInfectious Disease vol 13 article 602 2013
[22] K J N Ndamukong M A Ayuk J S Dinga T N Akenji VA Ndiforchu and V P K Titanji ldquoPrevalence and intensity ofurinary schistosomiasis in primary school children of the KottoBarombi health area Cameroonrdquo East African Medical Journalvol 78 no 6 pp 287ndash289 2001
[23] H N Ntonifor G N Mbunkur and N W Ndaleh ldquoEpidemi-ological survey of urinary schistosomiasis in some primaryschools in a new focus behind Mount Cameroon (Munyenge)South West Region Cameroonrdquo East African Medical Journalvol 89 no 3 pp 82ndash88 2012
[24] J F Friedman H K Kanzaria and S T McGarvey ldquoHumanschistosomiasis and anemia the relationship and potentialmechanismsrdquo Trends in Parasitology vol 21 no 8 pp 386ndash3922005
[25] A Ajanga N J S Lwambo L Blair U Nyandindi A Fenwickand S Brooker ldquoSchistosoma mansoni in pregnancy andassociations with anaemia in northwest Tanzaniardquo Transactionsof the Royal Society of Tropical Medicine and Hygiene vol 100no 1 pp 59ndash63 2006
[26] G Helling-Giese E F Kjetland S G Gundersen et al ldquoSchis-tosomiasis in women manifestations in the upper reproductivetractrdquo Acta Tropica vol 62 no 4 pp 225ndash238 1996
[27] R W Steketee B L Nahlen M E Parise and C MenendezldquoTheburden ofmalaria in pregnancy inmalaria-endemic areasrdquoAmerican Journal of Tropical Medicine and Hygiene vol 64 no1-2 pp 28ndash35 2001
[28] V V Laxman B Adamson and T Mahmood ldquoRecurrentectopic pregnancy due to Schistosoma hematobiumrdquo Journal ofObstetrics and Gynaecology vol 28 no 4 pp 461ndash462 2008
[29] S Bahrami H Alatassi S P Slone and D M OrsquoConnorldquoTubal gestation and schistosomiasis a case reportrdquo Journal ofReproductiveMedicine for theObstetrician andGynecologist vol51 no 7 pp 595ndash598 2006
[30] P S Mbabazi O Andan D W Fitzgerald L Chitsulo DEngels and J A Downs ldquoExamining the relationship betweenurogenital schistosomiasis and HIV infectionrdquo PLoS NeglectedTropical Diseases vol 5 no 12 Article ID e1396 2011
[31] R Tweyongyere P A Mawa N O Emojong et al ldquoEffectof praziquantel treatment of Schistosomamansoni during preg-nancy on intensity of infection and antibody responses to schis-tosome antigens results of a randomised placebo-controlledtrialrdquo BMC Infectious Diseases vol 9 article 32 2009
[32] H N Ntonifor A E Green M O S Bopda et al ldquoEpi-demiology of urinary schistosomiasis and soil transmittedhelminthiasis in a recently established focus behind MountCameroonrdquo International Journal of Current Microbiology andApplied Sciences vol 4 no 3 pp 1056ndash1066 2015
[33] S Wanji A J Kengne-Ouafo E E Joan Eyong et al ldquoGeneticdiversity of Plasmodium falciparummerozoite surface protein-1 block 2 in sites of contrasting altitudes and malaria endemic-ities in the Mount Cameroon Regionrdquo American Journal ofTropical Medicine and Hygiene vol 86 no 5 pp 764ndash774 2012
[34] J K Anchang-Kimbi E A Achidi B Nkegoum E Sverremark-Ekstrom and M Troye-Blomberg ldquoDiagnostic comparisonof malaria infection in peripheral blood placental blood andplacental biopsies in Cameroonian parturient womenrdquoMalariaJournal vol 8 no 1 article 126 2009
[35] F J Bryan The Design and Analysis of Research Studies Uni-versity ofOtago Dunedin NewZealand CambridgeUniversityPress Cambridge UK 1992
[36] World Health Organisation Haemoglobin Concentrations forthe Diagnosis of Anaemia and Assessment of Severity Vitaminand mineral Nutrition Information System WHO GenevaSwitzerland 2011
[37] M CheesbroughDistrict Laboratory Practice in Tropical Coun-tries Cambridge University Press Cambridge UK 2006
[39] N O Christensen G Gotsche and F Frandsen ParasitologicalTechniques for Use in Routine Laboratory Maintainance of Schis-tosomes and Used in Studies on the Epidemiology of Human andBovine Schistosomiasis Danish Bilhaziasis Laboratory Manual1984
[40] World Health OrganizationmdashTropical Disease Research TDRstrategic direction Schistosomiasis WHO-TDR 2002
[41] World Health OrganizationGuidelines for the Evaluation of SoilTransmitted Helminthiasis and Schistosomiasis at CommunityLevel A Guide for Managers of Control Programme WHOGeneva Switzerland 1993
[42] J E Eyo G C Onyishi and F C Okafor ldquoUrinary schisto-somiasis among pregnant women in some endemic tropicalsemi-urban communities of Anambra State Nigeriardquo TropicalBiomedicine vol 29 no 4 pp 575ndash579 2012
[43] O T Salawu and A B Odaibo ldquoSchistosomiasis among preg-nant women in rural communities in Nigeriardquo InternationalJournal of Gynecology andObstetrics vol 122 no 1 pp 1ndash4 2013
[44] K R Tan B L Katalenich K E Mace et al ldquoEfficacyof sulphadoxine-pyrimethamine for intermittent preventivetreatment of malaria in pregnancy Mansa Zambiardquo MalariaJournal vol 13 no 1 article 227 2014
12 Journal of Parasitology Research
[45] J Bethony J T Williams H Kloos et al ldquoExposure toSchistosoma mansoni infection in a rural area in Brazil IIhousehold risk factorsrdquo Tropical Medicine and InternationalHealth vol 6 no 2 pp 136ndash145 2001
[46] J C Sousa-Figueiredo D Gamboa J M Pedro et al ldquoEpi-demiology of malaria schistosomiasis geohelminths anemiaand malnutrition in the context of a demographic surveillancesystem in northern Angolardquo PLoS ONE vol 7 no 4 Article IDe33189 2012
[47] F Anto V Asoala M Adjuik et al ldquoWater contact activitiesand prevalence of schistosomiasis infection among school-agechildren in communities along an irrigation scheme in RuralNorthern Ghanardquo Journal of Bacteriology amp Parasitology vol 4article 177 2013
[48] L-A Tchuem Tchuente J M Behnke F S Gilbert V RSouthgate and J Vercruysse ldquoPolyparasitism with Schistosomahaematobium and soil-transmitted helminth infections amongschool children in Loum Cameroonrdquo Tropical Medicine andInternational Health vol 8 no 11 pp 975ndash986 2003
[49] J-F Etard M Audibert and A Dabo ldquoAge-acquired resistanceand predisposition to reinfection with Schistosoma haemato-bium after treatment with praziquantel in Malirdquo The AmericanJournal of TropicalMedicine andHygiene vol 52 no 6 pp 549ndash558 1995
[50] A Gazzinelli G Velasquez-Melendez S B Crawford P TLoVerde R Correa-Oliveira and H Kloos ldquoSocioeconomicdeterminants of schistosomiasis in a poor rural area in BrazilrdquoActa Tropica vol 99 no 2-3 pp 260ndash271 2006
[51] A P Kapito-Tembo V Mwapasa S R Meshnick et al ldquoPreva-lence distribution and risk factors for Schistosoma hematobiuminfection among school children in Blantyre Malawirdquo PLoSNeglected Tropical Diseases vol 3 no 1 article e361 2009
[52] N J Yatich J Yi T Agbenyega et al ldquoMalaria and intestinalhelminth co-infection among pregnant women in Ghanaprevalence and risk factorsrdquo The American Journal of TropicalMedicine and Hygiene vol 80 no 6 pp 896ndash901 2009
[53] M Nacher ldquoInteractions between worms and malaria goodworms or bad wormsrdquoMalaria Journal vol 10 article no 2592011
[54] A A Adegnika and P G Kremsner ldquoEpidemiology of malariaand helminth interaction a review from 2001 to 2011rdquo CurrentOpinion in HIV and AIDS vol 7 no 3 pp 221ndash224 2012
[55] S Getie Y Wondimeneh G Getnet et al ldquoPrevalence andclinical correlates of Schistosoma mansoni co-infection amongmalaria infected patients Northwest Ethiopiardquo BMC ResearchNotes vol 8 no 1 article no 480 2015
[56] E Okafor and A Elenwo ldquoHaemoglobin status of children withmixed infection ofmalaria and urinary schistosomiasis inOdauCommunity Rivers state Nigeriardquo Journal of Agriculture andSocial Research vol 7 no 1 pp 56ndash62 2008
[57] M A McDevitt J Xie V Gordeuk and R Bucala ldquoThe anemiaof malaria infection role of inflammatory cytokinesrdquo CurrentHematology Reports vol 3 no 2 pp 97ndash106 2004
[58] J G Shaw and J F Friedman ldquoIron deficiency anemia focus oninfectious diseases in lesser developed countriesrdquo Anemia vol2011 Article ID 260380 10 pages 2011
[59] H K Green J C Sousa-Figueiredo M-G Basanez et alldquoAnaemia in Ugandan preschool-aged children the relativecontribution of intestinal parasites and malariardquo Parasitologyvol 138 no 12 pp 1534ndash1545 2011
[60] E Ivan N J Crowther E Mutimura L O Osuwat S Janssenand M P Grobusch ldquoHelminthic infections rates and malaria
in HIV-infected pregnant women on anti-retroviral therapy inRwandardquo PLoS Neglected Tropical Diseases vol 7 no 8 ArticleID e2380 2013
CI 97ndash1159)were risk factors associatedwith S haematobiuminfection On the other hand less water contact frequency(1 to 2 times per day) (aOR = 28119864 minus 10 95 CI 94119864 minus11ndash85119864minus10) was associated with decreased risk of infectionSurprisingly primigravidity (OR = 02 95 CI 003ndash09)and secundigravidity (OR = 01 95 CI 002ndash04) wereless likely at risk Intensity of infection was associated withmalaria parasitaemia where light egg density infection wasless common (aOR = 04 95 CI 02ndash07 119875 = 0004)in malaria positive women (219 1464) than in malarianegative women (781 5064)
424 Factors Associated with Prevalence of P falciparumInfection The prevalence of P falciparum infection wasassociated (1205942 = 1782 119875 lt 001) with IPTp-SP uptake wheremalaria parasite infection was greater in women who had nottaken IPTp-SP (580) than in those who had at least one SPdose (302) The occurrence of P falciparum infection didnot differ significantly with maternal age gravidity status orITN usage
425 Factors Associated with Prevalence of Coinfection with Shaematobium and P falciparum Coinfection was associatedwith the type of activity carried out in the stream and watercontact frequency as well as IPTp-SP uptake Bathing anddomestic contact with stream (aOR = 133 95 CI 22ndash795) increased risk of coinfection among pregnant womenmeanwhile less water contact frequency (1 to 2 times per day(aOR = 01 95 CI 001ndash04) and 3 to 4 times per day (aOR =03 95 CI 01ndash09)) decreased risk of coinfection Womenwho had at least one SP dose were less likely (aOR= 006 95CI 002ndash02) to be coinfected (Table 3)
43 Haemoglobin Levels and Anaemia Themean (plusmnSD) hae-moglobin level of the pregnant women enrolled in the studywas 90 plusmn 16 gdL (range 61ndash137 gdL) Coinfection signif-icantly reduced Hb levels of pregnant women in the studyarea where levels in coinfected individuals were significantlylower (119875 lt 0001) when compared with levels seen withsingle infections (S haematobium and P falciparum) and noinfection (Table 4) In addition Hb levels were significantlylower among women coinfected with P falciparum and heavyS haematobium infections than in individuals coinfectedwith P falciparum and light S haematobium infection andthose with no infection (Table 5) Although age maritalstatus educational level occupational status infection statusand IPTp-SP uptake were identified as factors associatedwith Hb levels IPTp-SP was seen as the only independentpredictor of Hb levels taking into consideration all possibleconfounding variables (Table 4)
Anaemia prevalence was 888 (222250) with anaemiaseverity as follows mild (132 119899 = 33) moderate (628119899 = 157) and severe (128 119899 = 32) All cases diagnosedwithcoinfection were anaemic (Table 6) Coinfection accountedfor 938 (3032) of all severe anaemia cases with majority719 (2332) of the severe anaemic cases coinfected withP falciparum and heavy density S haematobium infections(Table 5) Uptake of IPTp-SP (438 1432) was associated
(1205942 = 1132 119875 = 001) with reduced percentage of severeanaemia compared with that observed among women withno SP (563 1832) Risk factors found to be associated withincreased odds of anaemia were P falciparum infection (OR=40 95 CI 10ndash145) and occupation (business) (OR = 20195 CI 40ndash101) (Table 6)
5 Discussion
To our knowledge this is the first study carried out on uro-genital schistosomiasis among pregnant women in Camer-oon This study determined the prevalence of S haemato-bium P falciparum and coinfection factors associated withthese infections and assessed their relative effect on anaemiaprevalence and severity among pregnant women in Mun-yenge S haematobium and P falciparum infections are com-mon among pregnant women living in Munyenge and theircoinfection exacerbates anaemia
The prevalence of S haematobium infection among preg-nant women in our study was 468 The high prevalencereflects high exposure to infection among pregnant womenliving in Munyenge due to absolute dependence on naturalwater sources for domestic activities and bathing Comparedto the level of infection in the present study lower prevalenceof urogenital schistosomiasis among pregnant women hasbeen reported inNigeria by Eyo et al [42] (238) and Salawuand Odaibo [43] (208) Differences in the method usedfor the detection of S haematobium infection may partlyexplain the observed differences in rates Although thesestudies attributed the lower prevalence levels of urinary schis-tosomiasis among pregnant women to a taboo restrictingpregnant women from visiting natural water bodies [42]compared with urine filtration method used in our study thelower sensitive centrifugation method use in the diagnosisof S haematobium infection in the Nigerian studies mayhave underestimated true infection levelsMalaria is commonamong pregnant women in the study area with a prevalenceof 392 The only factor seen to be associated with malariaparasite infection in this study site was IPTp uptake Theeffectiveness of IPTp-SP in the prevention of malaria inpregnancy is well established [34 44]
For transmission of schistosomiasis to take place theschistosomes parasite requires an avenue where it is indirect contact with the human host [9] Pregnant womenliving in Munyenge get in contact with infection duringactivities such as laundry plate washing and water fetchingfor domestic use In addition to domestic activities bathingin streams poses a greater risk of infection among pregnantwomen in this area Analyses from other studies have shownthat regularly bathing in water sources contaminated withthe developmental stages of the schistosomes parasite wasassociated with prevalence and intensity of schistosomiasis[45ndash47]Moreover increased risk of infection associatedwiththe number and duration of water contact with infestedwaters per day has also been reported [47] Women whoreported surface-water contact at least 3 to 5 times perday were at greater risk of infection due to longer periodof contact with contaminated water Health education toinstruct pregnant women to make less surface-water contact
Journal of Parasitology Research 7
Table 3 Risk factors associated with coinfection with S haematobium and P falciparum among pregnant women in Munyenge
1205942 119875 value 1329 lt00011205942 Pearson Chi-square test OR odd ratioAdjusted OR using multivariate regression analysis
frequency and the implication of voiding their bladder inwater bodies is paramount These behavioural changes willsignificantly reduce the risk of S haematobium infectionamong pregnant women and contamination of water sourcesin this setting Ultimately provision of portable water andimproved sanitation system will play a major role in decreas-ing disease transmission and incidence
Age as observed in most schistosomiasis surveys was amajor determinant of schistosomes infection among preg-nant women in our study area The highest prevalence val-ues of urogenital schistosomiasis were recorded in youngerwomen (le25 years) Individuals within le20 age group werefound to be at a greater risk of S haematobium infection withprevalence of 554 This is in agreement with trends estab-lished in schistosomiasis surveys carried out in Cameroon
