1Health Research Institute Infectious and Tropical Diseases Research Center Ahvaz Jundishapur University of Medical SciencesAhvaz Iran2Department of Medical Parasitology amp Student Research Committee Faculty of MedicineAhvaz Jundishapur University of Medical Sciences Ahvaz Iran3Cellular and Molecular Research Center and Department of Medical Parasitology and MycologyUrmia University of Medical Sciences PO Box 571551441 Urmia Iran4CDC Department Deputy of Health Ahvaz Jundishapur University of Medical Sciences Ahvaz Iran
Correspondence should be addressed to Shahram Khademvatan khademvatanyahoocom
Received 29 June 2015 Revised 28 October 2015 Accepted 28 October 2015
Academic Editor Carlos E P Corbett
Copyright copy 2015 Shokrollah Salmanzadeh et alThis is an open access article distributed under theCreativeCommonsAttributionLicense which permits unrestricted use distribution and reproduction in anymedium provided the originalwork is properly cited
Iran is considered as one of the malaria endemic countries of the Eastern Mediterranean Region (EMR) and is at risk due toneighboringAfghanistan Pakistan in the east and Iraq to thewestTherefore the aim of the present investigation is the evaluation ofthe trend ofmalaria distribution during the past decade (2001ndash2014) in Khuzestan province southwestern Iran In this retrospectivecross-sectional investigation blood samples were taken from all malaria suspicious cases who were referred to health centers acrossKhuzestan province For each positive subject a questionnaire containing demographic information was filled out Data analysiswas performed using SPSS 18 From a total of 541 malaria confirmed cases 498 (9205) were male and 43 (795) were femaleThehighest number of infections was seen in 2001 with 161 (2975) cases and the lowest was in 2014 with 0 (0) Also Plasmodiumvivaxwas identified as dominant species in 478 (8835) individuals and P falciparum comprised 63 (1165)The highest infectionrate was observed in non-Iranian populations with number 459 (8485) and imported cases 508 (9390) Also the majority ofsubjects were over 15 years of age 458 (8465) Due to proximity to endemic countries which has made the malaria campaigndifficult more effort is needed to control the infection in order to achieve malaria elimination
1 Introduction
Malaria is one of the most important infectious diseasesespecially in tropical and subtropical areas of the world where33 billion individuals in about 106 countries live at riskApproximately 200ndash300 million people worldwide becomeinfected annually and totally 06ndash1 million individuals losetheir lives most of them children under 5 years of age andpregnant women Malaria is often transmitted through thebite of female Anopheles mosquitoes from one person toanother Other transmission routes include blood transfu-sion transfer through the placenta (in the acute stage ofinfection from mother to fetus) and organ transplantation[1]
Despite considerable progress in the past decadesmalariais still considered a major public health concern in someareas Malaria in certain regions such as sub-Saharan AfricaThailand and India is very prevalent and comprises approxi-mately 95 of totalmalaria cases throughout theworld [2] Inthe Eastern Mediterranean Region (EMR) on average morethan 10 million clinical cases of malaria occur annually ofwhich nearly 50000 cases lead to death 60 of the EMRpopulations (287 million people) are at risk [3] EMR coun-tries based on malaria control program and disease statusare classified into three groups the first group countries thathave achieved complete cessation of transmission of malariaincluding Lebanon Cyprus Palestine Jordan Qatar Libya
Hindawi Publishing CorporationJournal of Tropical MedicineVolume 2015 Article ID 523767 6 pageshttpdxdoiorg1011552015523767
2 Journal of Tropical Medicine
Central Asia
Produced by the cartographic research labUniveristy of Alabama
Figure 1 Location of Khuzestan province in Iran (in the southwest of Iran)
Bahrain Tunisia and Kuwait and also countries where trans-mission is limited to small regions and is undermalaria elimi-nation program including Egypt Morocco Oman Syria andthe United Arabic Emirates (UAE) the second group coun-tries with intermediate endemicity including Iran and SaudiArabia the third group countries with extreme transmissionof malaria such as Afghanistan Pakistan Yemen Somaliaand Sudan [2] In addition to climate other factors such asresidence personal and social lifestyle cultural and economicstatus of the region number of enteredmigrants to the regionand quantity and quality of malaria control programs in theregion hamper the outbreak and spread of malaria [4]
In 1945 the first malaria-training course for preliminaryoperations of antimalarial campaign was initiated Then in1947 for the first time DDT was employed in order tocontrol vectors in hyperendemic villages of Varamin citywhich led to dramatic reduction in malaria transmissionAfterward antimalarial campaign was followed during 1948ndash1956 including antimosquito spraying with DDT antilarvalcontrol measures drug prophylaxis and treatment Eventu-ally in 1957 malaria eradication program was started aroundIran and continued till now [5] During recent years asignificant declining trend has been observed in the rateof malaria incidence throughout Iran Based on the 2009World Health Organization (WHO) malaria report Iran isin pre-elimination phase Cessation of local transmission ofmalaria in 2025 is the ultimate goal of themalaria eliminationprogram in Iran [6] Based on conducted studies in IranP vivax has been identified as the major species and Pfalciparum is more limited to the east and southeast ofthe country [6 7] The south and southeast of Iran areconsidered as malaria endemic zones and the provinces ofSistan-Baluchestan Hormozgan and Kerman with AnnualParasite Incidence (API) between 1 and 8 per 1000 populationconstitute approximately 95 of total cases 60 of whichwere allocated to Sistan-Baluchestan province [3]
An Sacharovi An dthali and An Stephensi are identifiedas definite vectors of malaria in Khuzestan province [8]
Khuzestan province is considered as a Free Trade Zone(FTZ) and agricultural center in Iran and a considerablenumber of workers are continually deployed to this provinceThis province due to its special geographical characteristicsand situation is considered as an immigration zone and insome seasons of the year receives several million touristsand pilgrims Also due to its proximity to Iraq traffic fromforeign nationals is observed throughout the year All of thesereasons put this province at risk thus the aimof present studywas to evaluate the epidemiological status of malaria diseasebetween 2001 and 2014 in the southwest of Iran Khuzestanprovince
2 Materials and Methods
21 Study Area This epidemiological study was performedin Khuzestan province southwestern Iran located within29∘571015840ndash33∘01015840N latitude and 47∘401015840ndash50∘331015840E longitude with anarea about 64055 km2 This province with a population of4531720 inhabitants (2286209 male and 2245511 female)is bordered by Iraq in the west Chahar Mahal and Bakhtiariand Kohgiluyeh and Boyer-Ahmad provinces in the east andnortheast Lorestan province in the north Bushehr provincein the southeast and the Persian Gulf in the south (Figure 1)
22 Data Collection Between 2001 and 2014 from all suspi-cious malaria subjects who were referred to health centersacross Khuzestan province blood sample was taken bysterile lancet Afterward one drop of blood was placed ona microscopic slide in order to prepare peripheral bloodsmears Peripheral blood smear after staining by Giemsa wasexamined by optical microscope in order to detect parasiteA questionnaire including some demographic details suchas name gender age residence nationality (Iranian or non-Iranian) causative agent (P vivax P falciparum) type oftransmission (imported or indigenous) and other detailswas completed for each positive subject Eventually all datawere gathered from all health centers throughout Khuzestan
Journal of Tropical Medicine 3
TotalP vivaxP falciparum
2002
2003
2004
2005
2006
2007
2008
2009
2010
2011
2012
2013
2014
2001
Year
020406080
100120140160180
Freq
uenc
y
Figure 2 Trend of malaria disease during 2001ndash2014
province and data were analyzed using SPSS software version18 (SPSS Inc Chicago IL USA)
3 Results
Trend of malaria during the past decade in Khuzestanprovince has dramatically slumped (Figure 2) The highestnumber of infections was seen in 2001 with 161 (2975)cases and the lowest was in 2014 with 0 (0) From atotal of 541 malaria confirmed cases during 2001ndash2014 498(9205) were male and 43 (795) were female P vivaxwas the predominant species in 478 (8835) individualsand P falciparum species comprised 63 (1165) Proportionof infection in different age groups of 0ndash5 5ndash15 and gt15years of age was 26 (481) 57 (1054) and 458 (8465)respectively Rate of malaria disease in Iranian and non-Iranian populations was found to be 82 (1515) and 459(8485) respectively Also number of imported cases was508 (9390) and the number of indigenous cases was 33(610) (Table 1) Our finding revealed that Ahvaz city (cap-ital of Khuzestan province) with 168 (3105) positive caseswas in the first rank Behbahan county with 158 (2920) wassecond andAndimeshkwith 42 (776) was third InDehdezand Haftkel counties no positive cases were reported duringthe years 2001ndash2014 (Figure 3) Highest and lowest API were004709 in 2001 and 0 in 2014 respectively (Table 1)
4 Discussion
Malaria in developing countries and tropical regions has beenof special importance historically [1] It was estimated in 1924that out of 13 million people who live in Iran 4-5 million ofthem became infected with malaria and 30ndash40 of the totaldeaths were allocated to this infection Also 75 of the totalIranian population lived in endemic and hyperendemic areasAt the same time one-third of the budget of the Ministryof Health (MoH) was spent to buy the quinine drug In1924 in Tehran 20 of patients referred to dispensaries hadmalaria Also in 1924 535 of all people who lived in Aras
5
42
168
8 13 6
158
419
020
38
2
3211
014
1020406080
100120140160180
Freq
uenc
y
Das
hte-
Aza
dega
n
Mas
jed
Sole
yman
Shad
egan
Shou
shta
r
Behb
ahan
Kho
rram
shah
rM
ahsh
ahr
Bagh
mal
ek
Ram
horm
oz
Hov
eize
h
And
