visceral leishmaniasis-malaria coinfection and their...

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Research Article Visceral Leishmaniasis-Malaria Coinfection and Their Associated Factors in Patients Attending Metema Hospital, Northwest Ethiopia: Suggestion for Integrated Vector Management Getachew Ferede, 1 Ermias Diro, 2 Sisay Getie, 1 Gebeyaw Getnet, 1 Yegnasew Takele, 3 Anteneh Amsalu, 4 and Yitayih Wondimeneh 1 1 College of Medicine and Health Sciences, School of Biomedical and Laboratory Sciences, Department of Medical Parasitology, University of Gondar, P.O. Box 196, Gondar, Ethiopia 2 College of Medicine and Health Sciences, School of Medicine, Department of Internal Medicine, University of Gondar, P.O. Box 196, Gondar, Ethiopia 3 Leishmaniasis Research and Treatment Center, University of Gondar, Gondar, Ethiopia 4 College of Medicine and Health Sciences, School of Biomedical and Laboratory Sciences, Department of Medical Microbiology, University of Gondar, P.O. Box 196, Gondar, Ethiopia Correspondence should be addressed to Getachew Ferede; [email protected] Received 18 April 2017; Revised 24 July 2017; Accepted 31 July 2017; Published 28 August 2017 Academic Editor: Rana Chattopadhyay Copyright © 2017 Getachew Ferede et al. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Background. Despite high prevalence of visceral leishmaniasis and malaria in the study area, their coinfection remains unknown. erefore, this study was aimed to document VL-malaria coinfections and their associated factors. Methods. A cross-sectional study was conducted among clinical suspected VL patients attending Metema hospital, Northwest Ethiopia, from January 2014 to June 2014. Blood sample was tested by rk39 antigen-based DiaMed IT-Leish dipstick and Giemsa stain microscopic examination of thick and thin blood smears for malaria detection was performed. Result. A total of 384 VL suspected patients were included in the study. Out of these, the prevalence of VL was 83 (21.6%) while the prevalence of malaria was 45 (11.7%). Of malaria cases, 40 (89%) were positive for P. falciparum and 5 (11%) positive for P. vivax. e overall prevalence of VL-malaria coinfection was 16 (4.2%). One-hundred eighty (46.9%) study participants have history of travel. Of these, 10 (5.6%) have VL-malaria coinfections. Age less than 5 years was associated with VL-malaria coinfection. Conclusion. is study highlights the importance of performing malaria screening amongst VL patients living in malaria-endemic areas, particularly in patients under five years. 1. Background Leishmaniasis and malaria are among the most important six diseases on the World Health Organization (WHO) or Tropical Disease Research list. ere are 2 million new cases of Leishmaniasis diagnosed every year [1]. As for malaria, 300–660 million people become infected yearly with the malignant Plasmodium falciparum, and 200–300 children are dying every hour from this disease [2, 3]. According to the world malaria report 2016, there were about 212 million cases of malaria and 429,000 deaths [4]. Visceral leishmaniasis (VL) is the phlebotomine sand flies borne disease caused by an intracellular protozoan parasite of the Leishmania donovani complex [5], while malaria is Anopheles mosquito borne disease caused by an intracellular protozoan parasite of Plasmodium species [6]. Usually, the transmission of both parasites occurs when the female insect takes a blood meal. Measures to combat these two diseases usually aimed at interrupting the life-cycle of the parasite by destroying the parasite or its vector. Destroying the parasite could be achieved by vaccination or treatment. Destroying the vector could be achieved by many ways such Hindawi Malaria Research and Treatment Volume 2017, Article ID 6816913, 6 pages https://doi.org/10.1155/2017/6816913

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Page 1: Visceral Leishmaniasis-Malaria Coinfection and Their ...downloads.hindawi.com/archive/2017/6816913.pdf · malaria.Individualswholiveintheurban8(5.3%)andrural 8(3.4%)werecoinfectedwithVL-malaria.5dailylaborers

Research ArticleVisceral Leishmaniasis-Malaria Coinfection andTheir Associated Factors in Patients Attending Metema HospitalNorthwest Ethiopia Suggestion forIntegrated Vector Management

Getachew Ferede1 Ermias Diro2 Sisay Getie1 Gebeyaw Getnet1 Yegnasew Takele3

Anteneh Amsalu4 and YitayihWondimeneh1

1College of Medicine and Health Sciences School of Biomedical and Laboratory Sciences Department of Medical ParasitologyUniversity of Gondar PO Box 196 Gondar Ethiopia2College of Medicine and Health Sciences School of Medicine Department of Internal Medicine University of Gondar PO Box 196Gondar Ethiopia3Leishmaniasis Research and Treatment Center University of Gondar Gondar Ethiopia4College of Medicine and Health Sciences School of Biomedical and Laboratory Sciences Department of Medical MicrobiologyUniversity of Gondar PO Box 196 Gondar Ethiopia