[32 48] and other parts of Africa [42 43] Alternativelythe decrease risk of infection observed in older age groups(gt25 years) conformed to earlier reports [32 42] Studieshave reported that age-acquired immunity to reinfection andchanges in water contact patterns contribute to the decliningtrend in prevalence with increasing age [49] Older womenare less likely to be engaged in water contact behaviourscompared to younger women Age dependent immunity toS haematobium has been shown to affect mean egg outputof infected persons [49] Socioeconomic status of the womenwas not an independent factor associated with S haema-tobium prevalence in this high-risk community Similarlyreports from other rural settings endemic for schistosomi-asis failed to identify any socioeconomic variables that arestrongly associated with schistosomiasis prevalence [50 51]
8 Journal of Parasitology Research
Table 4 Factors associated with mean (plusmnSD) haemoglobin levels among pregnant women in Munyenge Health Area
Factors Category Mean (plusmnSD) Hblevels Test-value Unadjusted
lowastAnalysis of variance test (ANOVA)$Studentrsquos 119905-testampAdjusted 119875 values using multilinear regression analysisNA not applicable variables with 119875 gt 02 in bivariate analysis were not included in regression analysis
Table 5 Association between S haematobium intensity P falciparum infection and mean (plusmnSD) haemoglobin levels and anaemia severity
lowastSignificance level 119865 = 1240 119875 lt 0001lowastAnalysis of variance test (ANOVA)ampPearson Chi-Square test
The absence of association between socioeconomic variablesand infection prevalencemay be attributed to general povertyand uniformity in high exposure risk in the population [50]
The overall prevalence of coinfection with S haema-tobium and P falciparum infection was 152 suggestingcoendemicity of both infections in the study area SimilarlyYatich et al [52] reported a helminth andmalaria coinfectionprevalence of 166 among pregnant women in Ghana Theimpact of helminth infections on malaria parasitaemia and
disease during coinfection is an established phenomenonalthough much is still unknown and contradictions persist[53 54]We observed that light S haematobium infectionwasless common (aOR= 04) among pregnant women coinfectedwith P falciparum suggesting a negative interaction betweenboth parasites [4] In accordance with findings of Getie etal [55] schistosomiasis coinfection could affect Plasmodiumparasitemia and vice versa depending on the intensity of theova in coinfected persons Nonetheless a further study is
Journal of Parasitology Research 9
Table 6 Risk factors associated with anaemia among pregnant women in Munyenge Health Area
Factors Category Anaemia prevalence Adjusted OR (95 CI) 119875 value
Adjusted OR using multivariate regression analysisNA not applicable variables with 119875 gt 02 in bivariate analysis were not included in multivariate analysis
needed to explore the underlying mechanisms of interactionbetween malaria parasitaemia and S haematobium
Schistosomiasis causes long term morbidity such asanaemia Our study showed that the magnitude of S haema-tobium egg counts is significantly related to haemoglobinconcentration confirming that urogenital schistosomiasiscontributes to anaemia [24 25] In this study anaemiawas more pronounced in women with heavy infectionintensity than in those with light infection Coinfection ofhelminth infections and P falciparum increases anaemiaseverity [8 9] Coinfection among pregnant women lowersHb concentration compared with single infection This is inagreement with findings of Okafor and Elenwo [56] Moreso coinfected women with heavy intensity S haematobiuminfection had the lowest mean Hb levels (66 gdL) andthis subpopulation of women contributed to about 72of all severe anaemic cases The combined presence and
interaction of S haematobium and P falciparum infectionsis partly responsible for the low haemoglobin concentrationin women with concurrent infectionMalaria causes anaemiaby destruction and removal of parasitized red blood cellsand shortening of the life span of nonparasitized red cellsas well as decreasing the rate of erythrocyte production inbone marrow [57]Themechanism by which schistosomiasiscauses anaemia is not fully understood but it is suggested thathelminth infections could contribute to increase in the preva-lence of inflammatory syndromes impairing erythropoiesisand interfering with mobilization of reticuloendothelial ironstorages and shortening erythrocyte survival [58] Similar toprevious reports of a study in Uganda [59] malaria parasiteinfection was an independent factor associated with increaseanaemia risk
The risk of coinfection was associated with streamusage (bathing and domestic contact with stream) while
10 Journal of Parasitology Research
less water contact and SP usage decreased risk of infectionThis finding suggests that intervention strategies focusingon combating malaria and schistosomiasis respectively byincreasing the uptake of IPTp-SPdoses and less water contactamong pregnant women living in Munyenge represents themost appropriate prevention of coinfection with consequentincrease in Hb levels
This study had one limitation We did not investigate theprevalence of HIV infection among the study participants Ithas been shown that coinfections with helminths andmalariacause considerable morbidity in the host particularly in thepresence of HIV infection [60]
To conclude the study has indicated that S haematobiumand P falciparum infections are common among pregnantwomen living in Munyenge and their coinfection is influ-enced by high frequencies of these parasites in the same pop-ulationThe study also revealed that younger age and bathingand domestic contact with stream are independently associ-ated with prevalence of S haematobium infection while noIPTp-SP was associated with P falciparum infection Streamusage increased risk of coinfection while less water contactand SP usage decreased its risk The fact that light S haema-tobium infection was less common in P falciparum infectedwomen suggests that Plasmodium falciparum parasitaemiamay be associatedwith intensity of urogenital schistosomiasisin coinfected individuals Anaemia is a severe public healthproblem in pregnancy in Munyenge and coinfection withS haematobium and P falciparum exacerbates anaemiaLess water contact frequency and increase uptake of IPTp-SPdoses will significantly reduce risk of coinfection andconsequently anaemia severity in pregnancy in this setting
Abbreviations
IPTp-SP Intermittent preventive treatment in pregnancy(IPTp) with sulfadoxine-pyrimethamine (SP)
ITN Insecticide treated bed netsHIV Human immunodeficiency virusANC Antenatal care
Competing Interests
The authors declare that they do not have any competinginterests
Authorsrsquo Contributions
Judith K Anchang-Kimbi conceived and designed the studyanalyzed the data and wrote the manuscript Dillys MansohElad participated in the design of the study performedthe experiments and made inputs in manuscript write-upGemain Taiwe Sotoing and Eric Akum Achidi supervisedreviewed and provided inputs to the manuscript All authorsread and approved the final manuscript
Acknowledgments
The authors are grateful to all the pregnant women whogave their consent to participate in the study Special thanks
are due to the chief medical officer nurses and laboratorytechnician of the Munyenge Health Centre for their cooper-ation and contribution This study received financial supportfrom the Ministry of Higher Education University ResearchModernisation grant given to authors Judith K Anchang-Kimbi and Eric Akum Achidi
References
[1] T N Petney and R H Andrews ldquoMultiparasite communitiesin animals and humans frequency structure and pathogenicsignificancerdquo International Journal for Parasitology vol 28 no3 pp 377ndash393 1998
[2] F E G Cox ldquoConcomitant infections parasites and immuneresponsesrdquo Parasitology vol 122 supplement 1 pp S23ndashS382001
[3] M Nacher P Singhasivanon S Yimsamran et al ldquoIntestinalhelminth infections are associated with increased incidenceof Plasmodium falciparum malaria in Thailandrdquo Journal ofParasitology vol 88 no 1 pp 55ndash58 2002
[4] J-Y Le Hesran J Akiana E H M Ndiaye M Dia P Senghorand L Konate ldquoSevere malaria attack is associated with highprevalence of Ascaris lumbricoides infection among childrenin rural Senegalrdquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 98 no 7 pp 397ndash399 2004
[5] M Nacher F Gay P Singhasivanon et al ldquoAscaris lumbricoidesinfection is associated with protection from cerebral malariardquoParasite Immunology vol 22 no 3 pp 107ndash113 2000
[6] V Briand L Watier J-Y Le Hesran A Garcia and M CotldquoCoinfection with Plasmodium falciparum and Schistosomahaematobium protective effect of schistosomiasis on malariain Senegalese childrenrdquo American Journal of Tropical Medicineand Hygiene vol 72 no 6 pp 702ndash707 2005
[7] N Oslash Christensen P Furu J Kurtzhals and A OdaiboldquoHeterologous synergistic interactions in concurrent experi-mental infection in the mouse with Schistosoma mansoniEchinostoma revolution Plasmodium yoelii Babesia microtiand Trypanosoma bruceirdquo Parasitology Research vol 74 no 6pp 544ndash551 1988
[8] G Raso A Luginbuhl C A Adjoua et al ldquoMultiple parasiteinfections and their relationship to self-reported morbidity ina community of rural Cote drsquoIvoirerdquo International Journal ofEpidemiology vol 33 no 5 pp 1092ndash1102 2004
[9] S Brooker W Akhwale R Pullan et al ldquoEpidemiology ofPlasmodium-helminth co-infection in Africa populations atrisk potential impact on anemia and prospects for combiningcontrolrdquo American Journal of Tropical Medicine and Hygienevol 77 no 6 pp 88ndash98 2007
[10] C E Shulman and E K Dorman ldquoReducing childhood mor-tality in poor countries importance and prevention of malariain pregnancyrdquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 97 no 1 pp 30ndash35 2003
[11] WorldHealthOrganisation andAfrica Regional OfficeMalariaPrevention and Control during Pregnancy in the African RegionWHOAFRO Brazzaville Congo 2004
[12] D Engels L Chitsulo A Montresor and L Savioli ldquoTheglobal epidemiological situation of schistosomiasis and newapproaches to control and researchrdquo Acta Tropica vol 82 no2 pp 139ndash146 2002
[13] P J Hotez and A Kamath ldquoNeglected tropical diseases in sub-Saharan Africa review of their prevalence distribution and
[14] M J Van Der Werf S J De Vlas S Brooker et al ldquoQuantifica-tion of clinical morbidity associated with schistosome infectionin sub-Saharan Africardquo Acta Tropica vol 86 no 2-3 pp 125ndash139 2003
[15] M N Nour ldquoSchistosomias health effect on womenrdquo Reviewsin Obstetrics amp Gynecology vol 3 no 1 pp 28ndash32 2010
[16] J F Friedman P Mital H K Kanzaria G R Olds and J DKurtis ldquoSchistosomiasis and pregnancyrdquo Trends in Parasitologyvol 23 no 4 pp 159ndash164 2007
[17] httpwwwwhointschistosomiasisstrategyen[18] H N Ntonifor and J A Ajayi ldquoWater contact and Schistosoma
haematobium infection A case study of some communitiesin Toro Local Government council Area (TLGCA) of BauchiStaterdquoNigeria Journal of Natural and Applied Sciences vol 1 no1 pp 54ndash59 2005
[19] P Saotoing T Vroumsia A M Njan F N Tchuenguem andJ Messi ldquoEpidemiological survey of schistosomiasis due toSchistosoma haematobium in some primary schools in thetown of Maroua far north region Cameroonrdquo InternationalJournal of Tropical Medicine vol 6 no 2 pp 19ndash24 2011
[20] L A Tchuem Tchuente R I K Ngassam L Sumo et al ldquoMap-ping of schistosomiasis and soil- transmitted helminthiasis inthe regions of centre east and west cameroonrdquo PLoS NeglectedTropical Diseases vol 6 no 3 p e1553 2012
[21] L A Tchuem Tchuente N C Dongmo P Ngassam et alldquoMapping of schistosomiasis and soil- transmitted helminthi-asis in the regions of Littoral North-West South and South-West Cameroon and recommendations for treatmentrdquo BMCInfectious Disease vol 13 article 602 2013
[22] K J N Ndamukong M A Ayuk J S Dinga T N Akenji VA Ndiforchu and V P K Titanji ldquoPrevalence and intensity ofurinary schistosomiasis in primary school children of the KottoBarombi health area Cameroonrdquo East African Medical Journalvol 78 no 6 pp 287ndash289 2001
[23] H N Ntonifor G N Mbunkur and N W Ndaleh ldquoEpidemi-ological survey of urinary schistosomiasis in some primaryschools in a new focus behind Mount Cameroon (Munyenge)South West Region Cameroonrdquo East African Medical Journalvol 89 no 3 pp 82ndash88 2012
[24] J F Friedman H K Kanzaria and S T McGarvey ldquoHumanschistosomiasis and anemia the relationship and potentialmechanismsrdquo Trends in Parasitology vol 21 no 8 pp 386ndash3922005
[25] A Ajanga N J S Lwambo L Blair U Nyandindi A Fenwickand S Brooker ldquoSchistosoma mansoni in pregnancy andassociations with anaemia in northwest Tanzaniardquo Transactionsof the Royal Society of Tropical Medicine and Hygiene vol 100no 1 pp 59ndash63 2006
[26] G Helling-Giese E F Kjetland S G Gundersen et al ldquoSchis-tosomiasis in women manifestations in the upper reproductivetractrdquo Acta Tropica vol 62 no 4 pp 225ndash238 1996
[27] R W Steketee B L Nahlen M E Parise and C MenendezldquoTheburden ofmalaria in pregnancy inmalaria-endemic areasrdquoAmerican Journal of Tropical Medicine and Hygiene vol 64 no1-2 pp 28ndash35 2001
[28] V V Laxman B Adamson and T Mahmood ldquoRecurrentectopic pregnancy due to Schistosoma hematobiumrdquo Journal ofObstetrics and Gynaecology vol 28 no 4 pp 461ndash462 2008
[29] S Bahrami H Alatassi S P Slone and D M OrsquoConnorldquoTubal gestation and schistosomiasis a case reportrdquo Journal ofReproductiveMedicine for theObstetrician andGynecologist vol51 no 7 pp 595ndash598 2006
[30] P S Mbabazi O Andan D W Fitzgerald L Chitsulo DEngels and J A Downs ldquoExamining the relationship betweenurogenital schistosomiasis and HIV infectionrdquo PLoS NeglectedTropical Diseases vol 5 no 12 Article ID e1396 2011
[31] R Tweyongyere P A Mawa N O Emojong et al ldquoEffectof praziquantel treatment of Schistosomamansoni during preg-nancy on intensity of infection and antibody responses to schis-tosome antigens results of a randomised placebo-controlledtrialrdquo BMC Infectious Diseases vol 9 article 32 2009
[32] H N Ntonifor A E Green M O S Bopda et al ldquoEpi-demiology of urinary schistosomiasis and soil transmittedhelminthiasis in a recently established focus behind MountCameroonrdquo International Journal of Current Microbiology andApplied Sciences vol 4 no 3 pp 1056ndash1066 2015
[33] S Wanji A J Kengne-Ouafo E E Joan Eyong et al ldquoGeneticdiversity of Plasmodium falciparummerozoite surface protein-1 block 2 in sites of contrasting altitudes and malaria endemic-ities in the Mount Cameroon Regionrdquo American Journal ofTropical Medicine and Hygiene vol 86 no 5 pp 764ndash774 2012
[34] J K Anchang-Kimbi E A Achidi B Nkegoum E Sverremark-Ekstrom and M Troye-Blomberg ldquoDiagnostic comparisonof malaria infection in peripheral blood placental blood andplacental biopsies in Cameroonian parturient womenrdquoMalariaJournal vol 8 no 1 article 126 2009
[35] F J Bryan The Design and Analysis of Research Studies Uni-versity ofOtago Dunedin NewZealand CambridgeUniversityPress Cambridge UK 1992