imes
hk
Om
idiy
eh
Abad
an
Deh
dez
Hen
dija
n
Haft
kel
Ahv
az
Izeh
City
Figure 3 Distribution of malaria infection in different counties ofKhuzestan province
river area were diagnosed with malaria and 415 of alldeaths in this region are allocated to this infection [5] In arecent study it has been reported that the annual incidenceof malaria cases in Iran declined significantly from 66075to 3200 between 1995 and 2012 [9] Epidemiological studieshave shown that malaria in Iran unlike Africa and othercountries is dependent on climatic conditions This meansthat the unstable situation with rainfall increase may lead toincrease in the incidence of disease in high-risk areas [5 6]
In this study the trend of malaria disease and its epi-demiological features was surveyed between 2001 and 2014The findings revealed that the rate of infection as a resultof malaria campaign has a continuous decreasing trend sothat the frequency from 161 in 2001 fell down to 0 in theend of 2014 in the southwest of Iran Khuzestan provinceBased on current findings imported cases and non-Iranianpatients were found to be 9390 and 8485 respectivelyBecause of existence of Free Trade Zone (FTZ) the harborregion and high financial activities in this province manymerchants investors and workers from different regions aredeployed to these areas annually Also this province is atouristic and pilgrimage zone where several thousands ofpassengers from Iraq country located at the west of Irancommute from Khuzestan province annually and this issuecould be a reason for high frequency of infection Salvadoet al in Spain reported that the main cause of malaria insubjects is migration of the passengers to endemic countries[10] In another study conducted by Mascarello et al in Italyduring 1990ndash1998 the number of malaria cases was shown tohave increased by 100 and the main causes of this increasewere commute and immigration from endemic areas to thecountry [11] Also based on Iqbal et alrsquos study the rate ofmalaria infection among immigrants to Kuwait was observedto be 23 [12] Population movements in malaria endemiczones and the lack of adequate intervention lead to increasingthe risk of malaria For instance Iran in recent years hashosted approximately 2millionAfghan refugees and unfortu-nately these refugees have created many serious problems in
4 Journal of Tropical Medicine
Table1Ep
idem
iologicalfactorsof
malariain
Khu
zestan
province
durin
g2001ndash2014
Year
Total
APIlowast
Causativea
gent
(119899)
Gender(119899)
Age
(119899)
Type
oftransm
ission(119899)
Nationality(119899)
119875Vlowastlowast
119875119891lowastlowastlowast
Male
Female
0ndash5
5ndash15
gt15
Indigeno
usIm
ported
Iranian
Non
-Iranian
2001
161
004709
142
19151
108
21132
8153
18143
2002
91002617
910
838
82
811
907
842003
62001742
557
584
26
543
5912
502004
69001922
5910
654
25
626
638
612005
25000
678
232
241
03
220
256
192006
25000
685
214
232
15
190
255
202007
33000
903
285
303
23
281
326
272008
44001165
3410
368
16
378
3611
332009
12000321
111
93
13
81
112
102010
6000155
51
60
00
60
61
52011
3000
075
30
30
11
10
32
12012
5000124
32
50
00
55
03
22013
5000124
32
50
02
30
51
42014
00
00
00
00
00
00
0To
tal119899
()
541(100)
478(8835)
63(116
5)498(9205)
43(795)
26(481)
57(1054)
458(8465)
33(610
)508(9390)
82(1515)
459(8485)
lowast
APIA
nnualP
arasite
Incidence=
totaln
umbero
fpositive
slidesfor
parasiteinay
eartimes
1000to
talp
opulation
lowastlowast
119875v
Plasmodium
vivax
lowastlowastlowast
119875f
Plasmodium
falciparum
Journal of Tropical Medicine 5
malaria control program in our country Entering and trafficof Afghan and Pakistani immigrants to Iran were continuedeven though Afghanistan and Pakistan are considered ashighly dangerous transferors of malaria [6] Some reportshave documented this issue such as Soleimanifard et al[13] in Isfahan province (91 and 56 of total positivecases belonged toAfghan immigrants and other nationalitiesresp) Saghafipour et al [14] inQomprovince (915) Khaliliet al [15] in Yazd province (773 in Afghan refugees) andZia-Sheikholeslami and Rezaeian [16] in Rafsanjan county(989 in Afghan refugees)
Current investigation indicated that the number ofmalaria patients in Khuzestan province southwest Iranduring the past years has dropped significantly and API inthis province ranged from 004709 in 2001 to 0 in 2014 whichreflects the success in achieving and reaching the malariacontrol program in this province Our finding was similarto results gained from Sarafraz et al [17] in East Azerbaijanprovince and Ghaffari et al [18] in Mazandaran provinceIn the present investigation the rate of infection in maleswas 9205which is consistent with other surveys conductedin Isfahan province [13] (935) Mazandaran province [19](884) and East Azerbaijan province [17] (8646) Alsoin some surveys the ratio of both genders was equal andno significant differences were seen between them suchas Alemu et al [20] in Ethiopia (526 male and 474female) and Barak et al [21] in Ardabil province during 2001ndash2010 (45 male and 55 female) However gender is notinvolved directly and naturally in sensitivity and resistance tomalaria but may be correlated with job type of coating andcultural habits Also social activities and attendance of menin the workplaces outdoors make them more susceptible tomosquito bites and becoming infected
In the present investigation it was demonstrated that Pvivax is the most common species (8835) among malariasubjects which is in agreementwith general pattern of diseasein Iran [13 14 17 22] According to the fact that P vivaxcould relapse due to presence of liver hypnozoites thesepatients should be identified and treated In our study thehighest number was observed in persons over 15 years ofage (8465) which is in agreement with the results ofstudies like Saghafipour et al [14] in Qom province (662)Soleimanifard et al [13] in Isfahan province and Bafghi et al[23] in Yazd province Presence of infected individuals as dis-ease reservoirs and Anopheles mosquitoes as carriers has animportant role in epidemiological status and spread of diseasein endemic regions thus existence of these factors will helpin the transmission of malaria and lead to unstable situationIt should be noted that despite the significant reduction ofmalaria cases in Khuzestan province the hot and humidclimate of the province presence of the Karoun MarounKarkheh Kheirabad and Dez rivers and the arable landsurrounding these rivers provide a favorable environmentalcondition for anopheline mosquitoes larvae developmentEvidence shows that malaria control programs with theparticipation of people in society aremore effective comparedwith those programs that are only designed and implementedby governments therefore awareness attitudes and behaviorof people who live in endemic and hyperendemic areas can be
more effective in planning for the control and prevention ofmalaria [1 2 6 13]
As rapid treatment of infected patients either Iranian orforeign subjects some interventions such as antimosquitospraying and antilarval controlmeasures are being carried outin order to eliminate infection throughout the province andof course in Iran Further surveys like spatial studies in orderto determine manage and analyze epidemiological featuresusing Geographic Information System (GIS) in Khuzestanprovince are necessary
5 Conclusions
Number of malaria patients during 2001ndash2014 was decreasedsignificantly in the southwest of Iran Khuzestan provinceUnfortunately as it was mentioned before proximity withendemic countries like Iraq Afghanistan and Pakistan hasmade the malaria control program more difficult Existenceof infected people and vectors in the region contributes tothe spread of disease around Khuzestan province Accordingto the specific climatic status in Khuzestan province theoptimum conditions exist for the growth of the Anophelesmosquitoes thus the risk ofmalaria epidemics and incidenceof severe cases should be considered constantly Accordinglymalaria control programs should be continued until diseaseelimination
Conflict of Interests
The authors declare no conflict of interests
Authorsrsquo Contribution
All authors had equal role in design work statistical analysisand writing of the paper
Acknowledgments
This study was financially supported by Student ResearchCommittee of Ahvaz Jundishapur University of MedicalScience Iran (no 93S88) The authors would like to thankall staff at the health care centers in Khuzestan ProvinceAlso the authors sincerely acknowledge their gratitude to theefforts of Center for Disease Control in Ahvaz JundishapurUniversity of Medical Sciences
References
[1] G R L Del Prado C H Garcıa L M Cea et al ldquoMalariain developing countriesrdquo Journal of Infection in DevelopingCountries vol 8 no 1 pp 1ndash4 2014
[2] R Bhatia R M Rastogi and L Ortega ldquoMalaria successes andchallenges in Asiardquo Journal of Vector Borne Diseases vol 50 no4 pp 239ndash247 2013
[3] A Raeisi M M Gouya A Nadim et al ldquoDeterminationof malaria epidemiological status in Iranrsquos malarious areas asbaseline information for implementation ofmalaria eliminationprogram in Iranrdquo Iranian Journal of Public Health vol 42 no 3pp 326ndash333 2013
6 Journal of Tropical Medicine
[4] M Halimi M Delavari and A Takhtardeshir ldquoSurvey ofclimatic condition of Malaria disease outbreak in Iran usingGISrdquo Journal of School of Public Health and Institute of PublicHealth Research vol 10 no 3 pp 41ndash52 2013
[5] G Edrissian ldquoMalaria in Iran past and present situationrdquoIranian Journal of Parasitology vol 1 no 1 pp 1ndash14 2006
[6] M R Hemami A A Sari A Raeisi H Vatandoost andR Majdzadeh ldquoMalaria elimination in Iran importance andchallengesrdquo International Journal of Preventive Medicine vol 4no 1 pp 88ndash94 2013
[7] A-A Haghdoost N Alexander and J Cox ldquoModelling ofmalaria temporal variations in Iranrdquo Tropical Medicine ampInternational Health vol 13 no 12 pp 1501ndash1508 2008
[8] A Salahi-MoghadamA KhoshdelM Barati andM SedaghatldquoAn overview and mapping of Malaria and its vectors in IranrdquoHormozgan Medical Journal vol 18 no 5 pp 473ndash485 2014
[9] A R Mesdaghinia H Vatandoost A A Hanafi-Bojd RMajdzadeh and A Raeisi ldquoConducting international diplomacourse on malaria program planning and management (1996ndash2012)rdquo Journal of Arthropod-Borne Diseases vol 7 no 2 pp100ndash112 2013