Correspondence should be addressed to Getachew Ferede get29fgmailcom

Received 18 April 2017 Revised 24 July 2017 Accepted 31 July 2017 Published 28 August 2017

Academic Editor Rana Chattopadhyay

Copyright copy 2017 Getachew Ferede et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

Background Despite high prevalence of visceral leishmaniasis and malaria in the study area their coinfection remains unknownTherefore this study was aimed to document VL-malaria coinfections and their associated factors Methods A cross-sectionalstudy was conducted among clinical suspected VL patients attending Metema hospital Northwest Ethiopia from January 2014 toJune 2014 Blood sample was tested by rk39 antigen-based DiaMed IT-Leish dipstick and Giemsa stain microscopic examination ofthick and thin blood smears for malaria detection was performed Result A total of 384 VL suspected patients were included in thestudy Out of these the prevalence of VL was 83 (216) while the prevalence of malaria was 45 (117) Of malaria cases 40 (89)were positive for P falciparum and 5 (11) positive for P vivax The overall prevalence of VL-malaria coinfection was 16 (42)One-hundred eighty (469) study participants have history of travel Of these 10 (56) have VL-malaria coinfections Age lessthan 5 years was associated with VL-malaria coinfection Conclusion This study highlights the importance of performing malariascreening amongst VL patients living in malaria-endemic areas particularly in patients under five years

1 Background

Leishmaniasis and malaria are among the most importantsix diseases on the World Health Organization (WHO) orTropical Disease Research list There are 2 million new casesof Leishmaniasis diagnosed every year [1] As for malaria300ndash660 million people become infected yearly with themalignant Plasmodium falciparum and 200ndash300 children aredying every hour from this disease [2 3] According to theworld malaria report 2016 there were about 212 million casesof malaria and 429000 deaths [4]

Visceral leishmaniasis (VL) is the phlebotomine sandflies borne disease caused by an intracellular protozoanparasite of the Leishmania donovani complex [5] whilemalaria is Anopheles mosquito borne disease caused by anintracellular protozoan parasite of Plasmodium species [6]Usually the transmission of both parasites occurs when thefemale insect takes a blood meal Measures to combat thesetwo diseases usually aimed at interrupting the life-cycle of theparasite by destroying the parasite or its vector Destroyingthe parasite could be achieved by vaccination or treatmentDestroying the vector could be achieved by many ways such

HindawiMalaria Research and TreatmentVolume 2017 Article ID 6816913 6 pageshttpsdoiorg10115520176816913

2 Malaria Research and Treatment

as introducing an enemy of the vector to the environmentusing the sterile male technique destroying the habitat of thevector or spraying pesticides [7]

Visceral leishmaniasis andmalaria are the twomajor life-threatening parasitic diseases that still remain a serious publichealth problem particularly in endemic areas [8 9] Differ-ential diagnosis of VL often includes malaria among otherfebrile splenomegalies due to its clinical overlap Malariain fact is widespread in tropical and subtropical regions ofthe world where it accounts for more than 250 million casesannually the vast majority of which occurs among childrenunder 5 years old [10] Transmission can occur throughoutthe year or be seasonal depending on the region [11] In thelatter case transmission seasons for VL and malaria may notcoincide but the two diseases still overlap due to the longerincubation period of VL The overlap in disease distributionsuggests the two diseases could cooccur in the same host

Visceral leishmaniasis and malaria coinfections havebeen reported across various African and Asian countrieswith the prevalence among VL patients ranging from 208and 64 in Uganda [12 13] to 107 in Sudan [14] and 12in Bangladesh [15] and a rate of 59 among Indian patientswith fever and splenomegaly [16] with the exception ofthe case-reports [17ndash20] whose evidence remains anecdotalDespite high prevalence of the VL [21] and malaria [22]in the study area their coinfection is unknown Thereforethis study was designed to document the prevalence ofVL-malaria coinfection and their associated factors amongpatients attending Metema hospital

2 Materials and Methods

21 Study Area and Period This study was conducted atMetema hospital from January 2014 to June 2014 Metema isa town in Northwestern Ethiopia on the border with SudanThis town is located in the North Gondar AdministrativeZone Amhara region 897 km North of Addis Ababa and197 km from the ancient city of Gondar and it has a latitudeand longitude of 12∘581015840N 36∘121015840E with an elevation of 685meters above sea level This area is malarious and has casesof VL