[36] World Health Organisation Haemoglobin Concentrations forthe Diagnosis of Anaemia and Assessment of Severity Vitaminand mineral Nutrition Information System WHO GenevaSwitzerland 2011
[37] M CheesbroughDistrict Laboratory Practice in Tropical Coun-tries Cambridge University Press Cambridge UK 2006
[39] N O Christensen G Gotsche and F Frandsen ParasitologicalTechniques for Use in Routine Laboratory Maintainance of Schis-tosomes and Used in Studies on the Epidemiology of Human andBovine Schistosomiasis Danish Bilhaziasis Laboratory Manual1984
[40] World Health OrganizationmdashTropical Disease Research TDRstrategic direction Schistosomiasis WHO-TDR 2002
[41] World Health OrganizationGuidelines for the Evaluation of SoilTransmitted Helminthiasis and Schistosomiasis at CommunityLevel A Guide for Managers of Control Programme WHOGeneva Switzerland 1993
[42] J E Eyo G C Onyishi and F C Okafor ldquoUrinary schisto-somiasis among pregnant women in some endemic tropicalsemi-urban communities of Anambra State Nigeriardquo TropicalBiomedicine vol 29 no 4 pp 575ndash579 2012
[43] O T Salawu and A B Odaibo ldquoSchistosomiasis among preg-nant women in rural communities in Nigeriardquo InternationalJournal of Gynecology andObstetrics vol 122 no 1 pp 1ndash4 2013
[44] K R Tan B L Katalenich K E Mace et al ldquoEfficacyof sulphadoxine-pyrimethamine for intermittent preventivetreatment of malaria in pregnancy Mansa Zambiardquo MalariaJournal vol 13 no 1 article 227 2014
12 Journal of Parasitology Research
[45] J Bethony J T Williams H Kloos et al ldquoExposure toSchistosoma mansoni infection in a rural area in Brazil IIhousehold risk factorsrdquo Tropical Medicine and InternationalHealth vol 6 no 2 pp 136ndash145 2001
[46] J C Sousa-Figueiredo D Gamboa J M Pedro et al ldquoEpi-demiology of malaria schistosomiasis geohelminths anemiaand malnutrition in the context of a demographic surveillancesystem in northern Angolardquo PLoS ONE vol 7 no 4 Article IDe33189 2012
[47] F Anto V Asoala M Adjuik et al ldquoWater contact activitiesand prevalence of schistosomiasis infection among school-agechildren in communities along an irrigation scheme in RuralNorthern Ghanardquo Journal of Bacteriology amp Parasitology vol 4article 177 2013
[48] L-A Tchuem Tchuente J M Behnke F S Gilbert V RSouthgate and J Vercruysse ldquoPolyparasitism with Schistosomahaematobium and soil-transmitted helminth infections amongschool children in Loum Cameroonrdquo Tropical Medicine andInternational Health vol 8 no 11 pp 975ndash986 2003
[49] J-F Etard M Audibert and A Dabo ldquoAge-acquired resistanceand predisposition to reinfection with Schistosoma haemato-bium after treatment with praziquantel in Malirdquo The AmericanJournal of TropicalMedicine andHygiene vol 52 no 6 pp 549ndash558 1995
[50] A Gazzinelli G Velasquez-Melendez S B Crawford P TLoVerde R Correa-Oliveira and H Kloos ldquoSocioeconomicdeterminants of schistosomiasis in a poor rural area in BrazilrdquoActa Tropica vol 99 no 2-3 pp 260ndash271 2006
[51] A P Kapito-Tembo V Mwapasa S R Meshnick et al ldquoPreva-lence distribution and risk factors for Schistosoma hematobiuminfection among school children in Blantyre Malawirdquo PLoSNeglected Tropical Diseases vol 3 no 1 article e361 2009
[52] N J Yatich J Yi T Agbenyega et al ldquoMalaria and intestinalhelminth co-infection among pregnant women in Ghanaprevalence and risk factorsrdquo The American Journal of TropicalMedicine and Hygiene vol 80 no 6 pp 896ndash901 2009
[53] M Nacher ldquoInteractions between worms and malaria goodworms or bad wormsrdquoMalaria Journal vol 10 article no 2592011
[54] A A Adegnika and P G Kremsner ldquoEpidemiology of malariaand helminth interaction a review from 2001 to 2011rdquo CurrentOpinion in HIV and AIDS vol 7 no 3 pp 221ndash224 2012
[55] S Getie Y Wondimeneh G Getnet et al ldquoPrevalence andclinical correlates of Schistosoma mansoni co-infection amongmalaria infected patients Northwest Ethiopiardquo BMC ResearchNotes vol 8 no 1 article no 480 2015
[56] E Okafor and A Elenwo ldquoHaemoglobin status of children withmixed infection ofmalaria and urinary schistosomiasis inOdauCommunity Rivers state Nigeriardquo Journal of Agriculture andSocial Research vol 7 no 1 pp 56ndash62 2008
[57] M A McDevitt J Xie V Gordeuk and R Bucala ldquoThe anemiaof malaria infection role of inflammatory cytokinesrdquo CurrentHematology Reports vol 3 no 2 pp 97ndash106 2004
[58] J G Shaw and J F Friedman ldquoIron deficiency anemia focus oninfectious diseases in lesser developed countriesrdquo Anemia vol2011 Article ID 260380 10 pages 2011
[59] H K Green J C Sousa-Figueiredo M-G Basanez et alldquoAnaemia in Ugandan preschool-aged children the relativecontribution of intestinal parasites and malariardquo Parasitologyvol 138 no 12 pp 1534ndash1545 2011
[60] E Ivan N J Crowther E Mutimura L O Osuwat S Janssenand M P Grobusch ldquoHelminthic infections rates and malaria
in HIV-infected pregnant women on anti-retroviral therapy inRwandardquo PLoS Neglected Tropical Diseases vol 7 no 8 ArticleID e2380 2013
1205942 119875 value 1329 lt00011205942 Pearson Chi-square test OR odd ratioAdjusted OR using multivariate regression analysis
frequency and the implication of voiding their bladder inwater bodies is paramount These behavioural changes willsignificantly reduce the risk of S haematobium infectionamong pregnant women and contamination of water sourcesin this setting Ultimately provision of portable water andimproved sanitation system will play a major role in decreas-ing disease transmission and incidence
Age as observed in most schistosomiasis surveys was amajor determinant of schistosomes infection among preg-nant women in our study area The highest prevalence val-ues of urogenital schistosomiasis were recorded in youngerwomen (le25 years) Individuals within le20 age group werefound to be at a greater risk of S haematobium infection withprevalence of 554 This is in agreement with trends estab-lished in schistosomiasis surveys carried out in Cameroon
[32 48] and other parts of Africa [42 43] Alternativelythe decrease risk of infection observed in older age groups(gt25 years) conformed to earlier reports [32 42] Studieshave reported that age-acquired immunity to reinfection andchanges in water contact patterns contribute to the decliningtrend in prevalence with increasing age [49] Older womenare less likely to be engaged in water contact behaviourscompared to younger women Age dependent immunity toS haematobium has been shown to affect mean egg outputof infected persons [49] Socioeconomic status of the womenwas not an independent factor associated with S haema-tobium prevalence in this high-risk community Similarlyreports from other rural settings endemic for schistosomi-asis failed to identify any socioeconomic variables that arestrongly associated with schistosomiasis prevalence [50 51]
8 Journal of Parasitology Research
Table 4 Factors associated with mean (plusmnSD) haemoglobin levels among pregnant women in Munyenge Health Area
Factors Category Mean (plusmnSD) Hblevels Test-value Unadjusted
lowastAnalysis of variance test (ANOVA)$Studentrsquos 119905-testampAdjusted 119875 values using multilinear regression analysisNA not applicable variables with 119875 gt 02 in bivariate analysis were not included in regression analysis
Table 5 Association between S haematobium intensity P falciparum infection and mean (plusmnSD) haemoglobin levels and anaemia severity
lowastSignificance level 119865 = 1240 119875 lt 0001lowastAnalysis of variance test (ANOVA)ampPearson Chi-Square test
The absence of association between socioeconomic variablesand infection prevalencemay be attributed to general povertyand uniformity in high exposure risk in the population [50]
The overall prevalence of coinfection with S haema-tobium and P falciparum infection was 152 suggestingcoendemicity of both infections in the study area SimilarlyYatich et al [52] reported a helminth andmalaria coinfectionprevalence of 166 among pregnant women in Ghana Theimpact of helminth infections on malaria parasitaemia and
disease during coinfection is an established phenomenonalthough much is still unknown and contradictions persist[53 54]We observed that light S haematobium infectionwasless common (aOR= 04) among pregnant women coinfectedwith P falciparum suggesting a negative interaction betweenboth parasites [4] In accordance with findings of Getie etal [55] schistosomiasis coinfection could affect Plasmodiumparasitemia and vice versa depending on the intensity of theova in coinfected persons Nonetheless a further study is
Journal of Parasitology Research 9
Table 6 Risk factors associated with anaemia among pregnant women in Munyenge Health Area
Factors Category Anaemia prevalence Adjusted OR (95 CI) 119875 value
Adjusted OR using multivariate regression analysisNA not applicable variables with 119875 gt 02 in bivariate analysis were not included in multivariate analysis
needed to explore the underlying mechanisms of interactionbetween malaria parasitaemia and S haematobium
Schistosomiasis causes long term morbidity such asanaemia Our study showed that the magnitude of S haema-tobium egg counts is significantly related to haemoglobinconcentration confirming that urogenital schistosomiasiscontributes to anaemia [24 25] In this study anaemiawas more pronounced in women with heavy infectionintensity than in those with light infection Coinfection ofhelminth infections and P falciparum increases anaemiaseverity [8 9] Coinfection among pregnant women lowersHb concentration compared with single infection This is inagreement with findings of Okafor and Elenwo [56] Moreso coinfected women with heavy intensity S haematobiuminfection had the lowest mean Hb levels (66 gdL) andthis subpopulation of women contributed to about 72of all severe anaemic cases The combined presence and
interaction of S haematobium and P falciparum infectionsis partly responsible for the low haemoglobin concentrationin women with concurrent infectionMalaria causes anaemiaby destruction and removal of parasitized red blood cellsand shortening of the life span of nonparasitized red cellsas well as decreasing the rate of erythrocyte production inbone marrow [57]Themechanism by which schistosomiasiscauses anaemia is not fully understood but it is suggested thathelminth infections could contribute to increase in the preva-lence of inflammatory syndromes impairing erythropoiesisand interfering with mobilization of reticuloendothelial ironstorages and shortening erythrocyte survival [58] Similar toprevious reports of a study in Uganda [59] malaria parasiteinfection was an independent factor associated with increaseanaemia risk
The risk of coinfection was associated with streamusage (bathing and domestic contact with stream) while
10 Journal of Parasitology Research
less water contact and SP usage decreased risk of infectionThis finding suggests that intervention strategies focusingon combating malaria and schistosomiasis respectively byincreasing the uptake of IPTp-SPdoses and less water contactamong pregnant women living in Munyenge represents themost appropriate prevention of coinfection with consequentincrease in Hb levels
This study had one limitation We did not investigate theprevalence of HIV infection among the study participants Ithas been shown that coinfections with helminths andmalariacause considerable morbidity in the host particularly in thepresence of HIV infection [60]
To conclude the study has indicated that S haematobiumand P falciparum infections are common among pregnantwomen living in Munyenge and their coinfection is influ-enced by high frequencies of these parasites in the same pop-ulationThe study also revealed that younger age and bathingand domestic contact with stream are independently associ-ated with prevalence of S haematobium infection while noIPTp-SP was associated with P falciparum infection Streamusage increased risk of coinfection while less water contactand SP usage decreased its risk The fact that light S haema-tobium infection was less common in P falciparum infectedwomen suggests that Plasmodium falciparum parasitaemiamay be associatedwith intensity of urogenital schistosomiasisin coinfected individuals Anaemia is a severe public healthproblem in pregnancy in Munyenge and coinfection withS haematobium and P falciparum exacerbates anaemiaLess water contact frequency and increase uptake of IPTp-SPdoses will significantly reduce risk of coinfection andconsequently anaemia severity in pregnancy in this setting
Abbreviations
IPTp-SP Intermittent preventive treatment in pregnancy(IPTp) with sulfadoxine-pyrimethamine (SP)
ITN Insecticide treated bed netsHIV Human immunodeficiency virusANC Antenatal care
Competing Interests
The authors declare that they do not have any competinginterests
Authorsrsquo Contributions
Judith K Anchang-Kimbi conceived and designed the studyanalyzed the data and wrote the manuscript Dillys MansohElad participated in the design of the study performedthe experiments and made inputs in manuscript write-upGemain Taiwe Sotoing and Eric Akum Achidi supervisedreviewed and provided inputs to the manuscript All authorsread and approved the final manuscript
Acknowledgments
The authors are grateful to all the pregnant women whogave their consent to participate in the study Special thanks
are due to the chief medical officer nurses and laboratorytechnician of the Munyenge Health Centre for their cooper-ation and contribution This study received financial supportfrom the Ministry of Higher Education University ResearchModernisation grant given to authors Judith K Anchang-Kimbi and Eric Akum Achidi
References
[1] T N Petney and R H Andrews ldquoMultiparasite communitiesin animals and humans frequency structure and pathogenicsignificancerdquo International Journal for Parasitology vol 28 no3 pp 377ndash393 1998
[2] F E G Cox ldquoConcomitant infections parasites and immuneresponsesrdquo Parasitology vol 122 supplement 1 pp S23ndashS382001
[3] M Nacher P Singhasivanon S Yimsamran et al ldquoIntestinalhelminth infections are associated with increased incidenceof Plasmodium falciparum malaria in Thailandrdquo Journal ofParasitology vol 88 no 1 pp 55ndash58 2002
[4] J-Y Le Hesran J Akiana E H M Ndiaye M Dia P Senghorand L Konate ldquoSevere malaria attack is associated with highprevalence of Ascaris lumbricoides infection among childrenin rural Senegalrdquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 98 no 7 pp 397ndash399 2004
[5] M Nacher F Gay P Singhasivanon et al ldquoAscaris lumbricoidesinfection is associated with protection from cerebral malariardquoParasite Immunology vol 22 no 3 pp 107ndash113 2000
[6] V Briand L Watier J-Y Le Hesran A Garcia and M CotldquoCoinfection with Plasmodium falciparum and Schistosomahaematobium protective effect of schistosomiasis on malariain Senegalese childrenrdquo American Journal of Tropical Medicineand Hygiene vol 72 no 6 pp 702ndash707 2005
[7] N Oslash Christensen P Furu J Kurtzhals and A OdaiboldquoHeterologous synergistic interactions in concurrent experi-mental infection in the mouse with Schistosoma mansoniEchinostoma revolution Plasmodium yoelii Babesia microtiand Trypanosoma bruceirdquo Parasitology Research vol 74 no 6pp 544ndash551 1988
[8] G Raso A Luginbuhl C A Adjoua et al ldquoMultiple parasiteinfections and their relationship to self-reported morbidity ina community of rural Cote drsquoIvoirerdquo International Journal ofEpidemiology vol 33 no 5 pp 1092ndash1102 2004