[10] E Salvado M J Pinazo J Munoz et al ldquoClinical presentationand complications of Plasmodium falciparum malaria in twopopulations travelers and immigrantsrdquo Enfermedades Infec-ciosas y Microbiologia Clinica vol 26 no 5 pp 282ndash284 2008
[11] M Mascarello B Allegranzi A Angheben et al ldquoImportedmalaria in adults and children epidemiological and clinicalcharacteristics of 380 consecutive cases observed in VeronaItalyrdquo Journal of Travel Medicine vol 15 no 4 pp 229ndash2362008
[12] J Iqbal A Sher P R Hira and R Al-Owaish ldquoComparisonof the OptiMAL test with PCR for diagnosis of malaria inimmigrantsrdquo Journal of Clinical Microbiology vol 37 no 11 pp3644ndash3646 1999
[13] S Soleimanifard M Akbari M Sabetghadam and S SaberildquoMalaria situation in Isfahan in the last five yearsrdquo Journal ofIsfahan Medical School vol 29 no 132 pp 273ndash280 2011
[14] A Saghafipour M Noroozi M Karami-Jooshin and P AbbasldquoEpidemiological features of Malaria in Qom Province from2001 to 2011rdquo Zahedan Journal of Research in Medical Sciencesvol 14 no 8 pp 70ndash73 2012
[15] M B Khalili M Anvari-Tafti and M Sadeh ldquoEpidemiologicalpattern of malarial disease in the province of Yazd Iran (Since1986-2006)rdquoWorld Journal of Medical Sciences vol 4 no 1 pp41ndash45 2009
[16] N Zia-Sheikholeslami andM Rezaeian ldquoThe retrospective epi-demiological study of Malaria in Rafsanjan Kerman provincefrom 1999 to 2005rdquo Persian Health Journal of Ardebil vol 1 no1 pp 24ndash30 2010
[17] S Sarafraz N G Mehrabani Y Mirzaei et al ldquoEpidemiologyof malaria in East Azerbaijan province Iran from 2001 to 2013rdquoJournal of Parasitic Diseases pp 1ndash5 2014
[18] S Ghaffari S A Mahdavi Z Moulana et al ldquoMalaria inMazandaran northern Iran passive case finding during 1997ndash2012rdquo Iranian Journal of Parasitology vol 7 no 3 pp 82ndash882012
[19] N Najafi R Ghasemian andM Farahmand ldquoEpidemiology ofMalaria in Mazandaran province during 1999ndash2003rdquo Journal ofMazandaran University of Medical Sciences vol 15 no 50 pp125ndash132 2006
[20] A Alemu DMuluye MMihret M Adugna andM GebeyawldquoTen year trend analysis of malaria prevalence in Kola DibaNorth Gondar Northwest Ethiopiardquo Parasites amp Vectors vol 5no 1 article 173 2012
[21] M Barak L Mottaghinia D Emdadi et al ldquoInvestigation ofa ten-year trend of local transmission of Malaria (Plasmodiumvivax) in endemic region of Ardabil province (Parsabad Dis-trict) from 2001 to 2010rdquo in Proceedings of the InternationalCongress on Malaria Elimination Kish Island Iran 2012
[22] N Sargolzaie M Salehi M Kiani et al ldquoMalaria epidemiologyin Sistan and Balouchestan province during April 2008ndashMarch2011 Iranrdquo Zahedan Journal of Research inMedical Sciences vol16 no 4 pp 41ndash43 2014
[23] A F Bafghi S Pourmazar and F Shamsi ldquoFive-year statusof Malaria (a disease causing Anemia) in Yazd 2008ndash2012rdquoIranian Journal of Pediatric Hematology Oncology vol 3 no 3pp 91ndash96 2013
Produced by the cartographic research labUniveristy of Alabama
Figure 1 Location of Khuzestan province in Iran (in the southwest of Iran)
Bahrain Tunisia and Kuwait and also countries where trans-mission is limited to small regions and is undermalaria elimi-nation program including Egypt Morocco Oman Syria andthe United Arabic Emirates (UAE) the second group coun-tries with intermediate endemicity including Iran and SaudiArabia the third group countries with extreme transmissionof malaria such as Afghanistan Pakistan Yemen Somaliaand Sudan [2] In addition to climate other factors such asresidence personal and social lifestyle cultural and economicstatus of the region number of enteredmigrants to the regionand quantity and quality of malaria control programs in theregion hamper the outbreak and spread of malaria [4]
In 1945 the first malaria-training course for preliminaryoperations of antimalarial campaign was initiated Then in1947 for the first time DDT was employed in order tocontrol vectors in hyperendemic villages of Varamin citywhich led to dramatic reduction in malaria transmissionAfterward antimalarial campaign was followed during 1948ndash1956 including antimosquito spraying with DDT antilarvalcontrol measures drug prophylaxis and treatment Eventu-ally in 1957 malaria eradication program was started aroundIran and continued till now [5] During recent years asignificant declining trend has been observed in the rateof malaria incidence throughout Iran Based on the 2009World Health Organization (WHO) malaria report Iran isin pre-elimination phase Cessation of local transmission ofmalaria in 2025 is the ultimate goal of themalaria eliminationprogram in Iran [6] Based on conducted studies in IranP vivax has been identified as the major species and Pfalciparum is more limited to the east and southeast ofthe country [6 7] The south and southeast of Iran areconsidered as malaria endemic zones and the provinces ofSistan-Baluchestan Hormozgan and Kerman with AnnualParasite Incidence (API) between 1 and 8 per 1000 populationconstitute approximately 95 of total cases 60 of whichwere allocated to Sistan-Baluchestan province [3]
An Sacharovi An dthali and An Stephensi are identifiedas definite vectors of malaria in Khuzestan province [8]
Khuzestan province is considered as a Free Trade Zone(FTZ) and agricultural center in Iran and a considerablenumber of workers are continually deployed to this provinceThis province due to its special geographical characteristicsand situation is considered as an immigration zone and insome seasons of the year receives several million touristsand pilgrims Also due to its proximity to Iraq traffic fromforeign nationals is observed throughout the year All of thesereasons put this province at risk thus the aimof present studywas to evaluate the epidemiological status of malaria diseasebetween 2001 and 2014 in the southwest of Iran Khuzestanprovince
2 Materials and Methods
21 Study Area This epidemiological study was performedin Khuzestan province southwestern Iran located within29∘571015840ndash33∘01015840N latitude and 47∘401015840ndash50∘331015840E longitude with anarea about 64055 km2 This province with a population of4531720 inhabitants (2286209 male and 2245511 female)is bordered by Iraq in the west Chahar Mahal and Bakhtiariand Kohgiluyeh and Boyer-Ahmad provinces in the east andnortheast Lorestan province in the north Bushehr provincein the southeast and the Persian Gulf in the south (Figure 1)
22 Data Collection Between 2001 and 2014 from all suspi-cious malaria subjects who were referred to health centersacross Khuzestan province blood sample was taken bysterile lancet Afterward one drop of blood was placed ona microscopic slide in order to prepare peripheral bloodsmears Peripheral blood smear after staining by Giemsa wasexamined by optical microscope in order to detect parasiteA questionnaire including some demographic details suchas name gender age residence nationality (Iranian or non-Iranian) causative agent (P vivax P falciparum) type oftransmission (imported or indigenous) and other detailswas completed for each positive subject Eventually all datawere gathered from all health centers throughout Khuzestan
Journal of Tropical Medicine 3
TotalP vivaxP falciparum
2002
2003
2004
2005
2006
2007
2008
2009
2010
2011
2012
2013
2014
2001
Year
020406080
100120140160180
Freq
uenc
y
Figure 2 Trend of malaria disease during 2001ndash2014
province and data were analyzed using SPSS software version18 (SPSS Inc Chicago IL USA)
3 Results
Trend of malaria during the past decade in Khuzestanprovince has dramatically slumped (Figure 2) The highestnumber of infections was seen in 2001 with 161 (2975)cases and the lowest was in 2014 with 0 (0) From atotal of 541 malaria confirmed cases during 2001ndash2014 498(9205) were male and 43 (795) were female P vivaxwas the predominant species in 478 (8835) individualsand P falciparum species comprised 63 (1165) Proportionof infection in different age groups of 0ndash5 5ndash15 and gt15years of age was 26 (481) 57 (1054) and 458 (8465)respectively Rate of malaria disease in Iranian and non-Iranian populations was found to be 82 (1515) and 459(8485) respectively Also number of imported cases was508 (9390) and the number of indigenous cases was 33(610) (Table 1) Our finding revealed that Ahvaz city (cap-ital of Khuzestan province) with 168 (3105) positive caseswas in the first rank Behbahan county with 158 (2920) wassecond andAndimeshkwith 42 (776) was third InDehdezand Haftkel counties no positive cases were reported duringthe years 2001ndash2014 (Figure 3) Highest and lowest API were004709 in 2001 and 0 in 2014 respectively (Table 1)
4 Discussion
Malaria in developing countries and tropical regions has beenof special importance historically [1] It was estimated in 1924that out of 13 million people who live in Iran 4-5 million ofthem became infected with malaria and 30ndash40 of the totaldeaths were allocated to this infection Also 75 of the totalIranian population lived in endemic and hyperendemic areasAt the same time one-third of the budget of the Ministryof Health (MoH) was spent to buy the quinine drug In1924 in Tehran 20 of patients referred to dispensaries hadmalaria Also in 1924 535 of all people who lived in Aras
5
42
168
8 13 6
158
419
020
38
2
3211
014
1020406080
100120140160180
Freq
uenc
y
Das
hte-
Aza
dega
n
Mas
jed
Sole
yman
Shad
egan
Shou
shta
r
Behb
ahan
Kho
rram
shah
rM
ahsh
ahr
Bagh
mal
ek
Ram
horm
oz
Hov
eize
h
And
imes
hk
Om
idiy
eh
Abad
an
Deh
dez
Hen
dija
n
Haft
kel
Ahv
az
Izeh
City
Figure 3 Distribution of malaria infection in different counties ofKhuzestan province
river area were diagnosed with malaria and 415 of alldeaths in this region are allocated to this infection [5] In arecent study it has been reported that the annual incidenceof malaria cases in Iran declined significantly from 66075to 3200 between 1995 and 2012 [9] Epidemiological studieshave shown that malaria in Iran unlike Africa and othercountries is dependent on climatic conditions This meansthat the unstable situation with rainfall increase may lead toincrease in the incidence of disease in high-risk areas [5 6]