22 Study Design Study Population and Sampling TechniqueA cross-sectional study was carried out atMetema hospital todetermine VL-malaria coinfection among all clinically sus-pected VL patients Visceral leishmaniasis suspected patientswho have taken treatment for malaria andor VL for the lasttwo weeks were excluded from the study Visceral leishma-niasis suspects are defined as those individuals who developclinical evidence of infection usually have fever loss ofappetite (anorexia) weight loss fatigue anemia enlargement(swelling) of the spleen and liver and abnormal blood tests[23]

23 Data Collection and Processing Well-structured ques-tionnaire was prepared in English version by the researchteam It was translated later into the local language AmharicThe questionnaire addresses patientsrsquo sociodemographicinformation and associated factors A pretest was conducted

among five percent of the total sample size by trained datacollectors and any ambiguous questions and repetitive ideaswere corrected Additional response categories were addedbased on the pretest findings

24 Parasitological Techniques After interviewing the pa-tients fresh peripheral whole blood sample was tested by therk39 ICT with sensitivity of 100 and specificity of 98 [24]for diagnosis of VL and Giemsa stain microscopic examina-tion of thick and thin blood smears for malaria detection andspecies differentiation was performed systematically

25 Data Analysis Data were entered and analyzed usingSPSS version 20 software The Pearson Chi-square test wasemployed to examine associated factors with the coinfection119875 value lt 005 was considered statistically significant

26 Ethical Consideration Ethical clearance was obtainedfrom Institutional Review Board of University of GondarWritten informed consent was obtained from each of thevolunteer study subjects or guardian of children Patientinformation was anonymized and deidentified prior to anal-ysis Positive results were given for physicians working in thehospital for treatment according to the national treatmentguideline

3 Results

31 Sociodemographic Characteristics A total of 384 VLsuspected participants were included in this study Out ofthese 334 (87) were males The mean (standard deviation)age was 281 (118) years (ranging from 2 to 78 years) Majority227 (591) of the study participants were in the age group of15ndash29 years old Among the study groups 230 (599) wereilliterate and 267 (695) were farmers followed by 54 (141)daily laborersThemajority of study participants 234 (609)were from rural residents (Table 1)

32 Visceral Leishmaniasis-Malaria Coinfection and Sociode-mographic Characteristics Out of the total VL suspectedcases 2 (333) VL-malaria coinfections were found in theage groups of lt5 years followed by 9 (4) within 15ndash29 yearsold (119875=0004) Visceral leishmaniasis-malaria coinfection bygender showed that 15 (45) ofmales were coinfected byVL-malaria Individuals who live in the urban 8 (53) and rural8 (34) were coinfected with VL-malaria 5 daily laborers(93) were coinfected with VL-malaria (Table 2)

33 Prevalence of VL-Malaria Coinfection Out of the totalVL suspected patients the overall prevalence of VL-malariacoinfection was 16 (42) The prevalence of VL was 83(216) while the prevalence of malaria was 45 (117)(Table 3) Of the malaria positive patients 40 (89) werepositive for P falciparum and 5 (11) were positive for P vivax(Figure 1)

34 Associated Factors for VL-Malaria Coinfection From thetotal study participants 292 (76) were used bed nets Ofthese 13 (45) patients were VL-malaria coinfected Mostof the study participants 217 (565) sleep inside home One

Malaria Research and Treatment 3

Table 1 Sociodemographic characteristics of the study participants at Metema hospital Northwest Ethiopia 2014

Characteristic Frequency Percentage

Age (years)

lt5 6 165ndash14 20 5215ndash29 227 59130ndash44 99 258ge45 32 83

Gender Male 334 870Female 50 130

Residence Rural 234 609Urban 150 391

Occupational status

Farmer 267 695Merchant 12 31Driver 2 05

Civil servant 12 31Daily laborer 54 141Housewife 18 47Student 19 49

Educational status

Illiterate 230 599Only read and write 85 221Elementary school 45 117

High school 21 55Collegeuniversities 3 08

Table 2 Sociodemographic characteristics of the study participants in relation to VL-malaria coinfection at Metema Hospital NorthwestEthiopia 2014

VariablesVL suspected cases

119875 valueNot VL-malariacoinfected ()

VL-malariacoinfected ()

Age

lt5 4 (667) 2 (333)

00045ndash14 20 (100) 0 (0)15ndash29 218 (960) 9 (40)30ndash44 94 (950) 5 (50)ge45 32 (100) 0 (0)

Gender Male 319 (955) 15 (45) 0411Female 49 (980) 1 (20)

Residence Rural 226 (966) 8 (34) 0360Urban 142 (947) 8 (53)