[9] S Brooker W Akhwale R Pullan et al ldquoEpidemiology ofPlasmodium-helminth co-infection in Africa populations atrisk potential impact on anemia and prospects for combiningcontrolrdquo American Journal of Tropical Medicine and Hygienevol 77 no 6 pp 88ndash98 2007
[10] C E Shulman and E K Dorman ldquoReducing childhood mor-tality in poor countries importance and prevention of malariain pregnancyrdquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 97 no 1 pp 30ndash35 2003
[11] WorldHealthOrganisation andAfrica Regional OfficeMalariaPrevention and Control during Pregnancy in the African RegionWHOAFRO Brazzaville Congo 2004
[12] D Engels L Chitsulo A Montresor and L Savioli ldquoTheglobal epidemiological situation of schistosomiasis and newapproaches to control and researchrdquo Acta Tropica vol 82 no2 pp 139ndash146 2002
[13] P J Hotez and A Kamath ldquoNeglected tropical diseases in sub-Saharan Africa review of their prevalence distribution and
[14] M J Van Der Werf S J De Vlas S Brooker et al ldquoQuantifica-tion of clinical morbidity associated with schistosome infectionin sub-Saharan Africardquo Acta Tropica vol 86 no 2-3 pp 125ndash139 2003
[15] M N Nour ldquoSchistosomias health effect on womenrdquo Reviewsin Obstetrics amp Gynecology vol 3 no 1 pp 28ndash32 2010
[16] J F Friedman P Mital H K Kanzaria G R Olds and J DKurtis ldquoSchistosomiasis and pregnancyrdquo Trends in Parasitologyvol 23 no 4 pp 159ndash164 2007
[17] httpwwwwhointschistosomiasisstrategyen[18] H N Ntonifor and J A Ajayi ldquoWater contact and Schistosoma
haematobium infection A case study of some communitiesin Toro Local Government council Area (TLGCA) of BauchiStaterdquoNigeria Journal of Natural and Applied Sciences vol 1 no1 pp 54ndash59 2005
[19] P Saotoing T Vroumsia A M Njan F N Tchuenguem andJ Messi ldquoEpidemiological survey of schistosomiasis due toSchistosoma haematobium in some primary schools in thetown of Maroua far north region Cameroonrdquo InternationalJournal of Tropical Medicine vol 6 no 2 pp 19ndash24 2011
[20] L A Tchuem Tchuente R I K Ngassam L Sumo et al ldquoMap-ping of schistosomiasis and soil- transmitted helminthiasis inthe regions of centre east and west cameroonrdquo PLoS NeglectedTropical Diseases vol 6 no 3 p e1553 2012
[21] L A Tchuem Tchuente N C Dongmo P Ngassam et alldquoMapping of schistosomiasis and soil- transmitted helminthi-asis in the regions of Littoral North-West South and South-West Cameroon and recommendations for treatmentrdquo BMCInfectious Disease vol 13 article 602 2013
[22] K J N Ndamukong M A Ayuk J S Dinga T N Akenji VA Ndiforchu and V P K Titanji ldquoPrevalence and intensity ofurinary schistosomiasis in primary school children of the KottoBarombi health area Cameroonrdquo East African Medical Journalvol 78 no 6 pp 287ndash289 2001
[23] H N Ntonifor G N Mbunkur and N W Ndaleh ldquoEpidemi-ological survey of urinary schistosomiasis in some primaryschools in a new focus behind Mount Cameroon (Munyenge)South West Region Cameroonrdquo East African Medical Journalvol 89 no 3 pp 82ndash88 2012
[24] J F Friedman H K Kanzaria and S T McGarvey ldquoHumanschistosomiasis and anemia the relationship and potentialmechanismsrdquo Trends in Parasitology vol 21 no 8 pp 386ndash3922005
[25] A Ajanga N J S Lwambo L Blair U Nyandindi A Fenwickand S Brooker ldquoSchistosoma mansoni in pregnancy andassociations with anaemia in northwest Tanzaniardquo Transactionsof the Royal Society of Tropical Medicine and Hygiene vol 100no 1 pp 59ndash63 2006
[26] G Helling-Giese E F Kjetland S G Gundersen et al ldquoSchis-tosomiasis in women manifestations in the upper reproductivetractrdquo Acta Tropica vol 62 no 4 pp 225ndash238 1996
[27] R W Steketee B L Nahlen M E Parise and C MenendezldquoTheburden ofmalaria in pregnancy inmalaria-endemic areasrdquoAmerican Journal of Tropical Medicine and Hygiene vol 64 no1-2 pp 28ndash35 2001
[28] V V Laxman B Adamson and T Mahmood ldquoRecurrentectopic pregnancy due to Schistosoma hematobiumrdquo Journal ofObstetrics and Gynaecology vol 28 no 4 pp 461ndash462 2008
[29] S Bahrami H Alatassi S P Slone and D M OrsquoConnorldquoTubal gestation and schistosomiasis a case reportrdquo Journal ofReproductiveMedicine for theObstetrician andGynecologist vol51 no 7 pp 595ndash598 2006
[30] P S Mbabazi O Andan D W Fitzgerald L Chitsulo DEngels and J A Downs ldquoExamining the relationship betweenurogenital schistosomiasis and HIV infectionrdquo PLoS NeglectedTropical Diseases vol 5 no 12 Article ID e1396 2011
[31] R Tweyongyere P A Mawa N O Emojong et al ldquoEffectof praziquantel treatment of Schistosomamansoni during preg-nancy on intensity of infection and antibody responses to schis-tosome antigens results of a randomised placebo-controlledtrialrdquo BMC Infectious Diseases vol 9 article 32 2009
[32] H N Ntonifor A E Green M O S Bopda et al ldquoEpi-demiology of urinary schistosomiasis and soil transmittedhelminthiasis in a recently established focus behind MountCameroonrdquo International Journal of Current Microbiology andApplied Sciences vol 4 no 3 pp 1056ndash1066 2015
[33] S Wanji A J Kengne-Ouafo E E Joan Eyong et al ldquoGeneticdiversity of Plasmodium falciparummerozoite surface protein-1 block 2 in sites of contrasting altitudes and malaria endemic-ities in the Mount Cameroon Regionrdquo American Journal ofTropical Medicine and Hygiene vol 86 no 5 pp 764ndash774 2012
[34] J K Anchang-Kimbi E A Achidi B Nkegoum E Sverremark-Ekstrom and M Troye-Blomberg ldquoDiagnostic comparisonof malaria infection in peripheral blood placental blood andplacental biopsies in Cameroonian parturient womenrdquoMalariaJournal vol 8 no 1 article 126 2009
[35] F J Bryan The Design and Analysis of Research Studies Uni-versity ofOtago Dunedin NewZealand CambridgeUniversityPress Cambridge UK 1992
[36] World Health Organisation Haemoglobin Concentrations forthe Diagnosis of Anaemia and Assessment of Severity Vitaminand mineral Nutrition Information System WHO GenevaSwitzerland 2011
[37] M CheesbroughDistrict Laboratory Practice in Tropical Coun-tries Cambridge University Press Cambridge UK 2006
[39] N O Christensen G Gotsche and F Frandsen ParasitologicalTechniques for Use in Routine Laboratory Maintainance of Schis-tosomes and Used in Studies on the Epidemiology of Human andBovine Schistosomiasis Danish Bilhaziasis Laboratory Manual1984
[40] World Health OrganizationmdashTropical Disease Research TDRstrategic direction Schistosomiasis WHO-TDR 2002
[41] World Health OrganizationGuidelines for the Evaluation of SoilTransmitted Helminthiasis and Schistosomiasis at CommunityLevel A Guide for Managers of Control Programme WHOGeneva Switzerland 1993
[42] J E Eyo G C Onyishi and F C Okafor ldquoUrinary schisto-somiasis among pregnant women in some endemic tropicalsemi-urban communities of Anambra State Nigeriardquo TropicalBiomedicine vol 29 no 4 pp 575ndash579 2012
[43] O T Salawu and A B Odaibo ldquoSchistosomiasis among preg-nant women in rural communities in Nigeriardquo InternationalJournal of Gynecology andObstetrics vol 122 no 1 pp 1ndash4 2013
[44] K R Tan B L Katalenich K E Mace et al ldquoEfficacyof sulphadoxine-pyrimethamine for intermittent preventivetreatment of malaria in pregnancy Mansa Zambiardquo MalariaJournal vol 13 no 1 article 227 2014
12 Journal of Parasitology Research
[45] J Bethony J T Williams H Kloos et al ldquoExposure toSchistosoma mansoni infection in a rural area in Brazil IIhousehold risk factorsrdquo Tropical Medicine and InternationalHealth vol 6 no 2 pp 136ndash145 2001
[46] J C Sousa-Figueiredo D Gamboa J M Pedro et al ldquoEpi-demiology of malaria schistosomiasis geohelminths anemiaand malnutrition in the context of a demographic surveillancesystem in northern Angolardquo PLoS ONE vol 7 no 4 Article IDe33189 2012
[47] F Anto V Asoala M Adjuik et al ldquoWater contact activitiesand prevalence of schistosomiasis infection among school-agechildren in communities along an irrigation scheme in RuralNorthern Ghanardquo Journal of Bacteriology amp Parasitology vol 4article 177 2013
[48] L-A Tchuem Tchuente J M Behnke F S Gilbert V RSouthgate and J Vercruysse ldquoPolyparasitism with Schistosomahaematobium and soil-transmitted helminth infections amongschool children in Loum Cameroonrdquo Tropical Medicine andInternational Health vol 8 no 11 pp 975ndash986 2003
[49] J-F Etard M Audibert and A Dabo ldquoAge-acquired resistanceand predisposition to reinfection with Schistosoma haemato-bium after treatment with praziquantel in Malirdquo The AmericanJournal of TropicalMedicine andHygiene vol 52 no 6 pp 549ndash558 1995
[50] A Gazzinelli G Velasquez-Melendez S B Crawford P TLoVerde R Correa-Oliveira and H Kloos ldquoSocioeconomicdeterminants of schistosomiasis in a poor rural area in BrazilrdquoActa Tropica vol 99 no 2-3 pp 260ndash271 2006
[51] A P Kapito-Tembo V Mwapasa S R Meshnick et al ldquoPreva-lence distribution and risk factors for Schistosoma hematobiuminfection among school children in Blantyre Malawirdquo PLoSNeglected Tropical Diseases vol 3 no 1 article e361 2009
[52] N J Yatich J Yi T Agbenyega et al ldquoMalaria and intestinalhelminth co-infection among pregnant women in Ghanaprevalence and risk factorsrdquo The American Journal of TropicalMedicine and Hygiene vol 80 no 6 pp 896ndash901 2009
[53] M Nacher ldquoInteractions between worms and malaria goodworms or bad wormsrdquoMalaria Journal vol 10 article no 2592011
[54] A A Adegnika and P G Kremsner ldquoEpidemiology of malariaand helminth interaction a review from 2001 to 2011rdquo CurrentOpinion in HIV and AIDS vol 7 no 3 pp 221ndash224 2012
[55] S Getie Y Wondimeneh G Getnet et al ldquoPrevalence andclinical correlates of Schistosoma mansoni co-infection amongmalaria infected patients Northwest Ethiopiardquo BMC ResearchNotes vol 8 no 1 article no 480 2015
[56] E Okafor and A Elenwo ldquoHaemoglobin status of children withmixed infection ofmalaria and urinary schistosomiasis inOdauCommunity Rivers state Nigeriardquo Journal of Agriculture andSocial Research vol 7 no 1 pp 56ndash62 2008
[57] M A McDevitt J Xie V Gordeuk and R Bucala ldquoThe anemiaof malaria infection role of inflammatory cytokinesrdquo CurrentHematology Reports vol 3 no 2 pp 97ndash106 2004
[58] J G Shaw and J F Friedman ldquoIron deficiency anemia focus oninfectious diseases in lesser developed countriesrdquo Anemia vol2011 Article ID 260380 10 pages 2011
[59] H K Green J C Sousa-Figueiredo M-G Basanez et alldquoAnaemia in Ugandan preschool-aged children the relativecontribution of intestinal parasites and malariardquo Parasitologyvol 138 no 12 pp 1534ndash1545 2011
[60] E Ivan N J Crowther E Mutimura L O Osuwat S Janssenand M P Grobusch ldquoHelminthic infections rates and malaria
in HIV-infected pregnant women on anti-retroviral therapy inRwandardquo PLoS Neglected Tropical Diseases vol 7 no 8 ArticleID e2380 2013
lowastAnalysis of variance test (ANOVA)$Studentrsquos 119905-testampAdjusted 119875 values using multilinear regression analysisNA not applicable variables with 119875 gt 02 in bivariate analysis were not included in regression analysis
Table 5 Association between S haematobium intensity P falciparum infection and mean (plusmnSD) haemoglobin levels and anaemia severity
lowastSignificance level 119865 = 1240 119875 lt 0001lowastAnalysis of variance test (ANOVA)ampPearson Chi-Square test
The absence of association between socioeconomic variablesand infection prevalencemay be attributed to general povertyand uniformity in high exposure risk in the population [50]
The overall prevalence of coinfection with S haema-tobium and P falciparum infection was 152 suggestingcoendemicity of both infections in the study area SimilarlyYatich et al [52] reported a helminth andmalaria coinfectionprevalence of 166 among pregnant women in Ghana Theimpact of helminth infections on malaria parasitaemia and
disease during coinfection is an established phenomenonalthough much is still unknown and contradictions persist[53 54]We observed that light S haematobium infectionwasless common (aOR= 04) among pregnant women coinfectedwith P falciparum suggesting a negative interaction betweenboth parasites [4] In accordance with findings of Getie etal [55] schistosomiasis coinfection could affect Plasmodiumparasitemia and vice versa depending on the intensity of theova in coinfected persons Nonetheless a further study is
Journal of Parasitology Research 9
Table 6 Risk factors associated with anaemia among pregnant women in Munyenge Health Area
Factors Category Anaemia prevalence Adjusted OR (95 CI) 119875 value
Adjusted OR using multivariate regression analysisNA not applicable variables with 119875 gt 02 in bivariate analysis were not included in multivariate analysis
needed to explore the underlying mechanisms of interactionbetween malaria parasitaemia and S haematobium
Schistosomiasis causes long term morbidity such asanaemia Our study showed that the magnitude of S haema-tobium egg counts is significantly related to haemoglobinconcentration confirming that urogenital schistosomiasiscontributes to anaemia [24 25] In this study anaemiawas more pronounced in women with heavy infectionintensity than in those with light infection Coinfection ofhelminth infections and P falciparum increases anaemiaseverity [8 9] Coinfection among pregnant women lowersHb concentration compared with single infection This is inagreement with findings of Okafor and Elenwo [56] Moreso coinfected women with heavy intensity S haematobiuminfection had the lowest mean Hb levels (66 gdL) andthis subpopulation of women contributed to about 72of all severe anaemic cases The combined presence and
interaction of S haematobium and P falciparum infectionsis partly responsible for the low haemoglobin concentrationin women with concurrent infectionMalaria causes anaemiaby destruction and removal of parasitized red blood cellsand shortening of the life span of nonparasitized red cellsas well as decreasing the rate of erythrocyte production inbone marrow [57]Themechanism by which schistosomiasiscauses anaemia is not fully understood but it is suggested thathelminth infections could contribute to increase in the preva-lence of inflammatory syndromes impairing erythropoiesisand interfering with mobilization of reticuloendothelial ironstorages and shortening erythrocyte survival [58] Similar toprevious reports of a study in Uganda [59] malaria parasiteinfection was an independent factor associated with increaseanaemia risk
The risk of coinfection was associated with streamusage (bathing and domestic contact with stream) while
10 Journal of Parasitology Research
less water contact and SP usage decreased risk of infectionThis finding suggests that intervention strategies focusingon combating malaria and schistosomiasis respectively byincreasing the uptake of IPTp-SPdoses and less water contactamong pregnant women living in Munyenge represents themost appropriate prevention of coinfection with consequentincrease in Hb levels
This study had one limitation We did not investigate theprevalence of HIV infection among the study participants Ithas been shown that coinfections with helminths andmalariacause considerable morbidity in the host particularly in thepresence of HIV infection [60]