In this study the trend of malaria disease and its epi-demiological features was surveyed between 2001 and 2014The findings revealed that the rate of infection as a resultof malaria campaign has a continuous decreasing trend sothat the frequency from 161 in 2001 fell down to 0 in theend of 2014 in the southwest of Iran Khuzestan provinceBased on current findings imported cases and non-Iranianpatients were found to be 9390 and 8485 respectivelyBecause of existence of Free Trade Zone (FTZ) the harborregion and high financial activities in this province manymerchants investors and workers from different regions aredeployed to these areas annually Also this province is atouristic and pilgrimage zone where several thousands ofpassengers from Iraq country located at the west of Irancommute from Khuzestan province annually and this issuecould be a reason for high frequency of infection Salvadoet al in Spain reported that the main cause of malaria insubjects is migration of the passengers to endemic countries[10] In another study conducted by Mascarello et al in Italyduring 1990ndash1998 the number of malaria cases was shown tohave increased by 100 and the main causes of this increasewere commute and immigration from endemic areas to thecountry [11] Also based on Iqbal et alrsquos study the rate ofmalaria infection among immigrants to Kuwait was observedto be 23 [12] Population movements in malaria endemiczones and the lack of adequate intervention lead to increasingthe risk of malaria For instance Iran in recent years hashosted approximately 2millionAfghan refugees and unfortu-nately these refugees have created many serious problems in
4 Journal of Tropical Medicine
Table1Ep
idem
iologicalfactorsof
malariain
Khu
zestan
province
durin
g2001ndash2014
Year
Total
APIlowast
Causativea
gent
(119899)
Gender(119899)
Age
(119899)
Type
oftransm
ission(119899)
Nationality(119899)
119875Vlowastlowast
119875119891lowastlowastlowast
Male
Female
0ndash5
5ndash15
gt15
Indigeno
usIm
ported
Iranian
Non
-Iranian
2001
161
004709
142
19151
108
21132
8153
18143
2002
91002617
910
838
82
811
907
842003
62001742
557
584
26
543
5912
502004
69001922
5910
654
25
626
638
612005
25000
678
232
241
03
220
256
192006
25000
685
214
232
15
190
255
202007
33000
903
285
303
23
281
326
272008
44001165
3410
368
16
378
3611
332009
12000321
111
93
13
81
112
102010
6000155
51
60
00
60
61
52011
3000
075
30
30
11
10
32
12012
5000124
32
50
00
55
03
22013
5000124
32
50
02
30
51
42014
00
00
00
00
00
00
0To
tal119899
()
541(100)
478(8835)
63(116
5)498(9205)
43(795)
26(481)
57(1054)
458(8465)
33(610
)508(9390)
82(1515)
459(8485)
lowast
APIA
nnualP
arasite
Incidence=
totaln
umbero
fpositive
slidesfor
parasiteinay
eartimes
1000to
talp
opulation
lowastlowast
119875v
Plasmodium
vivax
lowastlowastlowast
119875f
Plasmodium
falciparum
Journal of Tropical Medicine 5
malaria control program in our country Entering and trafficof Afghan and Pakistani immigrants to Iran were continuedeven though Afghanistan and Pakistan are considered ashighly dangerous transferors of malaria [6] Some reportshave documented this issue such as Soleimanifard et al[13] in Isfahan province (91 and 56 of total positivecases belonged toAfghan immigrants and other nationalitiesresp) Saghafipour et al [14] inQomprovince (915) Khaliliet al [15] in Yazd province (773 in Afghan refugees) andZia-Sheikholeslami and Rezaeian [16] in Rafsanjan county(989 in Afghan refugees)
Current investigation indicated that the number ofmalaria patients in Khuzestan province southwest Iranduring the past years has dropped significantly and API inthis province ranged from 004709 in 2001 to 0 in 2014 whichreflects the success in achieving and reaching the malariacontrol program in this province Our finding was similarto results gained from Sarafraz et al [17] in East Azerbaijanprovince and Ghaffari et al [18] in Mazandaran provinceIn the present investigation the rate of infection in maleswas 9205which is consistent with other surveys conductedin Isfahan province [13] (935) Mazandaran province [19](884) and East Azerbaijan province [17] (8646) Alsoin some surveys the ratio of both genders was equal andno significant differences were seen between them suchas Alemu et al [20] in Ethiopia (526 male and 474female) and Barak et al [21] in Ardabil province during 2001ndash2010 (45 male and 55 female) However gender is notinvolved directly and naturally in sensitivity and resistance tomalaria but may be correlated with job type of coating andcultural habits Also social activities and attendance of menin the workplaces outdoors make them more susceptible tomosquito bites and becoming infected
In the present investigation it was demonstrated that Pvivax is the most common species (8835) among malariasubjects which is in agreementwith general pattern of diseasein Iran [13 14 17 22] According to the fact that P vivaxcould relapse due to presence of liver hypnozoites thesepatients should be identified and treated In our study thehighest number was observed in persons over 15 years ofage (8465) which is in agreement with the results ofstudies like Saghafipour et al [14] in Qom province (662)Soleimanifard et al [13] in Isfahan province and Bafghi et al[23] in Yazd province Presence of infected individuals as dis-ease reservoirs and Anopheles mosquitoes as carriers has animportant role in epidemiological status and spread of diseasein endemic regions thus existence of these factors will helpin the transmission of malaria and lead to unstable situationIt should be noted that despite the significant reduction ofmalaria cases in Khuzestan province the hot and humidclimate of the province presence of the Karoun MarounKarkheh Kheirabad and Dez rivers and the arable landsurrounding these rivers provide a favorable environmentalcondition for anopheline mosquitoes larvae developmentEvidence shows that malaria control programs with theparticipation of people in society aremore effective comparedwith those programs that are only designed and implementedby governments therefore awareness attitudes and behaviorof people who live in endemic and hyperendemic areas can be
more effective in planning for the control and prevention ofmalaria [1 2 6 13]
As rapid treatment of infected patients either Iranian orforeign subjects some interventions such as antimosquitospraying and antilarval controlmeasures are being carried outin order to eliminate infection throughout the province andof course in Iran Further surveys like spatial studies in orderto determine manage and analyze epidemiological featuresusing Geographic Information System (GIS) in Khuzestanprovince are necessary
5 Conclusions
Number of malaria patients during 2001ndash2014 was decreasedsignificantly in the southwest of Iran Khuzestan provinceUnfortunately as it was mentioned before proximity withendemic countries like Iraq Afghanistan and Pakistan hasmade the malaria control program more difficult Existenceof infected people and vectors in the region contributes tothe spread of disease around Khuzestan province Accordingto the specific climatic status in Khuzestan province theoptimum conditions exist for the growth of the Anophelesmosquitoes thus the risk ofmalaria epidemics and incidenceof severe cases should be considered constantly Accordinglymalaria control programs should be continued until diseaseelimination
Conflict of Interests
The authors declare no conflict of interests
Authorsrsquo Contribution
All authors had equal role in design work statistical analysisand writing of the paper
Acknowledgments
This study was financially supported by Student ResearchCommittee of Ahvaz Jundishapur University of MedicalScience Iran (no 93S88) The authors would like to thankall staff at the health care centers in Khuzestan ProvinceAlso the authors sincerely acknowledge their gratitude to theefforts of Center for Disease Control in Ahvaz JundishapurUniversity of Medical Sciences
References
[1] G R L Del Prado C H Garcıa L M Cea et al ldquoMalariain developing countriesrdquo Journal of Infection in DevelopingCountries vol 8 no 1 pp 1ndash4 2014
[2] R Bhatia R M Rastogi and L Ortega ldquoMalaria successes andchallenges in Asiardquo Journal of Vector Borne Diseases vol 50 no4 pp 239ndash247 2013
[3] A Raeisi M M Gouya A Nadim et al ldquoDeterminationof malaria epidemiological status in Iranrsquos malarious areas asbaseline information for implementation ofmalaria eliminationprogram in Iranrdquo Iranian Journal of Public Health vol 42 no 3pp 326ndash333 2013
6 Journal of Tropical Medicine
[4] M Halimi M Delavari and A Takhtardeshir ldquoSurvey ofclimatic condition of Malaria disease outbreak in Iran usingGISrdquo Journal of School of Public Health and Institute of PublicHealth Research vol 10 no 3 pp 41ndash52 2013
[5] G Edrissian ldquoMalaria in Iran past and present situationrdquoIranian Journal of Parasitology vol 1 no 1 pp 1ndash14 2006
[6] M R Hemami A A Sari A Raeisi H Vatandoost andR Majdzadeh ldquoMalaria elimination in Iran importance andchallengesrdquo International Journal of Preventive Medicine vol 4no 1 pp 88ndash94 2013
[7] A-A Haghdoost N Alexander and J Cox ldquoModelling ofmalaria temporal variations in Iranrdquo Tropical Medicine ampInternational Health vol 13 no 12 pp 1501ndash1508 2008
[8] A Salahi-MoghadamA KhoshdelM Barati andM SedaghatldquoAn overview and mapping of Malaria and its vectors in IranrdquoHormozgan Medical Journal vol 18 no 5 pp 473ndash485 2014
[9] A R Mesdaghinia H Vatandoost A A Hanafi-Bojd RMajdzadeh and A Raeisi ldquoConducting international diplomacourse on malaria program planning and management (1996ndash2012)rdquo Journal of Arthropod-Borne Diseases vol 7 no 2 pp100ndash112 2013
[10] E Salvado M J Pinazo J Munoz et al ldquoClinical presentationand complications of Plasmodium falciparum malaria in twopopulations travelers and immigrantsrdquo Enfermedades Infec-ciosas y Microbiologia Clinica vol 26 no 5 pp 282ndash284 2008
[11] M Mascarello B Allegranzi A Angheben et al ldquoImportedmalaria in adults and children epidemiological and clinicalcharacteristics of 380 consecutive cases observed in VeronaItalyrdquo Journal of Travel Medicine vol 15 no 4 pp 229ndash2362008
[12] J Iqbal A Sher P R Hira and R Al-Owaish ldquoComparisonof the OptiMAL test with PCR for diagnosis of malaria inimmigrantsrdquo Journal of Clinical Microbiology vol 37 no 11 pp3644ndash3646 1999
[13] S Soleimanifard M Akbari M Sabetghadam and S SaberildquoMalaria situation in Isfahan in the last five yearsrdquo Journal ofIsfahan Medical School vol 29 no 132 pp 273ndash280 2011