Occupation status

Farmer 257 (963) 10 (37)

0384

Merchant 11 (917) 1 (83)Driver 2 (100) 0 (0)

Civil servant 12 (100) 0 (0)Daily laborer 49 (907) 5 (93)Housewife 18 (100) 0 (0)Student 19 (100) 0 (0)

Educational status

Illiterate 219 (952) 11 (48)

0181Only read and write 85 (100) 0 (0)Elementary school 42 (933) 3 (67)

High school 19 (905) 2 (95)Higher education 3 (100) 0 (0)

4 Malaria Research and Treatment

P falciparum40 (89)

P vivax5 (11)

Figure 1 Frequency of Plasmodium species at Metema hospitalNorthwest Ethiopia 2014

Table 3 Prevalence of VLmalaria and their coinfection amongVLsuspected patients at Metema hospital Northwest Ethiopia 2014

Variables and result VL () Malaria () VL-malariacoinfection ()

Negative 301 (784) 339 (883) 368 (958)Positive 83 (216) 45 (117) 16 (42)

hundred eighty (469) study participants have history oftravel fromMetema to any region of Ethiopia and vice versaOf these 10 (56) of them have VL-malaria coinfection Allstudy variables did not show statistical significance (Table 4)

4 Discussion

Visceral leishmaniasis and malaria coinfection may exist inendemic areas due to similarity in clinical manifestationsof the two diseases but their coinfection has been poorlyinvestigated In the present study the overall prevalenceof VL-malaria coinfection was 42 This is in agreementwith the study which is conducted in India 59 amongIndian patients with fever and splenomegaly [16] Howeverthis prevalence was lower as compared to study reported inUganda 19 [25]This variationmight be due to difference inthe VL and malaria prevalence which is 216 and 117 inthis study and 57 and 31 in Uganda respectively [25]

In this study prevalence of VL-malaria coinfection wasnonsignificantly higher in males than females A similarfinding was also reported in other studies [25ndash27]The higherprevalence rate might be due to the fact that males engage inactivities whichmake themmore prone to infectivemosquitoand sand fly bites as compared to females who are mostly athome and protected from such infective bites

Visceral leishmaniasis has been amajor health problem inNorthGondar especially in lowlands ofMetema andHumeraplains which are important endemic foci in Northwest ofEthiopia [28] In the present study its prevalence was 216which was consistent with the other study done in the same

study area 226 [21] however lower than the study inother areas of Ethiopia which was reported as 391 [29]The variation might be due to heterogeneity of the vectorsFollowing agricultural development in the region a largenumber of labor migrants from the different areas weremoved to the endemic areas for crop harvesting This led tooutbreaks of VL in many areas in the country which resultedin high morbidity and mortality [30]

Malaria is also one of the most public health problems inEthiopia The total land mass of the country is regarded asmalarious and about 68 of the total population is at risk ofmalaria infection [31] In this study the prevalence of malariawas 117 which is relatively lower than previous study donein the same study area (17) [22] The variation might bedue to difference in study participants The predominantPlasmodium species detected was P falciparum This was inagreement with other previous studies [22 32 33]

Visceral leishmaniasis-malaria coinfection was signifi-cantly higher in patients with the age groups of less thanfive years (119875 = 0004) followed by patients in the agegroups of fifteen to twenty-nine years This indicates thatchildren less than five years old are prone to acquire VL-malaria coinfections which might be associated with theirlow immune system On the other hand high prevalence ofVL-malaria coinfection within fifteen to twenty-nine yearsold might be associated with their daily activities Farmingis extensive in Metema due to the fact that young dailylaborers move to Metema from different areas for applicationof herbicide and for gathering of crops Because of hightemperature in this area daily activities are accomplishedespecially during night This may expose them to the bite ofmosquitoes and sand fly which means a more concentratedeffort should be given to educate these age groups about thisdisease and its vector

In this study majority of study subjects use their bednets However the prevalence of VL-malaria coinfection washigh in these subjects This might be due to improper andinfrequent use of their bed net or it might be due to lack ofimpregnating their bed nets regularly In the study area mostof study participants who were coinfected with VL-malariawere daily laborers followed by merchants This might beassociated with their daily activities which may expose themfor vector bite

This study is limited to the data obtained from the VLsuspected patients which may reduce the prevalence ofmalaria Moreover this study for VL diagnosis depends onlyon serological tests There is no microscopically confirmedparasitological data for VL To fill all these gaps there isa need for further study including all febrile patients withdifferent study design