To conclude the study has indicated that S haematobiumand P falciparum infections are common among pregnantwomen living in Munyenge and their coinfection is influ-enced by high frequencies of these parasites in the same pop-ulationThe study also revealed that younger age and bathingand domestic contact with stream are independently associ-ated with prevalence of S haematobium infection while noIPTp-SP was associated with P falciparum infection Streamusage increased risk of coinfection while less water contactand SP usage decreased its risk The fact that light S haema-tobium infection was less common in P falciparum infectedwomen suggests that Plasmodium falciparum parasitaemiamay be associatedwith intensity of urogenital schistosomiasisin coinfected individuals Anaemia is a severe public healthproblem in pregnancy in Munyenge and coinfection withS haematobium and P falciparum exacerbates anaemiaLess water contact frequency and increase uptake of IPTp-SPdoses will significantly reduce risk of coinfection andconsequently anaemia severity in pregnancy in this setting
Abbreviations
IPTp-SP Intermittent preventive treatment in pregnancy(IPTp) with sulfadoxine-pyrimethamine (SP)
ITN Insecticide treated bed netsHIV Human immunodeficiency virusANC Antenatal care
Competing Interests
The authors declare that they do not have any competinginterests
Authorsrsquo Contributions
Judith K Anchang-Kimbi conceived and designed the studyanalyzed the data and wrote the manuscript Dillys MansohElad participated in the design of the study performedthe experiments and made inputs in manuscript write-upGemain Taiwe Sotoing and Eric Akum Achidi supervisedreviewed and provided inputs to the manuscript All authorsread and approved the final manuscript
Acknowledgments
The authors are grateful to all the pregnant women whogave their consent to participate in the study Special thanks
are due to the chief medical officer nurses and laboratorytechnician of the Munyenge Health Centre for their cooper-ation and contribution This study received financial supportfrom the Ministry of Higher Education University ResearchModernisation grant given to authors Judith K Anchang-Kimbi and Eric Akum Achidi
References
[1] T N Petney and R H Andrews ldquoMultiparasite communitiesin animals and humans frequency structure and pathogenicsignificancerdquo International Journal for Parasitology vol 28 no3 pp 377ndash393 1998
[2] F E G Cox ldquoConcomitant infections parasites and immuneresponsesrdquo Parasitology vol 122 supplement 1 pp S23ndashS382001
[3] M Nacher P Singhasivanon S Yimsamran et al ldquoIntestinalhelminth infections are associated with increased incidenceof Plasmodium falciparum malaria in Thailandrdquo Journal ofParasitology vol 88 no 1 pp 55ndash58 2002
[4] J-Y Le Hesran J Akiana E H M Ndiaye M Dia P Senghorand L Konate ldquoSevere malaria attack is associated with highprevalence of Ascaris lumbricoides infection among childrenin rural Senegalrdquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 98 no 7 pp 397ndash399 2004
[5] M Nacher F Gay P Singhasivanon et al ldquoAscaris lumbricoidesinfection is associated with protection from cerebral malariardquoParasite Immunology vol 22 no 3 pp 107ndash113 2000
[6] V Briand L Watier J-Y Le Hesran A Garcia and M CotldquoCoinfection with Plasmodium falciparum and Schistosomahaematobium protective effect of schistosomiasis on malariain Senegalese childrenrdquo American Journal of Tropical Medicineand Hygiene vol 72 no 6 pp 702ndash707 2005
[7] N Oslash Christensen P Furu J Kurtzhals and A OdaiboldquoHeterologous synergistic interactions in concurrent experi-mental infection in the mouse with Schistosoma mansoniEchinostoma revolution Plasmodium yoelii Babesia microtiand Trypanosoma bruceirdquo Parasitology Research vol 74 no 6pp 544ndash551 1988
[8] G Raso A Luginbuhl C A Adjoua et al ldquoMultiple parasiteinfections and their relationship to self-reported morbidity ina community of rural Cote drsquoIvoirerdquo International Journal ofEpidemiology vol 33 no 5 pp 1092ndash1102 2004
[9] S Brooker W Akhwale R Pullan et al ldquoEpidemiology ofPlasmodium-helminth co-infection in Africa populations atrisk potential impact on anemia and prospects for combiningcontrolrdquo American Journal of Tropical Medicine and Hygienevol 77 no 6 pp 88ndash98 2007
[10] C E Shulman and E K Dorman ldquoReducing childhood mor-tality in poor countries importance and prevention of malariain pregnancyrdquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 97 no 1 pp 30ndash35 2003
[11] WorldHealthOrganisation andAfrica Regional OfficeMalariaPrevention and Control during Pregnancy in the African RegionWHOAFRO Brazzaville Congo 2004
[12] D Engels L Chitsulo A Montresor and L Savioli ldquoTheglobal epidemiological situation of schistosomiasis and newapproaches to control and researchrdquo Acta Tropica vol 82 no2 pp 139ndash146 2002
[13] P J Hotez and A Kamath ldquoNeglected tropical diseases in sub-Saharan Africa review of their prevalence distribution and
[14] M J Van Der Werf S J De Vlas S Brooker et al ldquoQuantifica-tion of clinical morbidity associated with schistosome infectionin sub-Saharan Africardquo Acta Tropica vol 86 no 2-3 pp 125ndash139 2003
[15] M N Nour ldquoSchistosomias health effect on womenrdquo Reviewsin Obstetrics amp Gynecology vol 3 no 1 pp 28ndash32 2010
[16] J F Friedman P Mital H K Kanzaria G R Olds and J DKurtis ldquoSchistosomiasis and pregnancyrdquo Trends in Parasitologyvol 23 no 4 pp 159ndash164 2007
[17] httpwwwwhointschistosomiasisstrategyen[18] H N Ntonifor and J A Ajayi ldquoWater contact and Schistosoma
haematobium infection A case study of some communitiesin Toro Local Government council Area (TLGCA) of BauchiStaterdquoNigeria Journal of Natural and Applied Sciences vol 1 no1 pp 54ndash59 2005
[19] P Saotoing T Vroumsia A M Njan F N Tchuenguem andJ Messi ldquoEpidemiological survey of schistosomiasis due toSchistosoma haematobium in some primary schools in thetown of Maroua far north region Cameroonrdquo InternationalJournal of Tropical Medicine vol 6 no 2 pp 19ndash24 2011
[20] L A Tchuem Tchuente R I K Ngassam L Sumo et al ldquoMap-ping of schistosomiasis and soil- transmitted helminthiasis inthe regions of centre east and west cameroonrdquo PLoS NeglectedTropical Diseases vol 6 no 3 p e1553 2012
[21] L A Tchuem Tchuente N C Dongmo P Ngassam et alldquoMapping of schistosomiasis and soil- transmitted helminthi-asis in the regions of Littoral North-West South and South-West Cameroon and recommendations for treatmentrdquo BMCInfectious Disease vol 13 article 602 2013
[22] K J N Ndamukong M A Ayuk J S Dinga T N Akenji VA Ndiforchu and V P K Titanji ldquoPrevalence and intensity ofurinary schistosomiasis in primary school children of the KottoBarombi health area Cameroonrdquo East African Medical Journalvol 78 no 6 pp 287ndash289 2001
[23] H N Ntonifor G N Mbunkur and N W Ndaleh ldquoEpidemi-ological survey of urinary schistosomiasis in some primaryschools in a new focus behind Mount Cameroon (Munyenge)South West Region Cameroonrdquo East African Medical Journalvol 89 no 3 pp 82ndash88 2012
[24] J F Friedman H K Kanzaria and S T McGarvey ldquoHumanschistosomiasis and anemia the relationship and potentialmechanismsrdquo Trends in Parasitology vol 21 no 8 pp 386ndash3922005
[25] A Ajanga N J S Lwambo L Blair U Nyandindi A Fenwickand S Brooker ldquoSchistosoma mansoni in pregnancy andassociations with anaemia in northwest Tanzaniardquo Transactionsof the Royal Society of Tropical Medicine and Hygiene vol 100no 1 pp 59ndash63 2006
[26] G Helling-Giese E F Kjetland S G Gundersen et al ldquoSchis-tosomiasis in women manifestations in the upper reproductivetractrdquo Acta Tropica vol 62 no 4 pp 225ndash238 1996
[27] R W Steketee B L Nahlen M E Parise and C MenendezldquoTheburden ofmalaria in pregnancy inmalaria-endemic areasrdquoAmerican Journal of Tropical Medicine and Hygiene vol 64 no1-2 pp 28ndash35 2001
[28] V V Laxman B Adamson and T Mahmood ldquoRecurrentectopic pregnancy due to Schistosoma hematobiumrdquo Journal ofObstetrics and Gynaecology vol 28 no 4 pp 461ndash462 2008
[29] S Bahrami H Alatassi S P Slone and D M OrsquoConnorldquoTubal gestation and schistosomiasis a case reportrdquo Journal ofReproductiveMedicine for theObstetrician andGynecologist vol51 no 7 pp 595ndash598 2006
[30] P S Mbabazi O Andan D W Fitzgerald L Chitsulo DEngels and J A Downs ldquoExamining the relationship betweenurogenital schistosomiasis and HIV infectionrdquo PLoS NeglectedTropical Diseases vol 5 no 12 Article ID e1396 2011
[31] R Tweyongyere P A Mawa N O Emojong et al ldquoEffectof praziquantel treatment of Schistosomamansoni during preg-nancy on intensity of infection and antibody responses to schis-tosome antigens results of a randomised placebo-controlledtrialrdquo BMC Infectious Diseases vol 9 article 32 2009
[32] H N Ntonifor A E Green M O S Bopda et al ldquoEpi-demiology of urinary schistosomiasis and soil transmittedhelminthiasis in a recently established focus behind MountCameroonrdquo International Journal of Current Microbiology andApplied Sciences vol 4 no 3 pp 1056ndash1066 2015
[33] S Wanji A J Kengne-Ouafo E E Joan Eyong et al ldquoGeneticdiversity of Plasmodium falciparummerozoite surface protein-1 block 2 in sites of contrasting altitudes and malaria endemic-ities in the Mount Cameroon Regionrdquo American Journal ofTropical Medicine and Hygiene vol 86 no 5 pp 764ndash774 2012
[34] J K Anchang-Kimbi E A Achidi B Nkegoum E Sverremark-Ekstrom and M Troye-Blomberg ldquoDiagnostic comparisonof malaria infection in peripheral blood placental blood andplacental biopsies in Cameroonian parturient womenrdquoMalariaJournal vol 8 no 1 article 126 2009
[35] F J Bryan The Design and Analysis of Research Studies Uni-versity ofOtago Dunedin NewZealand CambridgeUniversityPress Cambridge UK 1992
[36] World Health Organisation Haemoglobin Concentrations forthe Diagnosis of Anaemia and Assessment of Severity Vitaminand mineral Nutrition Information System WHO GenevaSwitzerland 2011
[37] M CheesbroughDistrict Laboratory Practice in Tropical Coun-tries Cambridge University Press Cambridge UK 2006
[39] N O Christensen G Gotsche and F Frandsen ParasitologicalTechniques for Use in Routine Laboratory Maintainance of Schis-tosomes and Used in Studies on the Epidemiology of Human andBovine Schistosomiasis Danish Bilhaziasis Laboratory Manual1984
[40] World Health OrganizationmdashTropical Disease Research TDRstrategic direction Schistosomiasis WHO-TDR 2002
[41] World Health OrganizationGuidelines for the Evaluation of SoilTransmitted Helminthiasis and Schistosomiasis at CommunityLevel A Guide for Managers of Control Programme WHOGeneva Switzerland 1993
[42] J E Eyo G C Onyishi and F C Okafor ldquoUrinary schisto-somiasis among pregnant women in some endemic tropicalsemi-urban communities of Anambra State Nigeriardquo TropicalBiomedicine vol 29 no 4 pp 575ndash579 2012
[43] O T Salawu and A B Odaibo ldquoSchistosomiasis among preg-nant women in rural communities in Nigeriardquo InternationalJournal of Gynecology andObstetrics vol 122 no 1 pp 1ndash4 2013
[44] K R Tan B L Katalenich K E Mace et al ldquoEfficacyof sulphadoxine-pyrimethamine for intermittent preventivetreatment of malaria in pregnancy Mansa Zambiardquo MalariaJournal vol 13 no 1 article 227 2014
12 Journal of Parasitology Research
[45] J Bethony J T Williams H Kloos et al ldquoExposure toSchistosoma mansoni infection in a rural area in Brazil IIhousehold risk factorsrdquo Tropical Medicine and InternationalHealth vol 6 no 2 pp 136ndash145 2001
[46] J C Sousa-Figueiredo D Gamboa J M Pedro et al ldquoEpi-demiology of malaria schistosomiasis geohelminths anemiaand malnutrition in the context of a demographic surveillancesystem in northern Angolardquo PLoS ONE vol 7 no 4 Article IDe33189 2012
[47] F Anto V Asoala M Adjuik et al ldquoWater contact activitiesand prevalence of schistosomiasis infection among school-agechildren in communities along an irrigation scheme in RuralNorthern Ghanardquo Journal of Bacteriology amp Parasitology vol 4article 177 2013
[48] L-A Tchuem Tchuente J M Behnke F S Gilbert V RSouthgate and J Vercruysse ldquoPolyparasitism with Schistosomahaematobium and soil-transmitted helminth infections amongschool children in Loum Cameroonrdquo Tropical Medicine andInternational Health vol 8 no 11 pp 975ndash986 2003
[49] J-F Etard M Audibert and A Dabo ldquoAge-acquired resistanceand predisposition to reinfection with Schistosoma haemato-bium after treatment with praziquantel in Malirdquo The AmericanJournal of TropicalMedicine andHygiene vol 52 no 6 pp 549ndash558 1995
[50] A Gazzinelli G Velasquez-Melendez S B Crawford P TLoVerde R Correa-Oliveira and H Kloos ldquoSocioeconomicdeterminants of schistosomiasis in a poor rural area in BrazilrdquoActa Tropica vol 99 no 2-3 pp 260ndash271 2006
[51] A P Kapito-Tembo V Mwapasa S R Meshnick et al ldquoPreva-lence distribution and risk factors for Schistosoma hematobiuminfection among school children in Blantyre Malawirdquo PLoSNeglected Tropical Diseases vol 3 no 1 article e361 2009
[52] N J Yatich J Yi T Agbenyega et al ldquoMalaria and intestinalhelminth co-infection among pregnant women in Ghanaprevalence and risk factorsrdquo The American Journal of TropicalMedicine and Hygiene vol 80 no 6 pp 896ndash901 2009
[53] M Nacher ldquoInteractions between worms and malaria goodworms or bad wormsrdquoMalaria Journal vol 10 article no 2592011
[54] A A Adegnika and P G Kremsner ldquoEpidemiology of malariaand helminth interaction a review from 2001 to 2011rdquo CurrentOpinion in HIV and AIDS vol 7 no 3 pp 221ndash224 2012
[55] S Getie Y Wondimeneh G Getnet et al ldquoPrevalence andclinical correlates of Schistosoma mansoni co-infection amongmalaria infected patients Northwest Ethiopiardquo BMC ResearchNotes vol 8 no 1 article no 480 2015
[56] E Okafor and A Elenwo ldquoHaemoglobin status of children withmixed infection ofmalaria and urinary schistosomiasis inOdauCommunity Rivers state Nigeriardquo Journal of Agriculture andSocial Research vol 7 no 1 pp 56ndash62 2008
[57] M A McDevitt J Xie V Gordeuk and R Bucala ldquoThe anemiaof malaria infection role of inflammatory cytokinesrdquo CurrentHematology Reports vol 3 no 2 pp 97ndash106 2004
[58] J G Shaw and J F Friedman ldquoIron deficiency anemia focus oninfectious diseases in lesser developed countriesrdquo Anemia vol2011 Article ID 260380 10 pages 2011
[59] H K Green J C Sousa-Figueiredo M-G Basanez et alldquoAnaemia in Ugandan preschool-aged children the relativecontribution of intestinal parasites and malariardquo Parasitologyvol 138 no 12 pp 1534ndash1545 2011
[60] E Ivan N J Crowther E Mutimura L O Osuwat S Janssenand M P Grobusch ldquoHelminthic infections rates and malaria
in HIV-infected pregnant women on anti-retroviral therapy inRwandardquo PLoS Neglected Tropical Diseases vol 7 no 8 ArticleID e2380 2013
Adjusted OR using multivariate regression analysisNA not applicable variables with 119875 gt 02 in bivariate analysis were not included in multivariate analysis
needed to explore the underlying mechanisms of interactionbetween malaria parasitaemia and S haematobium