[14] A Saghafipour M Noroozi M Karami-Jooshin and P AbbasldquoEpidemiological features of Malaria in Qom Province from2001 to 2011rdquo Zahedan Journal of Research in Medical Sciencesvol 14 no 8 pp 70ndash73 2012
[15] M B Khalili M Anvari-Tafti and M Sadeh ldquoEpidemiologicalpattern of malarial disease in the province of Yazd Iran (Since1986-2006)rdquoWorld Journal of Medical Sciences vol 4 no 1 pp41ndash45 2009
[16] N Zia-Sheikholeslami andM Rezaeian ldquoThe retrospective epi-demiological study of Malaria in Rafsanjan Kerman provincefrom 1999 to 2005rdquo Persian Health Journal of Ardebil vol 1 no1 pp 24ndash30 2010
[17] S Sarafraz N G Mehrabani Y Mirzaei et al ldquoEpidemiologyof malaria in East Azerbaijan province Iran from 2001 to 2013rdquoJournal of Parasitic Diseases pp 1ndash5 2014
[18] S Ghaffari S A Mahdavi Z Moulana et al ldquoMalaria inMazandaran northern Iran passive case finding during 1997ndash2012rdquo Iranian Journal of Parasitology vol 7 no 3 pp 82ndash882012
[19] N Najafi R Ghasemian andM Farahmand ldquoEpidemiology ofMalaria in Mazandaran province during 1999ndash2003rdquo Journal ofMazandaran University of Medical Sciences vol 15 no 50 pp125ndash132 2006
[20] A Alemu DMuluye MMihret M Adugna andM GebeyawldquoTen year trend analysis of malaria prevalence in Kola DibaNorth Gondar Northwest Ethiopiardquo Parasites amp Vectors vol 5no 1 article 173 2012
[21] M Barak L Mottaghinia D Emdadi et al ldquoInvestigation ofa ten-year trend of local transmission of Malaria (Plasmodiumvivax) in endemic region of Ardabil province (Parsabad Dis-trict) from 2001 to 2010rdquo in Proceedings of the InternationalCongress on Malaria Elimination Kish Island Iran 2012
[22] N Sargolzaie M Salehi M Kiani et al ldquoMalaria epidemiologyin Sistan and Balouchestan province during April 2008ndashMarch2011 Iranrdquo Zahedan Journal of Research inMedical Sciences vol16 no 4 pp 41ndash43 2014
[23] A F Bafghi S Pourmazar and F Shamsi ldquoFive-year statusof Malaria (a disease causing Anemia) in Yazd 2008ndash2012rdquoIranian Journal of Pediatric Hematology Oncology vol 3 no 3pp 91ndash96 2013
Figure 2 Trend of malaria disease during 2001ndash2014
province and data were analyzed using SPSS software version18 (SPSS Inc Chicago IL USA)
3 Results
Trend of malaria during the past decade in Khuzestanprovince has dramatically slumped (Figure 2) The highestnumber of infections was seen in 2001 with 161 (2975)cases and the lowest was in 2014 with 0 (0) From atotal of 541 malaria confirmed cases during 2001ndash2014 498(9205) were male and 43 (795) were female P vivaxwas the predominant species in 478 (8835) individualsand P falciparum species comprised 63 (1165) Proportionof infection in different age groups of 0ndash5 5ndash15 and gt15years of age was 26 (481) 57 (1054) and 458 (8465)respectively Rate of malaria disease in Iranian and non-Iranian populations was found to be 82 (1515) and 459(8485) respectively Also number of imported cases was508 (9390) and the number of indigenous cases was 33(610) (Table 1) Our finding revealed that Ahvaz city (cap-ital of Khuzestan province) with 168 (3105) positive caseswas in the first rank Behbahan county with 158 (2920) wassecond andAndimeshkwith 42 (776) was third InDehdezand Haftkel counties no positive cases were reported duringthe years 2001ndash2014 (Figure 3) Highest and lowest API were004709 in 2001 and 0 in 2014 respectively (Table 1)
4 Discussion
Malaria in developing countries and tropical regions has beenof special importance historically [1] It was estimated in 1924that out of 13 million people who live in Iran 4-5 million ofthem became infected with malaria and 30ndash40 of the totaldeaths were allocated to this infection Also 75 of the totalIranian population lived in endemic and hyperendemic areasAt the same time one-third of the budget of the Ministryof Health (MoH) was spent to buy the quinine drug In1924 in Tehran 20 of patients referred to dispensaries hadmalaria Also in 1924 535 of all people who lived in Aras
5
42
168
8 13 6
158
419
020
38
2
3211
014
1020406080
100120140160180
Freq
uenc
y
Das
hte-
Aza
dega
n
Mas
jed
Sole
yman
Shad
egan
Shou
shta
r
Behb
ahan
Kho
rram
shah
rM
ahsh
ahr
Bagh
mal
ek
Ram
horm
oz
Hov
eize
h
And
imes
hk
Om
idiy
eh
Abad
an
Deh
dez
Hen
dija
n
Haft
kel
Ahv
az
Izeh
City
Figure 3 Distribution of malaria infection in different counties ofKhuzestan province
river area were diagnosed with malaria and 415 of alldeaths in this region are allocated to this infection [5] In arecent study it has been reported that the annual incidenceof malaria cases in Iran declined significantly from 66075to 3200 between 1995 and 2012 [9] Epidemiological studieshave shown that malaria in Iran unlike Africa and othercountries is dependent on climatic conditions This meansthat the unstable situation with rainfall increase may lead toincrease in the incidence of disease in high-risk areas [5 6]
In this study the trend of malaria disease and its epi-demiological features was surveyed between 2001 and 2014The findings revealed that the rate of infection as a resultof malaria campaign has a continuous decreasing trend sothat the frequency from 161 in 2001 fell down to 0 in theend of 2014 in the southwest of Iran Khuzestan provinceBased on current findings imported cases and non-Iranianpatients were found to be 9390 and 8485 respectivelyBecause of existence of Free Trade Zone (FTZ) the harborregion and high financial activities in this province manymerchants investors and workers from different regions aredeployed to these areas annually Also this province is atouristic and pilgrimage zone where several thousands ofpassengers from Iraq country located at the west of Irancommute from Khuzestan province annually and this issuecould be a reason for high frequency of infection Salvadoet al in Spain reported that the main cause of malaria insubjects is migration of the passengers to endemic countries[10] In another study conducted by Mascarello et al in Italyduring 1990ndash1998 the number of malaria cases was shown tohave increased by 100 and the main causes of this increasewere commute and immigration from endemic areas to thecountry [11] Also based on Iqbal et alrsquos study the rate ofmalaria infection among immigrants to Kuwait was observedto be 23 [12] Population movements in malaria endemiczones and the lack of adequate intervention lead to increasingthe risk of malaria For instance Iran in recent years hashosted approximately 2millionAfghan refugees and unfortu-nately these refugees have created many serious problems in
4 Journal of Tropical Medicine
Table1Ep
idem
iologicalfactorsof
malariain
Khu
zestan
province
durin
g2001ndash2014
Year
Total
APIlowast
Causativea
gent
(119899)
Gender(119899)
Age
(119899)
Type
oftransm
ission(119899)
Nationality(119899)
119875Vlowastlowast
119875119891lowastlowastlowast
Male
Female
0ndash5
5ndash15
gt15
Indigeno
usIm
ported
Iranian
Non
-Iranian
2001
161
004709
142
19151
108
21132
8153
18143
2002
91002617
910
838
82
811
907
842003
62001742
557
584
26
543
5912
502004
69001922
5910
654
25
626
638
612005
25000
678
232
241
03
220
256
192006
25000
685
214
232
15
190
255
202007
33000
903
285
303
23
281
326
272008
44001165
3410
368
16
378
3611
332009
12000321
111
93
13
81
112
102010
6000155
51
60
00
60
61
52011
3000
075
30
30
11
10
32
12012
5000124
32
50
00
55
03
22013
5000124
32
50
02
30
51
42014
00
00
00
00
00
00
0To
tal119899
()
541(100)
478(8835)
63(116
5)498(9205)
43(795)
26(481)
57(1054)
458(8465)
33(610
)508(9390)
82(1515)
459(8485)
lowast
APIA
nnualP
arasite
Incidence=
totaln
umbero
fpositive
slidesfor
parasiteinay
eartimes
1000to
talp
opulation
lowastlowast
119875v
Plasmodium
vivax
lowastlowastlowast
119875f
Plasmodium
falciparum
Journal of Tropical Medicine 5
malaria control program in our country Entering and trafficof Afghan and Pakistani immigrants to Iran were continuedeven though Afghanistan and Pakistan are considered ashighly dangerous transferors of malaria [6] Some reportshave documented this issue such as Soleimanifard et al[13] in Isfahan province (91 and 56 of total positivecases belonged toAfghan immigrants and other nationalitiesresp) Saghafipour et al [14] inQomprovince (915) Khaliliet al [15] in Yazd province (773 in Afghan refugees) andZia-Sheikholeslami and Rezaeian [16] in Rafsanjan county(989 in Afghan refugees)
Current investigation indicated that the number ofmalaria patients in Khuzestan province southwest Iranduring the past years has dropped significantly and API inthis province ranged from 004709 in 2001 to 0 in 2014 whichreflects the success in achieving and reaching the malariacontrol program in this province Our finding was similarto results gained from Sarafraz et al [17] in East Azerbaijanprovince and Ghaffari et al [18] in Mazandaran provinceIn the present investigation the rate of infection in maleswas 9205which is consistent with other surveys conductedin Isfahan province [13] (935) Mazandaran province [19](884) and East Azerbaijan province [17] (8646) Alsoin some surveys the ratio of both genders was equal andno significant differences were seen between them suchas Alemu et al [20] in Ethiopia (526 male and 474female) and Barak et al [21] in Ardabil province during 2001ndash2010 (45 male and 55 female) However gender is notinvolved directly and naturally in sensitivity and resistance tomalaria but may be correlated with job type of coating andcultural habits Also social activities and attendance of menin the workplaces outdoors make them more susceptible tomosquito bites and becoming infected
In the present investigation it was demonstrated that Pvivax is the most common species (8835) among malariasubjects which is in agreementwith general pattern of diseasein Iran [13 14 17 22] According to the fact that P vivaxcould relapse due to presence of liver hypnozoites thesepatients should be identified and treated In our study thehighest number was observed in persons over 15 years ofage (8465) which is in agreement with the results ofstudies like Saghafipour et al [14] in Qom province (662)Soleimanifard et al [13] in Isfahan province and Bafghi et al[23] in Yazd province Presence of infected individuals as dis-ease reservoirs and Anopheles mosquitoes as carriers has animportant role in epidemiological status and spread of diseasein endemic regions thus existence of these factors will helpin the transmission of malaria and lead to unstable situationIt should be noted that despite the significant reduction ofmalaria cases in Khuzestan province the hot and humidclimate of the province presence of the Karoun MarounKarkheh Kheirabad and Dez rivers and the arable landsurrounding these rivers provide a favorable environmentalcondition for anopheline mosquitoes larvae developmentEvidence shows that malaria control programs with theparticipation of people in society aremore effective comparedwith those programs that are only designed and implementedby governments therefore awareness attitudes and behaviorof people who live in endemic and hyperendemic areas can be