In conclusion this study tries to see VL-malaria coin-fection for the first time and found 42 coinfection rateA significantly higher number of VL-malaria coinfectionswere showed in study subjects whose age was less thanfive years old Based on these findings we recommend thatmalaria screening be implemented for all VL patients wholive in malaria-endemic areas in order to promptly initiateantimalarial drug treatment Moreover to minimize thedisease burden health planners and administrators need to

Malaria Research and Treatment 5

Table 4 Associated factors of VL-malaria coinfection at Metema hospital Northwest Ethiopia 2014

Variables VL suspected cases119875 value

Not VL-malaria coinfected () VL-malaria coinfected ()Bed net useYes 279 (955) 13 (45) 0618No 89 (967) 3 (33)Sleep usuallyInside home 209 (963) 8 (37) 0592Outside home 158 (952) 8 (48)Lived in MetemaLess than 6 months 23 (958) 1 (42) 0999More than 6 months 345 (958) 15 (42)History of travelYes 170 (944) 10 (56) 0201No 198 (970) 6 (30)Seasonal migrant laborersYes 152 (962) 6 (38) 0762No 216 (956) 10 (44)

give intensive health education to increase the communityawareness about the two diseasesrsquo prevention and controlstrategies

Conflicts of Interest

The authors declared that they have no conflicts of interest

Authorsrsquo Contributions

GetachewFerede participated in conception anddesign of thestudy data collection and analysis interpretation of the find-ings drafting the paper and the write-up Ermias Diro SisayGetie Gebeyaw Getnet and Yegnasew Takele participated inconception and design of the study and interpretations of thefindings and reviewed the manuscript Yitayih Wondimenehand Anteneh Amsalu participated in conception and designof the study data analysis and interpretations of the findingsand reviewedmanuscript All authors reviewed and approvedthe final paper

Acknowledgments

The authors would like to acknowledge University of Gondarfor financial support and they also thank all the studyparticipants and all Metema hospital laboratory staffs fortheir cooperation during data collection

References

[1] RW Ashford P Desjeux and P deRaadt ldquoEstimation of popu-lation at risk of infection and number of cases of LeishmaniasisrdquoParasitology Today vol 8 no 3 pp 104-105 1992

[2] R SnowM Craig C Newton and R SteketeThePublic HealthBurden of Plasmodium Falciparum Malaria in Africa Derivingthe Numbers Forgarty International Center National Instituteof Health Bethesda MD USA 2003

[3] RW Snow C A Guerra AMNoor H YMyint and S I HayldquoThe global distribution of clinical episodes of Plasmodiumfalciparum malariardquo Nature vol 434 no 7030 pp 214ndash2172005

[4] World Health Organization World Malaria Report 2016httpappswhointirisbitstream1066525203819789241511711-engpdf

[5] J Lukes I L Mauricio G Schonian et al ldquoEvolutionary andgeographical history of the Leishmania donovani complex witha revision of current taxonomyrdquo Proceedings of the NationalAcademy of Sciences of the United States of America vol 104 no22 pp 9375ndash9380 2007

[6] H Gilles The Malaria Parasites Edward Arnold Bruce-Chwattrsquos Essential Malariology London UK 3rd edition 1993

[7] Tech Rep World Health Organization Vector Control forMalaria and Other Mosquito Born Diseases Technical ReportSeries Geneva 1995

[8] P Desjeux ldquoLeishmaniasis current situation and new perspec-tivesrdquo Comparative Immunology Microbiology and InfectiousDiseases vol 27 no 5 pp 305ndash318 2004

[9] World health Organization Malaria fact sheet [cited 2016]Available from httpwwwwhointithdiseasesmalariaen

[10] WHO World Malaria Report World Health organizationGeneva Switzerland 2010

[11] R E L Paul M Diallo and P T Brey ldquoMosquitoes and trans-mission ofmalaria parasites - Not just vectorsrdquoMalaria Journalvol 3 article no 39 2004

[12] Y Mueller D B Mbulamberi P Odermatt A Hoffmann LLoutan and F Chappuis ldquoRisk factors for in-hospital mortalityof visceral leishmaniasis patients in eastern Ugandardquo TropicalMedicine and International Health vol 14 no 8 pp 910ndash9172009

[13] J H Kolaczinski R Reithinger D T Worku et al ldquoRisk factorsof visceral leishmaniasis in East Africa A case-control study inPokot territory of Kenya and Ugandardquo International Journal ofEpidemiology vol 37 no 2 pp 344ndash352 2008

[14] P Beer A Harith L Deng S Semiao-Santos and B Chantal ldquoAkilling disease epidemic among displaced sudanese population

6 Malaria Research and Treatment

identified as visceral leishmaniasisrdquo The American Journal ofTropical Medicine and Hygiene vol 44 pp 283ndash289 1991