Schistosomiasis causes long term morbidity such asanaemia Our study showed that the magnitude of S haema-tobium egg counts is significantly related to haemoglobinconcentration confirming that urogenital schistosomiasiscontributes to anaemia [24 25] In this study anaemiawas more pronounced in women with heavy infectionintensity than in those with light infection Coinfection ofhelminth infections and P falciparum increases anaemiaseverity [8 9] Coinfection among pregnant women lowersHb concentration compared with single infection This is inagreement with findings of Okafor and Elenwo [56] Moreso coinfected women with heavy intensity S haematobiuminfection had the lowest mean Hb levels (66 gdL) andthis subpopulation of women contributed to about 72of all severe anaemic cases The combined presence and
interaction of S haematobium and P falciparum infectionsis partly responsible for the low haemoglobin concentrationin women with concurrent infectionMalaria causes anaemiaby destruction and removal of parasitized red blood cellsand shortening of the life span of nonparasitized red cellsas well as decreasing the rate of erythrocyte production inbone marrow [57]Themechanism by which schistosomiasiscauses anaemia is not fully understood but it is suggested thathelminth infections could contribute to increase in the preva-lence of inflammatory syndromes impairing erythropoiesisand interfering with mobilization of reticuloendothelial ironstorages and shortening erythrocyte survival [58] Similar toprevious reports of a study in Uganda [59] malaria parasiteinfection was an independent factor associated with increaseanaemia risk
The risk of coinfection was associated with streamusage (bathing and domestic contact with stream) while
10 Journal of Parasitology Research
less water contact and SP usage decreased risk of infectionThis finding suggests that intervention strategies focusingon combating malaria and schistosomiasis respectively byincreasing the uptake of IPTp-SPdoses and less water contactamong pregnant women living in Munyenge represents themost appropriate prevention of coinfection with consequentincrease in Hb levels
This study had one limitation We did not investigate theprevalence of HIV infection among the study participants Ithas been shown that coinfections with helminths andmalariacause considerable morbidity in the host particularly in thepresence of HIV infection [60]
To conclude the study has indicated that S haematobiumand P falciparum infections are common among pregnantwomen living in Munyenge and their coinfection is influ-enced by high frequencies of these parasites in the same pop-ulationThe study also revealed that younger age and bathingand domestic contact with stream are independently associ-ated with prevalence of S haematobium infection while noIPTp-SP was associated with P falciparum infection Streamusage increased risk of coinfection while less water contactand SP usage decreased its risk The fact that light S haema-tobium infection was less common in P falciparum infectedwomen suggests that Plasmodium falciparum parasitaemiamay be associatedwith intensity of urogenital schistosomiasisin coinfected individuals Anaemia is a severe public healthproblem in pregnancy in Munyenge and coinfection withS haematobium and P falciparum exacerbates anaemiaLess water contact frequency and increase uptake of IPTp-SPdoses will significantly reduce risk of coinfection andconsequently anaemia severity in pregnancy in this setting
Abbreviations
IPTp-SP Intermittent preventive treatment in pregnancy(IPTp) with sulfadoxine-pyrimethamine (SP)
ITN Insecticide treated bed netsHIV Human immunodeficiency virusANC Antenatal care
Competing Interests
The authors declare that they do not have any competinginterests
Authorsrsquo Contributions
Judith K Anchang-Kimbi conceived and designed the studyanalyzed the data and wrote the manuscript Dillys MansohElad participated in the design of the study performedthe experiments and made inputs in manuscript write-upGemain Taiwe Sotoing and Eric Akum Achidi supervisedreviewed and provided inputs to the manuscript All authorsread and approved the final manuscript
Acknowledgments
The authors are grateful to all the pregnant women whogave their consent to participate in the study Special thanks
are due to the chief medical officer nurses and laboratorytechnician of the Munyenge Health Centre for their cooper-ation and contribution This study received financial supportfrom the Ministry of Higher Education University ResearchModernisation grant given to authors Judith K Anchang-Kimbi and Eric Akum Achidi
References
[1] T N Petney and R H Andrews ldquoMultiparasite communitiesin animals and humans frequency structure and pathogenicsignificancerdquo International Journal for Parasitology vol 28 no3 pp 377ndash393 1998
[2] F E G Cox ldquoConcomitant infections parasites and immuneresponsesrdquo Parasitology vol 122 supplement 1 pp S23ndashS382001
[3] M Nacher P Singhasivanon S Yimsamran et al ldquoIntestinalhelminth infections are associated with increased incidenceof Plasmodium falciparum malaria in Thailandrdquo Journal ofParasitology vol 88 no 1 pp 55ndash58 2002
[4] J-Y Le Hesran J Akiana E H M Ndiaye M Dia P Senghorand L Konate ldquoSevere malaria attack is associated with highprevalence of Ascaris lumbricoides infection among childrenin rural Senegalrdquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 98 no 7 pp 397ndash399 2004
[5] M Nacher F Gay P Singhasivanon et al ldquoAscaris lumbricoidesinfection is associated with protection from cerebral malariardquoParasite Immunology vol 22 no 3 pp 107ndash113 2000
[6] V Briand L Watier J-Y Le Hesran A Garcia and M CotldquoCoinfection with Plasmodium falciparum and Schistosomahaematobium protective effect of schistosomiasis on malariain Senegalese childrenrdquo American Journal of Tropical Medicineand Hygiene vol 72 no 6 pp 702ndash707 2005
[7] N Oslash Christensen P Furu J Kurtzhals and A OdaiboldquoHeterologous synergistic interactions in concurrent experi-mental infection in the mouse with Schistosoma mansoniEchinostoma revolution Plasmodium yoelii Babesia microtiand Trypanosoma bruceirdquo Parasitology Research vol 74 no 6pp 544ndash551 1988
[8] G Raso A Luginbuhl C A Adjoua et al ldquoMultiple parasiteinfections and their relationship to self-reported morbidity ina community of rural Cote drsquoIvoirerdquo International Journal ofEpidemiology vol 33 no 5 pp 1092ndash1102 2004
[9] S Brooker W Akhwale R Pullan et al ldquoEpidemiology ofPlasmodium-helminth co-infection in Africa populations atrisk potential impact on anemia and prospects for combiningcontrolrdquo American Journal of Tropical Medicine and Hygienevol 77 no 6 pp 88ndash98 2007
[10] C E Shulman and E K Dorman ldquoReducing childhood mor-tality in poor countries importance and prevention of malariain pregnancyrdquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 97 no 1 pp 30ndash35 2003
[11] WorldHealthOrganisation andAfrica Regional OfficeMalariaPrevention and Control during Pregnancy in the African RegionWHOAFRO Brazzaville Congo 2004
[12] D Engels L Chitsulo A Montresor and L Savioli ldquoTheglobal epidemiological situation of schistosomiasis and newapproaches to control and researchrdquo Acta Tropica vol 82 no2 pp 139ndash146 2002
[13] P J Hotez and A Kamath ldquoNeglected tropical diseases in sub-Saharan Africa review of their prevalence distribution and
[14] M J Van Der Werf S J De Vlas S Brooker et al ldquoQuantifica-tion of clinical morbidity associated with schistosome infectionin sub-Saharan Africardquo Acta Tropica vol 86 no 2-3 pp 125ndash139 2003
[15] M N Nour ldquoSchistosomias health effect on womenrdquo Reviewsin Obstetrics amp Gynecology vol 3 no 1 pp 28ndash32 2010
[16] J F Friedman P Mital H K Kanzaria G R Olds and J DKurtis ldquoSchistosomiasis and pregnancyrdquo Trends in Parasitologyvol 23 no 4 pp 159ndash164 2007
[17] httpwwwwhointschistosomiasisstrategyen[18] H N Ntonifor and J A Ajayi ldquoWater contact and Schistosoma
haematobium infection A case study of some communitiesin Toro Local Government council Area (TLGCA) of BauchiStaterdquoNigeria Journal of Natural and Applied Sciences vol 1 no1 pp 54ndash59 2005
[19] P Saotoing T Vroumsia A M Njan F N Tchuenguem andJ Messi ldquoEpidemiological survey of schistosomiasis due toSchistosoma haematobium in some primary schools in thetown of Maroua far north region Cameroonrdquo InternationalJournal of Tropical Medicine vol 6 no 2 pp 19ndash24 2011
[20] L A Tchuem Tchuente R I K Ngassam L Sumo et al ldquoMap-ping of schistosomiasis and soil- transmitted helminthiasis inthe regions of centre east and west cameroonrdquo PLoS NeglectedTropical Diseases vol 6 no 3 p e1553 2012
[21] L A Tchuem Tchuente N C Dongmo P Ngassam et alldquoMapping of schistosomiasis and soil- transmitted helminthi-asis in the regions of Littoral North-West South and South-West Cameroon and recommendations for treatmentrdquo BMCInfectious Disease vol 13 article 602 2013
[22] K J N Ndamukong M A Ayuk J S Dinga T N Akenji VA Ndiforchu and V P K Titanji ldquoPrevalence and intensity ofurinary schistosomiasis in primary school children of the KottoBarombi health area Cameroonrdquo East African Medical Journalvol 78 no 6 pp 287ndash289 2001
[23] H N Ntonifor G N Mbunkur and N W Ndaleh ldquoEpidemi-ological survey of urinary schistosomiasis in some primaryschools in a new focus behind Mount Cameroon (Munyenge)South West Region Cameroonrdquo East African Medical Journalvol 89 no 3 pp 82ndash88 2012
[24] J F Friedman H K Kanzaria and S T McGarvey ldquoHumanschistosomiasis and anemia the relationship and potentialmechanismsrdquo Trends in Parasitology vol 21 no 8 pp 386ndash3922005
[25] A Ajanga N J S Lwambo L Blair U Nyandindi A Fenwickand S Brooker ldquoSchistosoma mansoni in pregnancy andassociations with anaemia in northwest Tanzaniardquo Transactionsof the Royal Society of Tropical Medicine and Hygiene vol 100no 1 pp 59ndash63 2006
[26] G Helling-Giese E F Kjetland S G Gundersen et al ldquoSchis-tosomiasis in women manifestations in the upper reproductivetractrdquo Acta Tropica vol 62 no 4 pp 225ndash238 1996
[27] R W Steketee B L Nahlen M E Parise and C MenendezldquoTheburden ofmalaria in pregnancy inmalaria-endemic areasrdquoAmerican Journal of Tropical Medicine and Hygiene vol 64 no1-2 pp 28ndash35 2001
[28] V V Laxman B Adamson and T Mahmood ldquoRecurrentectopic pregnancy due to Schistosoma hematobiumrdquo Journal ofObstetrics and Gynaecology vol 28 no 4 pp 461ndash462 2008
[29] S Bahrami H Alatassi S P Slone and D M OrsquoConnorldquoTubal gestation and schistosomiasis a case reportrdquo Journal ofReproductiveMedicine for theObstetrician andGynecologist vol51 no 7 pp 595ndash598 2006
[30] P S Mbabazi O Andan D W Fitzgerald L Chitsulo DEngels and J A Downs ldquoExamining the relationship betweenurogenital schistosomiasis and HIV infectionrdquo PLoS NeglectedTropical Diseases vol 5 no 12 Article ID e1396 2011
[31] R Tweyongyere P A Mawa N O Emojong et al ldquoEffectof praziquantel treatment of Schistosomamansoni during preg-nancy on intensity of infection and antibody responses to schis-tosome antigens results of a randomised placebo-controlledtrialrdquo BMC Infectious Diseases vol 9 article 32 2009
[32] H N Ntonifor A E Green M O S Bopda et al ldquoEpi-demiology of urinary schistosomiasis and soil transmittedhelminthiasis in a recently established focus behind MountCameroonrdquo International Journal of Current Microbiology andApplied Sciences vol 4 no 3 pp 1056ndash1066 2015
[33] S Wanji A J Kengne-Ouafo E E Joan Eyong et al ldquoGeneticdiversity of Plasmodium falciparummerozoite surface protein-1 block 2 in sites of contrasting altitudes and malaria endemic-ities in the Mount Cameroon Regionrdquo American Journal ofTropical Medicine and Hygiene vol 86 no 5 pp 764ndash774 2012
[34] J K Anchang-Kimbi E A Achidi B Nkegoum E Sverremark-Ekstrom and M Troye-Blomberg ldquoDiagnostic comparisonof malaria infection in peripheral blood placental blood andplacental biopsies in Cameroonian parturient womenrdquoMalariaJournal vol 8 no 1 article 126 2009
[35] F J Bryan The Design and Analysis of Research Studies Uni-versity ofOtago Dunedin NewZealand CambridgeUniversityPress Cambridge UK 1992
[36] World Health Organisation Haemoglobin Concentrations forthe Diagnosis of Anaemia and Assessment of Severity Vitaminand mineral Nutrition Information System WHO GenevaSwitzerland 2011
[37] M CheesbroughDistrict Laboratory Practice in Tropical Coun-tries Cambridge University Press Cambridge UK 2006
[39] N O Christensen G Gotsche and F Frandsen ParasitologicalTechniques for Use in Routine Laboratory Maintainance of Schis-tosomes and Used in Studies on the Epidemiology of Human andBovine Schistosomiasis Danish Bilhaziasis Laboratory Manual1984
[40] World Health OrganizationmdashTropical Disease Research TDRstrategic direction Schistosomiasis WHO-TDR 2002
[41] World Health OrganizationGuidelines for the Evaluation of SoilTransmitted Helminthiasis and Schistosomiasis at CommunityLevel A Guide for Managers of Control Programme WHOGeneva Switzerland 1993
[42] J E Eyo G C Onyishi and F C Okafor ldquoUrinary schisto-somiasis among pregnant women in some endemic tropicalsemi-urban communities of Anambra State Nigeriardquo TropicalBiomedicine vol 29 no 4 pp 575ndash579 2012
[43] O T Salawu and A B Odaibo ldquoSchistosomiasis among preg-nant women in rural communities in Nigeriardquo InternationalJournal of Gynecology andObstetrics vol 122 no 1 pp 1ndash4 2013
[44] K R Tan B L Katalenich K E Mace et al ldquoEfficacyof sulphadoxine-pyrimethamine for intermittent preventivetreatment of malaria in pregnancy Mansa Zambiardquo MalariaJournal vol 13 no 1 article 227 2014
12 Journal of Parasitology Research
[45] J Bethony J T Williams H Kloos et al ldquoExposure toSchistosoma mansoni infection in a rural area in Brazil IIhousehold risk factorsrdquo Tropical Medicine and InternationalHealth vol 6 no 2 pp 136ndash145 2001
[46] J C Sousa-Figueiredo D Gamboa J M Pedro et al ldquoEpi-demiology of malaria schistosomiasis geohelminths anemiaand malnutrition in the context of a demographic surveillancesystem in northern Angolardquo PLoS ONE vol 7 no 4 Article IDe33189 2012
[47] F Anto V Asoala M Adjuik et al ldquoWater contact activitiesand prevalence of schistosomiasis infection among school-agechildren in communities along an irrigation scheme in RuralNorthern Ghanardquo Journal of Bacteriology amp Parasitology vol 4article 177 2013
[48] L-A Tchuem Tchuente J M Behnke F S Gilbert V RSouthgate and J Vercruysse ldquoPolyparasitism with Schistosomahaematobium and soil-transmitted helminth infections amongschool children in Loum Cameroonrdquo Tropical Medicine andInternational Health vol 8 no 11 pp 975ndash986 2003
[49] J-F Etard M Audibert and A Dabo ldquoAge-acquired resistanceand predisposition to reinfection with Schistosoma haemato-bium after treatment with praziquantel in Malirdquo The AmericanJournal of TropicalMedicine andHygiene vol 52 no 6 pp 549ndash558 1995
[50] A Gazzinelli G Velasquez-Melendez S B Crawford P TLoVerde R Correa-Oliveira and H Kloos ldquoSocioeconomicdeterminants of schistosomiasis in a poor rural area in BrazilrdquoActa Tropica vol 99 no 2-3 pp 260ndash271 2006
[51] A P Kapito-Tembo V Mwapasa S R Meshnick et al ldquoPreva-lence distribution and risk factors for Schistosoma hematobiuminfection among school children in Blantyre Malawirdquo PLoSNeglected Tropical Diseases vol 3 no 1 article e361 2009
[52] N J Yatich J Yi T Agbenyega et al ldquoMalaria and intestinalhelminth co-infection among pregnant women in Ghanaprevalence and risk factorsrdquo The American Journal of TropicalMedicine and Hygiene vol 80 no 6 pp 896ndash901 2009