more effective in planning for the control and prevention ofmalaria [1 2 6 13]
As rapid treatment of infected patients either Iranian orforeign subjects some interventions such as antimosquitospraying and antilarval controlmeasures are being carried outin order to eliminate infection throughout the province andof course in Iran Further surveys like spatial studies in orderto determine manage and analyze epidemiological featuresusing Geographic Information System (GIS) in Khuzestanprovince are necessary
5 Conclusions
Number of malaria patients during 2001ndash2014 was decreasedsignificantly in the southwest of Iran Khuzestan provinceUnfortunately as it was mentioned before proximity withendemic countries like Iraq Afghanistan and Pakistan hasmade the malaria control program more difficult Existenceof infected people and vectors in the region contributes tothe spread of disease around Khuzestan province Accordingto the specific climatic status in Khuzestan province theoptimum conditions exist for the growth of the Anophelesmosquitoes thus the risk ofmalaria epidemics and incidenceof severe cases should be considered constantly Accordinglymalaria control programs should be continued until diseaseelimination
Conflict of Interests
The authors declare no conflict of interests
Authorsrsquo Contribution
All authors had equal role in design work statistical analysisand writing of the paper
Acknowledgments
This study was financially supported by Student ResearchCommittee of Ahvaz Jundishapur University of MedicalScience Iran (no 93S88) The authors would like to thankall staff at the health care centers in Khuzestan ProvinceAlso the authors sincerely acknowledge their gratitude to theefforts of Center for Disease Control in Ahvaz JundishapurUniversity of Medical Sciences
References
[1] G R L Del Prado C H Garcıa L M Cea et al ldquoMalariain developing countriesrdquo Journal of Infection in DevelopingCountries vol 8 no 1 pp 1ndash4 2014
[2] R Bhatia R M Rastogi and L Ortega ldquoMalaria successes andchallenges in Asiardquo Journal of Vector Borne Diseases vol 50 no4 pp 239ndash247 2013
[3] A Raeisi M M Gouya A Nadim et al ldquoDeterminationof malaria epidemiological status in Iranrsquos malarious areas asbaseline information for implementation ofmalaria eliminationprogram in Iranrdquo Iranian Journal of Public Health vol 42 no 3pp 326ndash333 2013
6 Journal of Tropical Medicine
[4] M Halimi M Delavari and A Takhtardeshir ldquoSurvey ofclimatic condition of Malaria disease outbreak in Iran usingGISrdquo Journal of School of Public Health and Institute of PublicHealth Research vol 10 no 3 pp 41ndash52 2013
[5] G Edrissian ldquoMalaria in Iran past and present situationrdquoIranian Journal of Parasitology vol 1 no 1 pp 1ndash14 2006
[6] M R Hemami A A Sari A Raeisi H Vatandoost andR Majdzadeh ldquoMalaria elimination in Iran importance andchallengesrdquo International Journal of Preventive Medicine vol 4no 1 pp 88ndash94 2013
[7] A-A Haghdoost N Alexander and J Cox ldquoModelling ofmalaria temporal variations in Iranrdquo Tropical Medicine ampInternational Health vol 13 no 12 pp 1501ndash1508 2008
[8] A Salahi-MoghadamA KhoshdelM Barati andM SedaghatldquoAn overview and mapping of Malaria and its vectors in IranrdquoHormozgan Medical Journal vol 18 no 5 pp 473ndash485 2014
[9] A R Mesdaghinia H Vatandoost A A Hanafi-Bojd RMajdzadeh and A Raeisi ldquoConducting international diplomacourse on malaria program planning and management (1996ndash2012)rdquo Journal of Arthropod-Borne Diseases vol 7 no 2 pp100ndash112 2013
[10] E Salvado M J Pinazo J Munoz et al ldquoClinical presentationand complications of Plasmodium falciparum malaria in twopopulations travelers and immigrantsrdquo Enfermedades Infec-ciosas y Microbiologia Clinica vol 26 no 5 pp 282ndash284 2008
[11] M Mascarello B Allegranzi A Angheben et al ldquoImportedmalaria in adults and children epidemiological and clinicalcharacteristics of 380 consecutive cases observed in VeronaItalyrdquo Journal of Travel Medicine vol 15 no 4 pp 229ndash2362008
[12] J Iqbal A Sher P R Hira and R Al-Owaish ldquoComparisonof the OptiMAL test with PCR for diagnosis of malaria inimmigrantsrdquo Journal of Clinical Microbiology vol 37 no 11 pp3644ndash3646 1999
[13] S Soleimanifard M Akbari M Sabetghadam and S SaberildquoMalaria situation in Isfahan in the last five yearsrdquo Journal ofIsfahan Medical School vol 29 no 132 pp 273ndash280 2011
[14] A Saghafipour M Noroozi M Karami-Jooshin and P AbbasldquoEpidemiological features of Malaria in Qom Province from2001 to 2011rdquo Zahedan Journal of Research in Medical Sciencesvol 14 no 8 pp 70ndash73 2012
[15] M B Khalili M Anvari-Tafti and M Sadeh ldquoEpidemiologicalpattern of malarial disease in the province of Yazd Iran (Since1986-2006)rdquoWorld Journal of Medical Sciences vol 4 no 1 pp41ndash45 2009
[16] N Zia-Sheikholeslami andM Rezaeian ldquoThe retrospective epi-demiological study of Malaria in Rafsanjan Kerman provincefrom 1999 to 2005rdquo Persian Health Journal of Ardebil vol 1 no1 pp 24ndash30 2010
[17] S Sarafraz N G Mehrabani Y Mirzaei et al ldquoEpidemiologyof malaria in East Azerbaijan province Iran from 2001 to 2013rdquoJournal of Parasitic Diseases pp 1ndash5 2014
[18] S Ghaffari S A Mahdavi Z Moulana et al ldquoMalaria inMazandaran northern Iran passive case finding during 1997ndash2012rdquo Iranian Journal of Parasitology vol 7 no 3 pp 82ndash882012
[19] N Najafi R Ghasemian andM Farahmand ldquoEpidemiology ofMalaria in Mazandaran province during 1999ndash2003rdquo Journal ofMazandaran University of Medical Sciences vol 15 no 50 pp125ndash132 2006
[20] A Alemu DMuluye MMihret M Adugna andM GebeyawldquoTen year trend analysis of malaria prevalence in Kola DibaNorth Gondar Northwest Ethiopiardquo Parasites amp Vectors vol 5no 1 article 173 2012
[21] M Barak L Mottaghinia D Emdadi et al ldquoInvestigation ofa ten-year trend of local transmission of Malaria (Plasmodiumvivax) in endemic region of Ardabil province (Parsabad Dis-trict) from 2001 to 2010rdquo in Proceedings of the InternationalCongress on Malaria Elimination Kish Island Iran 2012
[22] N Sargolzaie M Salehi M Kiani et al ldquoMalaria epidemiologyin Sistan and Balouchestan province during April 2008ndashMarch2011 Iranrdquo Zahedan Journal of Research inMedical Sciences vol16 no 4 pp 41ndash43 2014
[23] A F Bafghi S Pourmazar and F Shamsi ldquoFive-year statusof Malaria (a disease causing Anemia) in Yazd 2008ndash2012rdquoIranian Journal of Pediatric Hematology Oncology vol 3 no 3pp 91ndash96 2013
malaria control program in our country Entering and trafficof Afghan and Pakistani immigrants to Iran were continuedeven though Afghanistan and Pakistan are considered ashighly dangerous transferors of malaria [6] Some reportshave documented this issue such as Soleimanifard et al[13] in Isfahan province (91 and 56 of total positivecases belonged toAfghan immigrants and other nationalitiesresp) Saghafipour et al [14] inQomprovince (915) Khaliliet al [15] in Yazd province (773 in Afghan refugees) andZia-Sheikholeslami and Rezaeian [16] in Rafsanjan county(989 in Afghan refugees)
Current investigation indicated that the number ofmalaria patients in Khuzestan province southwest Iranduring the past years has dropped significantly and API inthis province ranged from 004709 in 2001 to 0 in 2014 whichreflects the success in achieving and reaching the malariacontrol program in this province Our finding was similarto results gained from Sarafraz et al [17] in East Azerbaijanprovince and Ghaffari et al [18] in Mazandaran provinceIn the present investigation the rate of infection in maleswas 9205which is consistent with other surveys conductedin Isfahan province [13] (935) Mazandaran province [19](884) and East Azerbaijan province [17] (8646) Alsoin some surveys the ratio of both genders was equal andno significant differences were seen between them suchas Alemu et al [20] in Ethiopia (526 male and 474female) and Barak et al [21] in Ardabil province during 2001ndash2010 (45 male and 55 female) However gender is notinvolved directly and naturally in sensitivity and resistance tomalaria but may be correlated with job type of coating andcultural habits Also social activities and attendance of menin the workplaces outdoors make them more susceptible tomosquito bites and becoming infected
In the present investigation it was demonstrated that Pvivax is the most common species (8835) among malariasubjects which is in agreementwith general pattern of diseasein Iran [13 14 17 22] According to the fact that P vivaxcould relapse due to presence of liver hypnozoites thesepatients should be identified and treated In our study thehighest number was observed in persons over 15 years ofage (8465) which is in agreement with the results ofstudies like Saghafipour et al [14] in Qom province (662)Soleimanifard et al [13] in Isfahan province and Bafghi et al[23] in Yazd province Presence of infected individuals as dis-ease reservoirs and Anopheles mosquitoes as carriers has animportant role in epidemiological status and spread of diseasein endemic regions thus existence of these factors will helpin the transmission of malaria and lead to unstable situationIt should be noted that despite the significant reduction ofmalaria cases in Khuzestan province the hot and humidclimate of the province presence of the Karoun MarounKarkheh Kheirabad and Dez rivers and the arable landsurrounding these rivers provide a favorable environmentalcondition for anopheline mosquitoes larvae developmentEvidence shows that malaria control programs with theparticipation of people in society aremore effective comparedwith those programs that are only designed and implementedby governments therefore awareness attitudes and behaviorof people who live in endemic and hyperendemic areas can be