[15] C Sarker K ChowdhuryN SiddiquiM Jamal and S RahmanldquoClinical profile of kala-azar in adults as seen in Mymen-singh medical college hospital Mymensingh BangladeshrdquoMy-mensingh Medical Journal vol 12 pp 41ndash44 2003

[16] A Nandy M Addy S K Guha A K Maji H M Chauahuriand P Chatterjee ldquoCo-existent kala-azar and malaria in IndiardquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 89 no 5 p 516 1995

[17] K Saha D Chattopadhya and D Kulpati ldquoConcomitant kala-azar malaria and progressive unstable indeterminate leprosy inan 8-year-old childrdquo Journal of Tropical Pediatrics vol 44 pp247-248 1998

[18] S Sah S Sharma and S Rani ldquoKala azar associated withmalariardquo Archives of Pathology amp Laboratory Medicine vol 126p 383 2002

[19] J Woodrow J Hartzell J Czarnik D Brett-Major and GWortmann ldquoCutaneous and presumed visceral leishmaniasisin a soldier deployed to Afghanistanrdquo International Journal ofGeneral Medicine vol 8 article 43 2006

[20] A K Ab Rahman and F H Abdullah ldquoVisceral leishmaniasis(kala-azar) andmalaria coinfection in an immigrant in the stateof TerengganuMalaysia A case reportrdquo Journal ofMicrobiologyImmunology and Infection vol 44 no 1 pp 72ndash76 2011

[21] S Yeromenesh W Yitayih W Habtamu and F GetachewldquoTrend analysis of visceral leishmaniasis in Metema HospitalNorthwest Ethiopiardquo Journal of Epidemiology and Public HealthReviews vol 1 pp 2471ndash8211 2016

[22] F Getachew W Abiyu G Alemtegna A Ali H Tarekegn AYenus et al ldquoPrevalence ofmalaria fromblood smears examina-tion a seven-year retrospective study from Metema HospitalNorthwest EthiopiardquoMalaria Research and Treatment vol 2013Article ID 704730 5 pages 2013

[23] M Siddig H Ghalib D Shillington E Petersen and S KhidirldquoVisceral leishmaniasis in Sudan Clinical featuresrdquoTropical andGeographical Medicine vol 42 pp 107ndash112 1990

[24] S Sundar S G Reed V P Singh P C K Kumar and H WMurray ldquoRapid accurate field diagnosis of Indian visceral leish-maniasisrdquo Lancet vol 351 no 9102 pp 563ndash565 1998

[25] E van den Bogaart M M Z Berkhout E R Adams et alldquoPrevalence features and risk factors for malaria co-infectionsamongst visceral leishmaniasis patients from Amudat hospitalUgandardquo PLoS Neglected Tropical Diseases vol 6 no 4 ArticleID e1617 2012

[26] S Bashaye N Nombela and D Argaw ldquoRisk factors forvisceral leishmaniasis in a new epidemic site in Amhara regionEthiopiardquo The American Journal of Tropical Medicine andHygiene vol 81 pp 34ndash39 2009

[27] B Bucheton M M Kheir S H El-Safi et al ldquoThe interplaybetween environmental and host factors during an outbreak ofvisceral leishmaniasis in eastern SudanrdquoMicrobes and Infectionvol 4 no 14 pp 1449ndash1457 2002

[28] A Hailu and D Frommel ldquoLeishmaniasis in Ethiopiardquo in TheEcology of Health and Disease in Ethiopia H Kloos and Z AZein Eds pp 375ndash388 Westview Press Boulder Colo USA1993

[29] YWondimeneh Y Takele A Atnafu G Ferede andDMuluyeldquoTrend analysis of visceral leishmaniasis at Addis Zemen healthcenter northwest Ethiopiardquo BioMed Research International vol2014 Article ID 545393 2014

[30] D Abyot K Solomon and AndargachewModule on Leishma-niasis for the Ethiopian Health Center Team Debub UniversitEthiopia 2005

[31] FMoH National Five Year Strategic Plan for Malaria Preventionand Control in Ethiopia 2006-2010 Ministry of Health AddisAbaba Ethiopia 2006

[32] Federal Republic of Ethiopia Ministry of HealthNational GuideLines Federal Republic of Ethiopia Ministry of Health AddisAbeba Ethiopia 3rd edition 2012

[33] K Karunamoorthi and M Bekele ldquoPrevalence of malaria fromperipheral blood smears examination a 1-year retrospectivestudy from the Serbo Health Center Kersa Woreda EthiopiardquoJournal of Infection and Public Health vol 2 no 4 pp 171ndash1762009