[53] M Nacher ldquoInteractions between worms and malaria goodworms or bad wormsrdquoMalaria Journal vol 10 article no 2592011
[54] A A Adegnika and P G Kremsner ldquoEpidemiology of malariaand helminth interaction a review from 2001 to 2011rdquo CurrentOpinion in HIV and AIDS vol 7 no 3 pp 221ndash224 2012
[55] S Getie Y Wondimeneh G Getnet et al ldquoPrevalence andclinical correlates of Schistosoma mansoni co-infection amongmalaria infected patients Northwest Ethiopiardquo BMC ResearchNotes vol 8 no 1 article no 480 2015
[56] E Okafor and A Elenwo ldquoHaemoglobin status of children withmixed infection ofmalaria and urinary schistosomiasis inOdauCommunity Rivers state Nigeriardquo Journal of Agriculture andSocial Research vol 7 no 1 pp 56ndash62 2008
[57] M A McDevitt J Xie V Gordeuk and R Bucala ldquoThe anemiaof malaria infection role of inflammatory cytokinesrdquo CurrentHematology Reports vol 3 no 2 pp 97ndash106 2004
[58] J G Shaw and J F Friedman ldquoIron deficiency anemia focus oninfectious diseases in lesser developed countriesrdquo Anemia vol2011 Article ID 260380 10 pages 2011
[59] H K Green J C Sousa-Figueiredo M-G Basanez et alldquoAnaemia in Ugandan preschool-aged children the relativecontribution of intestinal parasites and malariardquo Parasitologyvol 138 no 12 pp 1534ndash1545 2011
[60] E Ivan N J Crowther E Mutimura L O Osuwat S Janssenand M P Grobusch ldquoHelminthic infections rates and malaria
in HIV-infected pregnant women on anti-retroviral therapy inRwandardquo PLoS Neglected Tropical Diseases vol 7 no 8 ArticleID e2380 2013
less water contact and SP usage decreased risk of infectionThis finding suggests that intervention strategies focusingon combating malaria and schistosomiasis respectively byincreasing the uptake of IPTp-SPdoses and less water contactamong pregnant women living in Munyenge represents themost appropriate prevention of coinfection with consequentincrease in Hb levels
This study had one limitation We did not investigate theprevalence of HIV infection among the study participants Ithas been shown that coinfections with helminths andmalariacause considerable morbidity in the host particularly in thepresence of HIV infection [60]
To conclude the study has indicated that S haematobiumand P falciparum infections are common among pregnantwomen living in Munyenge and their coinfection is influ-enced by high frequencies of these parasites in the same pop-ulationThe study also revealed that younger age and bathingand domestic contact with stream are independently associ-ated with prevalence of S haematobium infection while noIPTp-SP was associated with P falciparum infection Streamusage increased risk of coinfection while less water contactand SP usage decreased its risk The fact that light S haema-tobium infection was less common in P falciparum infectedwomen suggests that Plasmodium falciparum parasitaemiamay be associatedwith intensity of urogenital schistosomiasisin coinfected individuals Anaemia is a severe public healthproblem in pregnancy in Munyenge and coinfection withS haematobium and P falciparum exacerbates anaemiaLess water contact frequency and increase uptake of IPTp-SPdoses will significantly reduce risk of coinfection andconsequently anaemia severity in pregnancy in this setting
Abbreviations
IPTp-SP Intermittent preventive treatment in pregnancy(IPTp) with sulfadoxine-pyrimethamine (SP)
ITN Insecticide treated bed netsHIV Human immunodeficiency virusANC Antenatal care
Competing Interests
The authors declare that they do not have any competinginterests
Authorsrsquo Contributions
Judith K Anchang-Kimbi conceived and designed the studyanalyzed the data and wrote the manuscript Dillys MansohElad participated in the design of the study performedthe experiments and made inputs in manuscript write-upGemain Taiwe Sotoing and Eric Akum Achidi supervisedreviewed and provided inputs to the manuscript All authorsread and approved the final manuscript
Acknowledgments
The authors are grateful to all the pregnant women whogave their consent to participate in the study Special thanks
are due to the chief medical officer nurses and laboratorytechnician of the Munyenge Health Centre for their cooper-ation and contribution This study received financial supportfrom the Ministry of Higher Education University ResearchModernisation grant given to authors Judith K Anchang-Kimbi and Eric Akum Achidi
References
[1] T N Petney and R H Andrews ldquoMultiparasite communitiesin animals and humans frequency structure and pathogenicsignificancerdquo International Journal for Parasitology vol 28 no3 pp 377ndash393 1998
[2] F E G Cox ldquoConcomitant infections parasites and immuneresponsesrdquo Parasitology vol 122 supplement 1 pp S23ndashS382001
[3] M Nacher P Singhasivanon S Yimsamran et al ldquoIntestinalhelminth infections are associated with increased incidenceof Plasmodium falciparum malaria in Thailandrdquo Journal ofParasitology vol 88 no 1 pp 55ndash58 2002
[4] J-Y Le Hesran J Akiana E H M Ndiaye M Dia P Senghorand L Konate ldquoSevere malaria attack is associated with highprevalence of Ascaris lumbricoides infection among childrenin rural Senegalrdquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 98 no 7 pp 397ndash399 2004
[5] M Nacher F Gay P Singhasivanon et al ldquoAscaris lumbricoidesinfection is associated with protection from cerebral malariardquoParasite Immunology vol 22 no 3 pp 107ndash113 2000
[6] V Briand L Watier J-Y Le Hesran A Garcia and M CotldquoCoinfection with Plasmodium falciparum and Schistosomahaematobium protective effect of schistosomiasis on malariain Senegalese childrenrdquo American Journal of Tropical Medicineand Hygiene vol 72 no 6 pp 702ndash707 2005
[7] N Oslash Christensen P Furu J Kurtzhals and A OdaiboldquoHeterologous synergistic interactions in concurrent experi-mental infection in the mouse with Schistosoma mansoniEchinostoma revolution Plasmodium yoelii Babesia microtiand Trypanosoma bruceirdquo Parasitology Research vol 74 no 6pp 544ndash551 1988
[8] G Raso A Luginbuhl C A Adjoua et al ldquoMultiple parasiteinfections and their relationship to self-reported morbidity ina community of rural Cote drsquoIvoirerdquo International Journal ofEpidemiology vol 33 no 5 pp 1092ndash1102 2004
[9] S Brooker W Akhwale R Pullan et al ldquoEpidemiology ofPlasmodium-helminth co-infection in Africa populations atrisk potential impact on anemia and prospects for combiningcontrolrdquo American Journal of Tropical Medicine and Hygienevol 77 no 6 pp 88ndash98 2007
[10] C E Shulman and E K Dorman ldquoReducing childhood mor-tality in poor countries importance and prevention of malariain pregnancyrdquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 97 no 1 pp 30ndash35 2003
[11] WorldHealthOrganisation andAfrica Regional OfficeMalariaPrevention and Control during Pregnancy in the African RegionWHOAFRO Brazzaville Congo 2004
[12] D Engels L Chitsulo A Montresor and L Savioli ldquoTheglobal epidemiological situation of schistosomiasis and newapproaches to control and researchrdquo Acta Tropica vol 82 no2 pp 139ndash146 2002
[13] P J Hotez and A Kamath ldquoNeglected tropical diseases in sub-Saharan Africa review of their prevalence distribution and
[14] M J Van Der Werf S J De Vlas S Brooker et al ldquoQuantifica-tion of clinical morbidity associated with schistosome infectionin sub-Saharan Africardquo Acta Tropica vol 86 no 2-3 pp 125ndash139 2003
[15] M N Nour ldquoSchistosomias health effect on womenrdquo Reviewsin Obstetrics amp Gynecology vol 3 no 1 pp 28ndash32 2010
[16] J F Friedman P Mital H K Kanzaria G R Olds and J DKurtis ldquoSchistosomiasis and pregnancyrdquo Trends in Parasitologyvol 23 no 4 pp 159ndash164 2007
[17] httpwwwwhointschistosomiasisstrategyen[18] H N Ntonifor and J A Ajayi ldquoWater contact and Schistosoma
haematobium infection A case study of some communitiesin Toro Local Government council Area (TLGCA) of BauchiStaterdquoNigeria Journal of Natural and Applied Sciences vol 1 no1 pp 54ndash59 2005
[19] P Saotoing T Vroumsia A M Njan F N Tchuenguem andJ Messi ldquoEpidemiological survey of schistosomiasis due toSchistosoma haematobium in some primary schools in thetown of Maroua far north region Cameroonrdquo InternationalJournal of Tropical Medicine vol 6 no 2 pp 19ndash24 2011
[20] L A Tchuem Tchuente R I K Ngassam L Sumo et al ldquoMap-ping of schistosomiasis and soil- transmitted helminthiasis inthe regions of centre east and west cameroonrdquo PLoS NeglectedTropical Diseases vol 6 no 3 p e1553 2012
[21] L A Tchuem Tchuente N C Dongmo P Ngassam et alldquoMapping of schistosomiasis and soil- transmitted helminthi-asis in the regions of Littoral North-West South and South-West Cameroon and recommendations for treatmentrdquo BMCInfectious Disease vol 13 article 602 2013
[22] K J N Ndamukong M A Ayuk J S Dinga T N Akenji VA Ndiforchu and V P K Titanji ldquoPrevalence and intensity ofurinary schistosomiasis in primary school children of the KottoBarombi health area Cameroonrdquo East African Medical Journalvol 78 no 6 pp 287ndash289 2001
[23] H N Ntonifor G N Mbunkur and N W Ndaleh ldquoEpidemi-ological survey of urinary schistosomiasis in some primaryschools in a new focus behind Mount Cameroon (Munyenge)South West Region Cameroonrdquo East African Medical Journalvol 89 no 3 pp 82ndash88 2012
[24] J F Friedman H K Kanzaria and S T McGarvey ldquoHumanschistosomiasis and anemia the relationship and potentialmechanismsrdquo Trends in Parasitology vol 21 no 8 pp 386ndash3922005
[25] A Ajanga N J S Lwambo L Blair U Nyandindi A Fenwickand S Brooker ldquoSchistosoma mansoni in pregnancy andassociations with anaemia in northwest Tanzaniardquo Transactionsof the Royal Society of Tropical Medicine and Hygiene vol 100no 1 pp 59ndash63 2006
[26] G Helling-Giese E F Kjetland S G Gundersen et al ldquoSchis-tosomiasis in women manifestations in the upper reproductivetractrdquo Acta Tropica vol 62 no 4 pp 225ndash238 1996
[27] R W Steketee B L Nahlen M E Parise and C MenendezldquoTheburden ofmalaria in pregnancy inmalaria-endemic areasrdquoAmerican Journal of Tropical Medicine and Hygiene vol 64 no1-2 pp 28ndash35 2001
[28] V V Laxman B Adamson and T Mahmood ldquoRecurrentectopic pregnancy due to Schistosoma hematobiumrdquo Journal ofObstetrics and Gynaecology vol 28 no 4 pp 461ndash462 2008
[29] S Bahrami H Alatassi S P Slone and D M OrsquoConnorldquoTubal gestation and schistosomiasis a case reportrdquo Journal ofReproductiveMedicine for theObstetrician andGynecologist vol51 no 7 pp 595ndash598 2006
[30] P S Mbabazi O Andan D W Fitzgerald L Chitsulo DEngels and J A Downs ldquoExamining the relationship betweenurogenital schistosomiasis and HIV infectionrdquo PLoS NeglectedTropical Diseases vol 5 no 12 Article ID e1396 2011
[31] R Tweyongyere P A Mawa N O Emojong et al ldquoEffectof praziquantel treatment of Schistosomamansoni during preg-nancy on intensity of infection and antibody responses to schis-tosome antigens results of a randomised placebo-controlledtrialrdquo BMC Infectious Diseases vol 9 article 32 2009
[32] H N Ntonifor A E Green M O S Bopda et al ldquoEpi-demiology of urinary schistosomiasis and soil transmittedhelminthiasis in a recently established focus behind MountCameroonrdquo International Journal of Current Microbiology andApplied Sciences vol 4 no 3 pp 1056ndash1066 2015
[33] S Wanji A J Kengne-Ouafo E E Joan Eyong et al ldquoGeneticdiversity of Plasmodium falciparummerozoite surface protein-1 block 2 in sites of contrasting altitudes and malaria endemic-ities in the Mount Cameroon Regionrdquo American Journal ofTropical Medicine and Hygiene vol 86 no 5 pp 764ndash774 2012
[34] J K Anchang-Kimbi E A Achidi B Nkegoum E Sverremark-Ekstrom and M Troye-Blomberg ldquoDiagnostic comparisonof malaria infection in peripheral blood placental blood andplacental biopsies in Cameroonian parturient womenrdquoMalariaJournal vol 8 no 1 article 126 2009
[35] F J Bryan The Design and Analysis of Research Studies Uni-versity ofOtago Dunedin NewZealand CambridgeUniversityPress Cambridge UK 1992
[36] World Health Organisation Haemoglobin Concentrations forthe Diagnosis of Anaemia and Assessment of Severity Vitaminand mineral Nutrition Information System WHO GenevaSwitzerland 2011
[37] M CheesbroughDistrict Laboratory Practice in Tropical Coun-tries Cambridge University Press Cambridge UK 2006
[39] N O Christensen G Gotsche and F Frandsen ParasitologicalTechniques for Use in Routine Laboratory Maintainance of Schis-tosomes and Used in Studies on the Epidemiology of Human andBovine Schistosomiasis Danish Bilhaziasis Laboratory Manual1984
[40] World Health OrganizationmdashTropical Disease Research TDRstrategic direction Schistosomiasis WHO-TDR 2002
[41] World Health OrganizationGuidelines for the Evaluation of SoilTransmitted Helminthiasis and Schistosomiasis at CommunityLevel A Guide for Managers of Control Programme WHOGeneva Switzerland 1993
[42] J E Eyo G C Onyishi and F C Okafor ldquoUrinary schisto-somiasis among pregnant women in some endemic tropicalsemi-urban communities of Anambra State Nigeriardquo TropicalBiomedicine vol 29 no 4 pp 575ndash579 2012
[43] O T Salawu and A B Odaibo ldquoSchistosomiasis among preg-nant women in rural communities in Nigeriardquo InternationalJournal of Gynecology andObstetrics vol 122 no 1 pp 1ndash4 2013
[44] K R Tan B L Katalenich K E Mace et al ldquoEfficacyof sulphadoxine-pyrimethamine for intermittent preventivetreatment of malaria in pregnancy Mansa Zambiardquo MalariaJournal vol 13 no 1 article 227 2014
12 Journal of Parasitology Research
[45] J Bethony J T Williams H Kloos et al ldquoExposure toSchistosoma mansoni infection in a rural area in Brazil IIhousehold risk factorsrdquo Tropical Medicine and InternationalHealth vol 6 no 2 pp 136ndash145 2001
[46] J C Sousa-Figueiredo D Gamboa J M Pedro et al ldquoEpi-demiology of malaria schistosomiasis geohelminths anemiaand malnutrition in the context of a demographic surveillancesystem in northern Angolardquo PLoS ONE vol 7 no 4 Article IDe33189 2012
[47] F Anto V Asoala M Adjuik et al ldquoWater contact activitiesand prevalence of schistosomiasis infection among school-agechildren in communities along an irrigation scheme in RuralNorthern Ghanardquo Journal of Bacteriology amp Parasitology vol 4article 177 2013
[48] L-A Tchuem Tchuente J M Behnke F S Gilbert V RSouthgate and J Vercruysse ldquoPolyparasitism with Schistosomahaematobium and soil-transmitted helminth infections amongschool children in Loum Cameroonrdquo Tropical Medicine andInternational Health vol 8 no 11 pp 975ndash986 2003
[49] J-F Etard M Audibert and A Dabo ldquoAge-acquired resistanceand predisposition to reinfection with Schistosoma haemato-bium after treatment with praziquantel in Malirdquo The AmericanJournal of TropicalMedicine andHygiene vol 52 no 6 pp 549ndash558 1995
[50] A Gazzinelli G Velasquez-Melendez S B Crawford P TLoVerde R Correa-Oliveira and H Kloos ldquoSocioeconomicdeterminants of schistosomiasis in a poor rural area in BrazilrdquoActa Tropica vol 99 no 2-3 pp 260ndash271 2006
[51] A P Kapito-Tembo V Mwapasa S R Meshnick et al ldquoPreva-lence distribution and risk factors for Schistosoma hematobiuminfection among school children in Blantyre Malawirdquo PLoSNeglected Tropical Diseases vol 3 no 1 article e361 2009
[52] N J Yatich J Yi T Agbenyega et al ldquoMalaria and intestinalhelminth co-infection among pregnant women in Ghanaprevalence and risk factorsrdquo The American Journal of TropicalMedicine and Hygiene vol 80 no 6 pp 896ndash901 2009