more effective in planning for the control and prevention ofmalaria [1 2 6 13]
As rapid treatment of infected patients either Iranian orforeign subjects some interventions such as antimosquitospraying and antilarval controlmeasures are being carried outin order to eliminate infection throughout the province andof course in Iran Further surveys like spatial studies in orderto determine manage and analyze epidemiological featuresusing Geographic Information System (GIS) in Khuzestanprovince are necessary
5 Conclusions
Number of malaria patients during 2001ndash2014 was decreasedsignificantly in the southwest of Iran Khuzestan provinceUnfortunately as it was mentioned before proximity withendemic countries like Iraq Afghanistan and Pakistan hasmade the malaria control program more difficult Existenceof infected people and vectors in the region contributes tothe spread of disease around Khuzestan province Accordingto the specific climatic status in Khuzestan province theoptimum conditions exist for the growth of the Anophelesmosquitoes thus the risk ofmalaria epidemics and incidenceof severe cases should be considered constantly Accordinglymalaria control programs should be continued until diseaseelimination
Conflict of Interests
The authors declare no conflict of interests
Authorsrsquo Contribution
All authors had equal role in design work statistical analysisand writing of the paper
Acknowledgments
This study was financially supported by Student ResearchCommittee of Ahvaz Jundishapur University of MedicalScience Iran (no 93S88) The authors would like to thankall staff at the health care centers in Khuzestan ProvinceAlso the authors sincerely acknowledge their gratitude to theefforts of Center for Disease Control in Ahvaz JundishapurUniversity of Medical Sciences
References
[1] G R L Del Prado C H Garcıa L M Cea et al ldquoMalariain developing countriesrdquo Journal of Infection in DevelopingCountries vol 8 no 1 pp 1ndash4 2014
[2] R Bhatia R M Rastogi and L Ortega ldquoMalaria successes andchallenges in Asiardquo Journal of Vector Borne Diseases vol 50 no4 pp 239ndash247 2013
[3] A Raeisi M M Gouya A Nadim et al ldquoDeterminationof malaria epidemiological status in Iranrsquos malarious areas asbaseline information for implementation ofmalaria eliminationprogram in Iranrdquo Iranian Journal of Public Health vol 42 no 3pp 326ndash333 2013
6 Journal of Tropical Medicine
[4] M Halimi M Delavari and A Takhtardeshir ldquoSurvey ofclimatic condition of Malaria disease outbreak in Iran usingGISrdquo Journal of School of Public Health and Institute of PublicHealth Research vol 10 no 3 pp 41ndash52 2013
[5] G Edrissian ldquoMalaria in Iran past and present situationrdquoIranian Journal of Parasitology vol 1 no 1 pp 1ndash14 2006
[6] M R Hemami A A Sari A Raeisi H Vatandoost andR Majdzadeh ldquoMalaria elimination in Iran importance andchallengesrdquo International Journal of Preventive Medicine vol 4no 1 pp 88ndash94 2013
[7] A-A Haghdoost N Alexander and J Cox ldquoModelling ofmalaria temporal variations in Iranrdquo Tropical Medicine ampInternational Health vol 13 no 12 pp 1501ndash1508 2008
[8] A Salahi-MoghadamA KhoshdelM Barati andM SedaghatldquoAn overview and mapping of Malaria and its vectors in IranrdquoHormozgan Medical Journal vol 18 no 5 pp 473ndash485 2014
[9] A R Mesdaghinia H Vatandoost A A Hanafi-Bojd RMajdzadeh and A Raeisi ldquoConducting international diplomacourse on malaria program planning and management (1996ndash2012)rdquo Journal of Arthropod-Borne Diseases vol 7 no 2 pp100ndash112 2013
[10] E Salvado M J Pinazo J Munoz et al ldquoClinical presentationand complications of Plasmodium falciparum malaria in twopopulations travelers and immigrantsrdquo Enfermedades Infec-ciosas y Microbiologia Clinica vol 26 no 5 pp 282ndash284 2008
[11] M Mascarello B Allegranzi A Angheben et al ldquoImportedmalaria in adults and children epidemiological and clinicalcharacteristics of 380 consecutive cases observed in VeronaItalyrdquo Journal of Travel Medicine vol 15 no 4 pp 229ndash2362008
[12] J Iqbal A Sher P R Hira and R Al-Owaish ldquoComparisonof the OptiMAL test with PCR for diagnosis of malaria inimmigrantsrdquo Journal of Clinical Microbiology vol 37 no 11 pp3644ndash3646 1999
[13] S Soleimanifard M Akbari M Sabetghadam and S SaberildquoMalaria situation in Isfahan in the last five yearsrdquo Journal ofIsfahan Medical School vol 29 no 132 pp 273ndash280 2011
[14] A Saghafipour M Noroozi M Karami-Jooshin and P AbbasldquoEpidemiological features of Malaria in Qom Province from2001 to 2011rdquo Zahedan Journal of Research in Medical Sciencesvol 14 no 8 pp 70ndash73 2012
[15] M B Khalili M Anvari-Tafti and M Sadeh ldquoEpidemiologicalpattern of malarial disease in the province of Yazd Iran (Since1986-2006)rdquoWorld Journal of Medical Sciences vol 4 no 1 pp41ndash45 2009
[16] N Zia-Sheikholeslami andM Rezaeian ldquoThe retrospective epi-demiological study of Malaria in Rafsanjan Kerman provincefrom 1999 to 2005rdquo Persian Health Journal of Ardebil vol 1 no1 pp 24ndash30 2010
[17] S Sarafraz N G Mehrabani Y Mirzaei et al ldquoEpidemiologyof malaria in East Azerbaijan province Iran from 2001 to 2013rdquoJournal of Parasitic Diseases pp 1ndash5 2014
[18] S Ghaffari S A Mahdavi Z Moulana et al ldquoMalaria inMazandaran northern Iran passive case finding during 1997ndash2012rdquo Iranian Journal of Parasitology vol 7 no 3 pp 82ndash882012
[19] N Najafi R Ghasemian andM Farahmand ldquoEpidemiology ofMalaria in Mazandaran province during 1999ndash2003rdquo Journal ofMazandaran University of Medical Sciences vol 15 no 50 pp125ndash132 2006
[20] A Alemu DMuluye MMihret M Adugna andM GebeyawldquoTen year trend analysis of malaria prevalence in Kola DibaNorth Gondar Northwest Ethiopiardquo Parasites amp Vectors vol 5no 1 article 173 2012
[21] M Barak L Mottaghinia D Emdadi et al ldquoInvestigation ofa ten-year trend of local transmission of Malaria (Plasmodiumvivax) in endemic region of Ardabil province (Parsabad Dis-trict) from 2001 to 2010rdquo in Proceedings of the InternationalCongress on Malaria Elimination Kish Island Iran 2012
[22] N Sargolzaie M Salehi M Kiani et al ldquoMalaria epidemiologyin Sistan and Balouchestan province during April 2008ndashMarch2011 Iranrdquo Zahedan Journal of Research inMedical Sciences vol16 no 4 pp 41ndash43 2014
[23] A F Bafghi S Pourmazar and F Shamsi ldquoFive-year statusof Malaria (a disease causing Anemia) in Yazd 2008ndash2012rdquoIranian Journal of Pediatric Hematology Oncology vol 3 no 3pp 91ndash96 2013
malaria control program in our country Entering and trafficof Afghan and Pakistani immigrants to Iran were continuedeven though Afghanistan and Pakistan are considered ashighly dangerous transferors of malaria [6] Some reportshave documented this issue such as Soleimanifard et al[13] in Isfahan province (91 and 56 of total positivecases belonged toAfghan immigrants and other nationalitiesresp) Saghafipour et al [14] inQomprovince (915) Khaliliet al [15] in Yazd province (773 in Afghan refugees) andZia-Sheikholeslami and Rezaeian [16] in Rafsanjan county(989 in Afghan refugees)
Current investigation indicated that the number ofmalaria patients in Khuzestan province southwest Iranduring the past years has dropped significantly and API inthis province ranged from 004709 in 2001 to 0 in 2014 whichreflects the success in achieving and reaching the malariacontrol program in this province Our finding was similarto results gained from Sarafraz et al [17] in East Azerbaijanprovince and Ghaffari et al [18] in Mazandaran provinceIn the present investigation the rate of infection in maleswas 9205which is consistent with other surveys conductedin Isfahan province [13] (935) Mazandaran province [19](884) and East Azerbaijan province [17] (8646) Alsoin some surveys the ratio of both genders was equal andno significant differences were seen between them suchas Alemu et al [20] in Ethiopia (526 male and 474female) and Barak et al [21] in Ardabil province during 2001ndash2010 (45 male and 55 female) However gender is notinvolved directly and naturally in sensitivity and resistance tomalaria but may be correlated with job type of coating andcultural habits Also social activities and attendance of menin the workplaces outdoors make them more susceptible tomosquito bites and becoming infected
In the present investigation it was demonstrated that Pvivax is the most common species (8835) among malariasubjects which is in agreementwith general pattern of diseasein Iran [13 14 17 22] According to the fact that P vivaxcould relapse due to presence of liver hypnozoites thesepatients should be identified and treated In our study thehighest number was observed in persons over 15 years ofage (8465) which is in agreement with the results ofstudies like Saghafipour et al [14] in Qom province (662)Soleimanifard et al [13] in Isfahan province and Bafghi et al[23] in Yazd province Presence of infected individuals as dis-ease reservoirs and Anopheles mosquitoes as carriers has animportant role in epidemiological status and spread of diseasein endemic regions thus existence of these factors will helpin the transmission of malaria and lead to unstable situationIt should be noted that despite the significant reduction ofmalaria cases in Khuzestan province the hot and humidclimate of the province presence of the Karoun MarounKarkheh Kheirabad and Dez rivers and the arable landsurrounding these rivers provide a favorable environmentalcondition for anopheline mosquitoes larvae developmentEvidence shows that malaria control programs with theparticipation of people in society aremore effective comparedwith those programs that are only designed and implementedby governments therefore awareness attitudes and behaviorof people who live in endemic and hyperendemic areas can be
more effective in planning for the control and prevention ofmalaria [1 2 6 13]
As rapid treatment of infected patients either Iranian orforeign subjects some interventions such as antimosquitospraying and antilarval controlmeasures are being carried outin order to eliminate infection throughout the province andof course in Iran Further surveys like spatial studies in orderto determine manage and analyze epidemiological featuresusing Geographic Information System (GIS) in Khuzestanprovince are necessary