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Page 2: Visceral Leishmaniasis-Malaria Coinfection and Their ...downloads.hindawi.com/archive/2017/6816913.pdf · malaria.Individualswholiveintheurban8(5.3%)andrural 8(3.4%)werecoinfectedwithVL-malaria.5dailylaborers

2 Malaria Research and Treatment

as introducing an enemy of the vector to the environmentusing the sterile male technique destroying the habitat of thevector or spraying pesticides [7]

Visceral leishmaniasis andmalaria are the twomajor life-threatening parasitic diseases that still remain a serious publichealth problem particularly in endemic areas [8 9] Differ-ential diagnosis of VL often includes malaria among otherfebrile splenomegalies due to its clinical overlap Malariain fact is widespread in tropical and subtropical regions ofthe world where it accounts for more than 250 million casesannually the vast majority of which occurs among childrenunder 5 years old [10] Transmission can occur throughoutthe year or be seasonal depending on the region [11] In thelatter case transmission seasons for VL and malaria may notcoincide but the two diseases still overlap due to the longerincubation period of VL The overlap in disease distributionsuggests the two diseases could cooccur in the same host

Visceral leishmaniasis and malaria coinfections havebeen reported across various African and Asian countrieswith the prevalence among VL patients ranging from 208and 64 in Uganda [12 13] to 107 in Sudan [14] and 12in Bangladesh [15] and a rate of 59 among Indian patientswith fever and splenomegaly [16] with the exception ofthe case-reports [17ndash20] whose evidence remains anecdotalDespite high prevalence of the VL [21] and malaria [22]in the study area their coinfection is unknown Thereforethis study was designed to document the prevalence ofVL-malaria coinfection and their associated factors amongpatients attending Metema hospital

2 Materials and Methods

21 Study Area and Period This study was conducted atMetema hospital from January 2014 to June 2014 Metema isa town in Northwestern Ethiopia on the border with SudanThis town is located in the North Gondar AdministrativeZone Amhara region 897 km North of Addis Ababa and197 km from the ancient city of Gondar and it has a latitudeand longitude of 12∘581015840N 36∘121015840E with an elevation of 685meters above sea level This area is malarious and has casesof VL

22 Study Design Study Population and Sampling TechniqueA cross-sectional study was carried out atMetema hospital todetermine VL-malaria coinfection among all clinically sus-pected VL patients Visceral leishmaniasis suspected patientswho have taken treatment for malaria andor VL for the lasttwo weeks were excluded from the study Visceral leishma-niasis suspects are defined as those individuals who developclinical evidence of infection usually have fever loss ofappetite (anorexia) weight loss fatigue anemia enlargement(swelling) of the spleen and liver and abnormal blood tests[23]

23 Data Collection and Processing Well-structured ques-tionnaire was prepared in English version by the researchteam It was translated later into the local language AmharicThe questionnaire addresses patientsrsquo sociodemographicinformation and associated factors A pretest was conducted

among five percent of the total sample size by trained datacollectors and any ambiguous questions and repetitive ideaswere corrected Additional response categories were addedbased on the pretest findings

24 Parasitological Techniques After interviewing the pa-tients fresh peripheral whole blood sample was tested by therk39 ICT with sensitivity of 100 and specificity of 98 [24]for diagnosis of VL and Giemsa stain microscopic examina-tion of thick and thin blood smears for malaria detection andspecies differentiation was performed systematically

25 Data Analysis Data were entered and analyzed usingSPSS version 20 software The Pearson Chi-square test wasemployed to examine associated factors with the coinfection119875 value lt 005 was considered statistically significant

26 Ethical Consideration Ethical clearance was obtainedfrom Institutional Review Board of University of GondarWritten informed consent was obtained from each of thevolunteer study subjects or guardian of children Patientinformation was anonymized and deidentified prior to anal-ysis Positive results were given for physicians working in thehospital for treatment according to the national treatmentguideline

3 Results

31 Sociodemographic Characteristics A total of 384 VLsuspected participants were included in this study Out ofthese 334 (87) were males The mean (standard deviation)age was 281 (118) years (ranging from 2 to 78 years) Majority227 (591) of the study participants were in the age group of15ndash29 years old Among the study groups 230 (599) wereilliterate and 267 (695) were farmers followed by 54 (141)daily laborersThemajority of study participants 234 (609)were from rural residents (Table 1)

32 Visceral Leishmaniasis-Malaria Coinfection and Sociode-mographic Characteristics Out of the total VL suspectedcases 2 (333) VL-malaria coinfections were found in theage groups of lt5 years followed by 9 (4) within 15ndash29 yearsold (119875=0004) Visceral leishmaniasis-malaria coinfection bygender showed that 15 (45) ofmales were coinfected byVL-malaria Individuals who live in the urban 8 (53) and rural8 (34) were coinfected with VL-malaria 5 daily laborers(93) were coinfected with VL-malaria (Table 2)