[53] M Nacher ldquoInteractions between worms and malaria goodworms or bad wormsrdquoMalaria Journal vol 10 article no 2592011
[54] A A Adegnika and P G Kremsner ldquoEpidemiology of malariaand helminth interaction a review from 2001 to 2011rdquo CurrentOpinion in HIV and AIDS vol 7 no 3 pp 221ndash224 2012
[55] S Getie Y Wondimeneh G Getnet et al ldquoPrevalence andclinical correlates of Schistosoma mansoni co-infection amongmalaria infected patients Northwest Ethiopiardquo BMC ResearchNotes vol 8 no 1 article no 480 2015
[56] E Okafor and A Elenwo ldquoHaemoglobin status of children withmixed infection ofmalaria and urinary schistosomiasis inOdauCommunity Rivers state Nigeriardquo Journal of Agriculture andSocial Research vol 7 no 1 pp 56ndash62 2008
[57] M A McDevitt J Xie V Gordeuk and R Bucala ldquoThe anemiaof malaria infection role of inflammatory cytokinesrdquo CurrentHematology Reports vol 3 no 2 pp 97ndash106 2004
[58] J G Shaw and J F Friedman ldquoIron deficiency anemia focus oninfectious diseases in lesser developed countriesrdquo Anemia vol2011 Article ID 260380 10 pages 2011
[59] H K Green J C Sousa-Figueiredo M-G Basanez et alldquoAnaemia in Ugandan preschool-aged children the relativecontribution of intestinal parasites and malariardquo Parasitologyvol 138 no 12 pp 1534ndash1545 2011
[60] E Ivan N J Crowther E Mutimura L O Osuwat S Janssenand M P Grobusch ldquoHelminthic infections rates and malaria
in HIV-infected pregnant women on anti-retroviral therapy inRwandardquo PLoS Neglected Tropical Diseases vol 7 no 8 ArticleID e2380 2013
[14] M J Van Der Werf S J De Vlas S Brooker et al ldquoQuantifica-tion of clinical morbidity associated with schistosome infectionin sub-Saharan Africardquo Acta Tropica vol 86 no 2-3 pp 125ndash139 2003
[15] M N Nour ldquoSchistosomias health effect on womenrdquo Reviewsin Obstetrics amp Gynecology vol 3 no 1 pp 28ndash32 2010
[16] J F Friedman P Mital H K Kanzaria G R Olds and J DKurtis ldquoSchistosomiasis and pregnancyrdquo Trends in Parasitologyvol 23 no 4 pp 159ndash164 2007
[17] httpwwwwhointschistosomiasisstrategyen[18] H N Ntonifor and J A Ajayi ldquoWater contact and Schistosoma
haematobium infection A case study of some communitiesin Toro Local Government council Area (TLGCA) of BauchiStaterdquoNigeria Journal of Natural and Applied Sciences vol 1 no1 pp 54ndash59 2005
[19] P Saotoing T Vroumsia A M Njan F N Tchuenguem andJ Messi ldquoEpidemiological survey of schistosomiasis due toSchistosoma haematobium in some primary schools in thetown of Maroua far north region Cameroonrdquo InternationalJournal of Tropical Medicine vol 6 no 2 pp 19ndash24 2011
[20] L A Tchuem Tchuente R I K Ngassam L Sumo et al ldquoMap-ping of schistosomiasis and soil- transmitted helminthiasis inthe regions of centre east and west cameroonrdquo PLoS NeglectedTropical Diseases vol 6 no 3 p e1553 2012
[21] L A Tchuem Tchuente N C Dongmo P Ngassam et alldquoMapping of schistosomiasis and soil- transmitted helminthi-asis in the regions of Littoral North-West South and South-West Cameroon and recommendations for treatmentrdquo BMCInfectious Disease vol 13 article 602 2013
[22] K J N Ndamukong M A Ayuk J S Dinga T N Akenji VA Ndiforchu and V P K Titanji ldquoPrevalence and intensity ofurinary schistosomiasis in primary school children of the KottoBarombi health area Cameroonrdquo East African Medical Journalvol 78 no 6 pp 287ndash289 2001
[23] H N Ntonifor G N Mbunkur and N W Ndaleh ldquoEpidemi-ological survey of urinary schistosomiasis in some primaryschools in a new focus behind Mount Cameroon (Munyenge)South West Region Cameroonrdquo East African Medical Journalvol 89 no 3 pp 82ndash88 2012
[24] J F Friedman H K Kanzaria and S T McGarvey ldquoHumanschistosomiasis and anemia the relationship and potentialmechanismsrdquo Trends in Parasitology vol 21 no 8 pp 386ndash3922005
[25] A Ajanga N J S Lwambo L Blair U Nyandindi A Fenwickand S Brooker ldquoSchistosoma mansoni in pregnancy andassociations with anaemia in northwest Tanzaniardquo Transactionsof the Royal Society of Tropical Medicine and Hygiene vol 100no 1 pp 59ndash63 2006
[26] G Helling-Giese E F Kjetland S G Gundersen et al ldquoSchis-tosomiasis in women manifestations in the upper reproductivetractrdquo Acta Tropica vol 62 no 4 pp 225ndash238 1996
[27] R W Steketee B L Nahlen M E Parise and C MenendezldquoTheburden ofmalaria in pregnancy inmalaria-endemic areasrdquoAmerican Journal of Tropical Medicine and Hygiene vol 64 no1-2 pp 28ndash35 2001
[28] V V Laxman B Adamson and T Mahmood ldquoRecurrentectopic pregnancy due to Schistosoma hematobiumrdquo Journal ofObstetrics and Gynaecology vol 28 no 4 pp 461ndash462 2008
[29] S Bahrami H Alatassi S P Slone and D M OrsquoConnorldquoTubal gestation and schistosomiasis a case reportrdquo Journal ofReproductiveMedicine for theObstetrician andGynecologist vol51 no 7 pp 595ndash598 2006
[30] P S Mbabazi O Andan D W Fitzgerald L Chitsulo DEngels and J A Downs ldquoExamining the relationship betweenurogenital schistosomiasis and HIV infectionrdquo PLoS NeglectedTropical Diseases vol 5 no 12 Article ID e1396 2011
[31] R Tweyongyere P A Mawa N O Emojong et al ldquoEffectof praziquantel treatment of Schistosomamansoni during preg-nancy on intensity of infection and antibody responses to schis-tosome antigens results of a randomised placebo-controlledtrialrdquo BMC Infectious Diseases vol 9 article 32 2009
[32] H N Ntonifor A E Green M O S Bopda et al ldquoEpi-demiology of urinary schistosomiasis and soil transmittedhelminthiasis in a recently established focus behind MountCameroonrdquo International Journal of Current Microbiology andApplied Sciences vol 4 no 3 pp 1056ndash1066 2015
[33] S Wanji A J Kengne-Ouafo E E Joan Eyong et al ldquoGeneticdiversity of Plasmodium falciparummerozoite surface protein-1 block 2 in sites of contrasting altitudes and malaria endemic-ities in the Mount Cameroon Regionrdquo American Journal ofTropical Medicine and Hygiene vol 86 no 5 pp 764ndash774 2012
[34] J K Anchang-Kimbi E A Achidi B Nkegoum E Sverremark-Ekstrom and M Troye-Blomberg ldquoDiagnostic comparisonof malaria infection in peripheral blood placental blood andplacental biopsies in Cameroonian parturient womenrdquoMalariaJournal vol 8 no 1 article 126 2009
[35] F J Bryan The Design and Analysis of Research Studies Uni-versity ofOtago Dunedin NewZealand CambridgeUniversityPress Cambridge UK 1992
[36] World Health Organisation Haemoglobin Concentrations forthe Diagnosis of Anaemia and Assessment of Severity Vitaminand mineral Nutrition Information System WHO GenevaSwitzerland 2011
[37] M CheesbroughDistrict Laboratory Practice in Tropical Coun-tries Cambridge University Press Cambridge UK 2006
[39] N O Christensen G Gotsche and F Frandsen ParasitologicalTechniques for Use in Routine Laboratory Maintainance of Schis-tosomes and Used in Studies on the Epidemiology of Human andBovine Schistosomiasis Danish Bilhaziasis Laboratory Manual1984
[40] World Health OrganizationmdashTropical Disease Research TDRstrategic direction Schistosomiasis WHO-TDR 2002
[41] World Health OrganizationGuidelines for the Evaluation of SoilTransmitted Helminthiasis and Schistosomiasis at CommunityLevel A Guide for Managers of Control Programme WHOGeneva Switzerland 1993
[42] J E Eyo G C Onyishi and F C Okafor ldquoUrinary schisto-somiasis among pregnant women in some endemic tropicalsemi-urban communities of Anambra State Nigeriardquo TropicalBiomedicine vol 29 no 4 pp 575ndash579 2012
[43] O T Salawu and A B Odaibo ldquoSchistosomiasis among preg-nant women in rural communities in Nigeriardquo InternationalJournal of Gynecology andObstetrics vol 122 no 1 pp 1ndash4 2013
[44] K R Tan B L Katalenich K E Mace et al ldquoEfficacyof sulphadoxine-pyrimethamine for intermittent preventivetreatment of malaria in pregnancy Mansa Zambiardquo MalariaJournal vol 13 no 1 article 227 2014
12 Journal of Parasitology Research
[45] J Bethony J T Williams H Kloos et al ldquoExposure toSchistosoma mansoni infection in a rural area in Brazil IIhousehold risk factorsrdquo Tropical Medicine and InternationalHealth vol 6 no 2 pp 136ndash145 2001
[46] J C Sousa-Figueiredo D Gamboa J M Pedro et al ldquoEpi-demiology of malaria schistosomiasis geohelminths anemiaand malnutrition in the context of a demographic surveillancesystem in northern Angolardquo PLoS ONE vol 7 no 4 Article IDe33189 2012
[47] F Anto V Asoala M Adjuik et al ldquoWater contact activitiesand prevalence of schistosomiasis infection among school-agechildren in communities along an irrigation scheme in RuralNorthern Ghanardquo Journal of Bacteriology amp Parasitology vol 4article 177 2013
[48] L-A Tchuem Tchuente J M Behnke F S Gilbert V RSouthgate and J Vercruysse ldquoPolyparasitism with Schistosomahaematobium and soil-transmitted helminth infections amongschool children in Loum Cameroonrdquo Tropical Medicine andInternational Health vol 8 no 11 pp 975ndash986 2003
[49] J-F Etard M Audibert and A Dabo ldquoAge-acquired resistanceand predisposition to reinfection with Schistosoma haemato-bium after treatment with praziquantel in Malirdquo The AmericanJournal of TropicalMedicine andHygiene vol 52 no 6 pp 549ndash558 1995
[50] A Gazzinelli G Velasquez-Melendez S B Crawford P TLoVerde R Correa-Oliveira and H Kloos ldquoSocioeconomicdeterminants of schistosomiasis in a poor rural area in BrazilrdquoActa Tropica vol 99 no 2-3 pp 260ndash271 2006
[51] A P Kapito-Tembo V Mwapasa S R Meshnick et al ldquoPreva-lence distribution and risk factors for Schistosoma hematobiuminfection among school children in Blantyre Malawirdquo PLoSNeglected Tropical Diseases vol 3 no 1 article e361 2009
[52] N J Yatich J Yi T Agbenyega et al ldquoMalaria and intestinalhelminth co-infection among pregnant women in Ghanaprevalence and risk factorsrdquo The American Journal of TropicalMedicine and Hygiene vol 80 no 6 pp 896ndash901 2009
[53] M Nacher ldquoInteractions between worms and malaria goodworms or bad wormsrdquoMalaria Journal vol 10 article no 2592011
[54] A A Adegnika and P G Kremsner ldquoEpidemiology of malariaand helminth interaction a review from 2001 to 2011rdquo CurrentOpinion in HIV and AIDS vol 7 no 3 pp 221ndash224 2012
[55] S Getie Y Wondimeneh G Getnet et al ldquoPrevalence andclinical correlates of Schistosoma mansoni co-infection amongmalaria infected patients Northwest Ethiopiardquo BMC ResearchNotes vol 8 no 1 article no 480 2015
[56] E Okafor and A Elenwo ldquoHaemoglobin status of children withmixed infection ofmalaria and urinary schistosomiasis inOdauCommunity Rivers state Nigeriardquo Journal of Agriculture andSocial Research vol 7 no 1 pp 56ndash62 2008
[57] M A McDevitt J Xie V Gordeuk and R Bucala ldquoThe anemiaof malaria infection role of inflammatory cytokinesrdquo CurrentHematology Reports vol 3 no 2 pp 97ndash106 2004
[58] J G Shaw and J F Friedman ldquoIron deficiency anemia focus oninfectious diseases in lesser developed countriesrdquo Anemia vol2011 Article ID 260380 10 pages 2011
[59] H K Green J C Sousa-Figueiredo M-G Basanez et alldquoAnaemia in Ugandan preschool-aged children the relativecontribution of intestinal parasites and malariardquo Parasitologyvol 138 no 12 pp 1534ndash1545 2011
[60] E Ivan N J Crowther E Mutimura L O Osuwat S Janssenand M P Grobusch ldquoHelminthic infections rates and malaria
in HIV-infected pregnant women on anti-retroviral therapy inRwandardquo PLoS Neglected Tropical Diseases vol 7 no 8 ArticleID e2380 2013
[45] J Bethony J T Williams H Kloos et al ldquoExposure toSchistosoma mansoni infection in a rural area in Brazil IIhousehold risk factorsrdquo Tropical Medicine and InternationalHealth vol 6 no 2 pp 136ndash145 2001
[46] J C Sousa-Figueiredo D Gamboa J M Pedro et al ldquoEpi-demiology of malaria schistosomiasis geohelminths anemiaand malnutrition in the context of a demographic surveillancesystem in northern Angolardquo PLoS ONE vol 7 no 4 Article IDe33189 2012
[47] F Anto V Asoala M Adjuik et al ldquoWater contact activitiesand prevalence of schistosomiasis infection among school-agechildren in communities along an irrigation scheme in RuralNorthern Ghanardquo Journal of Bacteriology amp Parasitology vol 4article 177 2013
[48] L-A Tchuem Tchuente J M Behnke F S Gilbert V RSouthgate and J Vercruysse ldquoPolyparasitism with Schistosomahaematobium and soil-transmitted helminth infections amongschool children in Loum Cameroonrdquo Tropical Medicine andInternational Health vol 8 no 11 pp 975ndash986 2003
[49] J-F Etard M Audibert and A Dabo ldquoAge-acquired resistanceand predisposition to reinfection with Schistosoma haemato-bium after treatment with praziquantel in Malirdquo The AmericanJournal of TropicalMedicine andHygiene vol 52 no 6 pp 549ndash558 1995
[50] A Gazzinelli G Velasquez-Melendez S B Crawford P TLoVerde R Correa-Oliveira and H Kloos ldquoSocioeconomicdeterminants of schistosomiasis in a poor rural area in BrazilrdquoActa Tropica vol 99 no 2-3 pp 260ndash271 2006
[51] A P Kapito-Tembo V Mwapasa S R Meshnick et al ldquoPreva-lence distribution and risk factors for Schistosoma hematobiuminfection among school children in Blantyre Malawirdquo PLoSNeglected Tropical Diseases vol 3 no 1 article e361 2009
[52] N J Yatich J Yi T Agbenyega et al ldquoMalaria and intestinalhelminth co-infection among pregnant women in Ghanaprevalence and risk factorsrdquo The American Journal of TropicalMedicine and Hygiene vol 80 no 6 pp 896ndash901 2009
[53] M Nacher ldquoInteractions between worms and malaria goodworms or bad wormsrdquoMalaria Journal vol 10 article no 2592011
[54] A A Adegnika and P G Kremsner ldquoEpidemiology of malariaand helminth interaction a review from 2001 to 2011rdquo CurrentOpinion in HIV and AIDS vol 7 no 3 pp 221ndash224 2012
[55] S Getie Y Wondimeneh G Getnet et al ldquoPrevalence andclinical correlates of Schistosoma mansoni co-infection amongmalaria infected patients Northwest Ethiopiardquo BMC ResearchNotes vol 8 no 1 article no 480 2015
[56] E Okafor and A Elenwo ldquoHaemoglobin status of children withmixed infection ofmalaria and urinary schistosomiasis inOdauCommunity Rivers state Nigeriardquo Journal of Agriculture andSocial Research vol 7 no 1 pp 56ndash62 2008
[57] M A McDevitt J Xie V Gordeuk and R Bucala ldquoThe anemiaof malaria infection role of inflammatory cytokinesrdquo CurrentHematology Reports vol 3 no 2 pp 97ndash106 2004
[58] J G Shaw and J F Friedman ldquoIron deficiency anemia focus oninfectious diseases in lesser developed countriesrdquo Anemia vol2011 Article ID 260380 10 pages 2011
[59] H K Green J C Sousa-Figueiredo M-G Basanez et alldquoAnaemia in Ugandan preschool-aged children the relativecontribution of intestinal parasites and malariardquo Parasitologyvol 138 no 12 pp 1534ndash1545 2011
[60] E Ivan N J Crowther E Mutimura L O Osuwat S Janssenand M P Grobusch ldquoHelminthic infections rates and malaria
in HIV-infected pregnant women on anti-retroviral therapy inRwandardquo PLoS Neglected Tropical Diseases vol 7 no 8 ArticleID e2380 2013
![Deep, multi-stage transcriptome of the schistosomiasis vector … · 2017. 8. 28. · schistosomiasis - Schistosoma mansoni [7], Schistosoma japonicum [53] and Schistosoma haematobium](https://static.documents.pub/doc/80x56/60f8a53e7bdd0764ad39282d/deep-multi-stage-transcriptome-of-the-schistosomiasis-vector-2017-8-28-schistosomiasis.jpg)