5 Conclusions
Number of malaria patients during 2001ndash2014 was decreasedsignificantly in the southwest of Iran Khuzestan provinceUnfortunately as it was mentioned before proximity withendemic countries like Iraq Afghanistan and Pakistan hasmade the malaria control program more difficult Existenceof infected people and vectors in the region contributes tothe spread of disease around Khuzestan province Accordingto the specific climatic status in Khuzestan province theoptimum conditions exist for the growth of the Anophelesmosquitoes thus the risk ofmalaria epidemics and incidenceof severe cases should be considered constantly Accordinglymalaria control programs should be continued until diseaseelimination
Conflict of Interests
The authors declare no conflict of interests
Authorsrsquo Contribution
All authors had equal role in design work statistical analysisand writing of the paper
Acknowledgments
This study was financially supported by Student ResearchCommittee of Ahvaz Jundishapur University of MedicalScience Iran (no 93S88) The authors would like to thankall staff at the health care centers in Khuzestan ProvinceAlso the authors sincerely acknowledge their gratitude to theefforts of Center for Disease Control in Ahvaz JundishapurUniversity of Medical Sciences
References
[1] G R L Del Prado C H Garcıa L M Cea et al ldquoMalariain developing countriesrdquo Journal of Infection in DevelopingCountries vol 8 no 1 pp 1ndash4 2014
[2] R Bhatia R M Rastogi and L Ortega ldquoMalaria successes andchallenges in Asiardquo Journal of Vector Borne Diseases vol 50 no4 pp 239ndash247 2013
[3] A Raeisi M M Gouya A Nadim et al ldquoDeterminationof malaria epidemiological status in Iranrsquos malarious areas asbaseline information for implementation ofmalaria eliminationprogram in Iranrdquo Iranian Journal of Public Health vol 42 no 3pp 326ndash333 2013
6 Journal of Tropical Medicine
[4] M Halimi M Delavari and A Takhtardeshir ldquoSurvey ofclimatic condition of Malaria disease outbreak in Iran usingGISrdquo Journal of School of Public Health and Institute of PublicHealth Research vol 10 no 3 pp 41ndash52 2013
[5] G Edrissian ldquoMalaria in Iran past and present situationrdquoIranian Journal of Parasitology vol 1 no 1 pp 1ndash14 2006
[6] M R Hemami A A Sari A Raeisi H Vatandoost andR Majdzadeh ldquoMalaria elimination in Iran importance andchallengesrdquo International Journal of Preventive Medicine vol 4no 1 pp 88ndash94 2013
[7] A-A Haghdoost N Alexander and J Cox ldquoModelling ofmalaria temporal variations in Iranrdquo Tropical Medicine ampInternational Health vol 13 no 12 pp 1501ndash1508 2008
[8] A Salahi-MoghadamA KhoshdelM Barati andM SedaghatldquoAn overview and mapping of Malaria and its vectors in IranrdquoHormozgan Medical Journal vol 18 no 5 pp 473ndash485 2014
[9] A R Mesdaghinia H Vatandoost A A Hanafi-Bojd RMajdzadeh and A Raeisi ldquoConducting international diplomacourse on malaria program planning and management (1996ndash2012)rdquo Journal of Arthropod-Borne Diseases vol 7 no 2 pp100ndash112 2013
[10] E Salvado M J Pinazo J Munoz et al ldquoClinical presentationand complications of Plasmodium falciparum malaria in twopopulations travelers and immigrantsrdquo Enfermedades Infec-ciosas y Microbiologia Clinica vol 26 no 5 pp 282ndash284 2008
[11] M Mascarello B Allegranzi A Angheben et al ldquoImportedmalaria in adults and children epidemiological and clinicalcharacteristics of 380 consecutive cases observed in VeronaItalyrdquo Journal of Travel Medicine vol 15 no 4 pp 229ndash2362008
[12] J Iqbal A Sher P R Hira and R Al-Owaish ldquoComparisonof the OptiMAL test with PCR for diagnosis of malaria inimmigrantsrdquo Journal of Clinical Microbiology vol 37 no 11 pp3644ndash3646 1999
[13] S Soleimanifard M Akbari M Sabetghadam and S SaberildquoMalaria situation in Isfahan in the last five yearsrdquo Journal ofIsfahan Medical School vol 29 no 132 pp 273ndash280 2011
[14] A Saghafipour M Noroozi M Karami-Jooshin and P AbbasldquoEpidemiological features of Malaria in Qom Province from2001 to 2011rdquo Zahedan Journal of Research in Medical Sciencesvol 14 no 8 pp 70ndash73 2012
[15] M B Khalili M Anvari-Tafti and M Sadeh ldquoEpidemiologicalpattern of malarial disease in the province of Yazd Iran (Since1986-2006)rdquoWorld Journal of Medical Sciences vol 4 no 1 pp41ndash45 2009
[16] N Zia-Sheikholeslami andM Rezaeian ldquoThe retrospective epi-demiological study of Malaria in Rafsanjan Kerman provincefrom 1999 to 2005rdquo Persian Health Journal of Ardebil vol 1 no1 pp 24ndash30 2010
[17] S Sarafraz N G Mehrabani Y Mirzaei et al ldquoEpidemiologyof malaria in East Azerbaijan province Iran from 2001 to 2013rdquoJournal of Parasitic Diseases pp 1ndash5 2014
[18] S Ghaffari S A Mahdavi Z Moulana et al ldquoMalaria inMazandaran northern Iran passive case finding during 1997ndash2012rdquo Iranian Journal of Parasitology vol 7 no 3 pp 82ndash882012
[19] N Najafi R Ghasemian andM Farahmand ldquoEpidemiology ofMalaria in Mazandaran province during 1999ndash2003rdquo Journal ofMazandaran University of Medical Sciences vol 15 no 50 pp125ndash132 2006
[20] A Alemu DMuluye MMihret M Adugna andM GebeyawldquoTen year trend analysis of malaria prevalence in Kola DibaNorth Gondar Northwest Ethiopiardquo Parasites amp Vectors vol 5no 1 article 173 2012
[21] M Barak L Mottaghinia D Emdadi et al ldquoInvestigation ofa ten-year trend of local transmission of Malaria (Plasmodiumvivax) in endemic region of Ardabil province (Parsabad Dis-trict) from 2001 to 2010rdquo in Proceedings of the InternationalCongress on Malaria Elimination Kish Island Iran 2012
[22] N Sargolzaie M Salehi M Kiani et al ldquoMalaria epidemiologyin Sistan and Balouchestan province during April 2008ndashMarch2011 Iranrdquo Zahedan Journal of Research inMedical Sciences vol16 no 4 pp 41ndash43 2014
[23] A F Bafghi S Pourmazar and F Shamsi ldquoFive-year statusof Malaria (a disease causing Anemia) in Yazd 2008ndash2012rdquoIranian Journal of Pediatric Hematology Oncology vol 3 no 3pp 91ndash96 2013
[4] M Halimi M Delavari and A Takhtardeshir ldquoSurvey ofclimatic condition of Malaria disease outbreak in Iran usingGISrdquo Journal of School of Public Health and Institute of PublicHealth Research vol 10 no 3 pp 41ndash52 2013
[5] G Edrissian ldquoMalaria in Iran past and present situationrdquoIranian Journal of Parasitology vol 1 no 1 pp 1ndash14 2006
[6] M R Hemami A A Sari A Raeisi H Vatandoost andR Majdzadeh ldquoMalaria elimination in Iran importance andchallengesrdquo International Journal of Preventive Medicine vol 4no 1 pp 88ndash94 2013
[7] A-A Haghdoost N Alexander and J Cox ldquoModelling ofmalaria temporal variations in Iranrdquo Tropical Medicine ampInternational Health vol 13 no 12 pp 1501ndash1508 2008
[8] A Salahi-MoghadamA KhoshdelM Barati andM SedaghatldquoAn overview and mapping of Malaria and its vectors in IranrdquoHormozgan Medical Journal vol 18 no 5 pp 473ndash485 2014
[9] A R Mesdaghinia H Vatandoost A A Hanafi-Bojd RMajdzadeh and A Raeisi ldquoConducting international diplomacourse on malaria program planning and management (1996ndash2012)rdquo Journal of Arthropod-Borne Diseases vol 7 no 2 pp100ndash112 2013
[10] E Salvado M J Pinazo J Munoz et al ldquoClinical presentationand complications of Plasmodium falciparum malaria in twopopulations travelers and immigrantsrdquo Enfermedades Infec-ciosas y Microbiologia Clinica vol 26 no 5 pp 282ndash284 2008
[11] M Mascarello B Allegranzi A Angheben et al ldquoImportedmalaria in adults and children epidemiological and clinicalcharacteristics of 380 consecutive cases observed in VeronaItalyrdquo Journal of Travel Medicine vol 15 no 4 pp 229ndash2362008
[12] J Iqbal A Sher P R Hira and R Al-Owaish ldquoComparisonof the OptiMAL test with PCR for diagnosis of malaria inimmigrantsrdquo Journal of Clinical Microbiology vol 37 no 11 pp3644ndash3646 1999
[13] S Soleimanifard M Akbari M Sabetghadam and S SaberildquoMalaria situation in Isfahan in the last five yearsrdquo Journal ofIsfahan Medical School vol 29 no 132 pp 273ndash280 2011
[14] A Saghafipour M Noroozi M Karami-Jooshin and P AbbasldquoEpidemiological features of Malaria in Qom Province from2001 to 2011rdquo Zahedan Journal of Research in Medical Sciencesvol 14 no 8 pp 70ndash73 2012
[15] M B Khalili M Anvari-Tafti and M Sadeh ldquoEpidemiologicalpattern of malarial disease in the province of Yazd Iran (Since1986-2006)rdquoWorld Journal of Medical Sciences vol 4 no 1 pp41ndash45 2009
[16] N Zia-Sheikholeslami andM Rezaeian ldquoThe retrospective epi-demiological study of Malaria in Rafsanjan Kerman provincefrom 1999 to 2005rdquo Persian Health Journal of Ardebil vol 1 no1 pp 24ndash30 2010
[17] S Sarafraz N G Mehrabani Y Mirzaei et al ldquoEpidemiologyof malaria in East Azerbaijan province Iran from 2001 to 2013rdquoJournal of Parasitic Diseases pp 1ndash5 2014
[18] S Ghaffari S A Mahdavi Z Moulana et al ldquoMalaria inMazandaran northern Iran passive case finding during 1997ndash2012rdquo Iranian Journal of Parasitology vol 7 no 3 pp 82ndash882012
[19] N Najafi R Ghasemian andM Farahmand ldquoEpidemiology ofMalaria in Mazandaran province during 1999ndash2003rdquo Journal ofMazandaran University of Medical Sciences vol 15 no 50 pp125ndash132 2006
[20] A Alemu DMuluye MMihret M Adugna andM GebeyawldquoTen year trend analysis of malaria prevalence in Kola DibaNorth Gondar Northwest Ethiopiardquo Parasites amp Vectors vol 5no 1 article 173 2012
[21] M Barak L Mottaghinia D Emdadi et al ldquoInvestigation ofa ten-year trend of local transmission of Malaria (Plasmodiumvivax) in endemic region of Ardabil province (Parsabad Dis-trict) from 2001 to 2010rdquo in Proceedings of the InternationalCongress on Malaria Elimination Kish Island Iran 2012
[22] N Sargolzaie M Salehi M Kiani et al ldquoMalaria epidemiologyin Sistan and Balouchestan province during April 2008ndashMarch2011 Iranrdquo Zahedan Journal of Research inMedical Sciences vol16 no 4 pp 41ndash43 2014
[23] A F Bafghi S Pourmazar and F Shamsi ldquoFive-year statusof Malaria (a disease causing Anemia) in Yazd 2008ndash2012rdquoIranian Journal of Pediatric Hematology Oncology vol 3 no 3pp 91ndash96 2013