33 Prevalence of VL-Malaria Coinfection Out of the totalVL suspected patients the overall prevalence of VL-malariacoinfection was 16 (42) The prevalence of VL was 83(216) while the prevalence of malaria was 45 (117)(Table 3) Of the malaria positive patients 40 (89) werepositive for P falciparum and 5 (11) were positive for P vivax(Figure 1)

34 Associated Factors for VL-Malaria Coinfection From thetotal study participants 292 (76) were used bed nets Ofthese 13 (45) patients were VL-malaria coinfected Mostof the study participants 217 (565) sleep inside home One

Malaria Research and Treatment 3

Table 1 Sociodemographic characteristics of the study participants at Metema hospital Northwest Ethiopia 2014

Characteristic Frequency Percentage

Age (years)

lt5 6 165ndash14 20 5215ndash29 227 59130ndash44 99 258ge45 32 83

Gender Male 334 870Female 50 130

Residence Rural 234 609Urban 150 391

Occupational status

Farmer 267 695Merchant 12 31Driver 2 05

Civil servant 12 31Daily laborer 54 141Housewife 18 47Student 19 49

Educational status

Illiterate 230 599Only read and write 85 221Elementary school 45 117

High school 21 55Collegeuniversities 3 08

Table 2 Sociodemographic characteristics of the study participants in relation to VL-malaria coinfection at Metema Hospital NorthwestEthiopia 2014

VariablesVL suspected cases

119875 valueNot VL-malariacoinfected ()

VL-malariacoinfected ()

Age

lt5 4 (667) 2 (333)

00045ndash14 20 (100) 0 (0)15ndash29 218 (960) 9 (40)30ndash44 94 (950) 5 (50)ge45 32 (100) 0 (0)

Gender Male 319 (955) 15 (45) 0411Female 49 (980) 1 (20)

Residence Rural 226 (966) 8 (34) 0360Urban 142 (947) 8 (53)

Occupation status

Farmer 257 (963) 10 (37)

0384

Merchant 11 (917) 1 (83)Driver 2 (100) 0 (0)

Civil servant 12 (100) 0 (0)Daily laborer 49 (907) 5 (93)Housewife 18 (100) 0 (0)Student 19 (100) 0 (0)

Educational status

Illiterate 219 (952) 11 (48)

0181Only read and write 85 (100) 0 (0)Elementary school 42 (933) 3 (67)

High school 19 (905) 2 (95)Higher education 3 (100) 0 (0)

4 Malaria Research and Treatment

P falciparum40 (89)

P vivax5 (11)

Figure 1 Frequency of Plasmodium species at Metema hospitalNorthwest Ethiopia 2014

Table 3 Prevalence of VLmalaria and their coinfection amongVLsuspected patients at Metema hospital Northwest Ethiopia 2014

Variables and result VL () Malaria () VL-malariacoinfection ()

Negative 301 (784) 339 (883) 368 (958)Positive 83 (216) 45 (117) 16 (42)

hundred eighty (469) study participants have history oftravel fromMetema to any region of Ethiopia and vice versaOf these 10 (56) of them have VL-malaria coinfection Allstudy variables did not show statistical significance (Table 4)

4 Discussion

Visceral leishmaniasis and malaria coinfection may exist inendemic areas due to similarity in clinical manifestationsof the two diseases but their coinfection has been poorlyinvestigated In the present study the overall prevalenceof VL-malaria coinfection was 42 This is in agreementwith the study which is conducted in India 59 amongIndian patients with fever and splenomegaly [16] Howeverthis prevalence was lower as compared to study reported inUganda 19 [25]This variationmight be due to difference inthe VL and malaria prevalence which is 216 and 117 inthis study and 57 and 31 in Uganda respectively [25]

In this study prevalence of VL-malaria coinfection wasnonsignificantly higher in males than females A similarfinding was also reported in other studies [25ndash27]The higherprevalence rate might be due to the fact that males engage inactivities whichmake themmore prone to infectivemosquitoand sand fly bites as compared to females who are mostly athome and protected from such infective bites

Visceral leishmaniasis has been amajor health problem inNorthGondar especially in lowlands ofMetema andHumeraplains which are important endemic foci in Northwest ofEthiopia [28] In the present study its prevalence was 216which was consistent with the other study done in the same

study area 226 [21] however lower than the study inother areas of Ethiopia which was reported as 391 [29]The variation might be due to heterogeneity of the vectorsFollowing agricultural development in the region a largenumber of labor migrants from the different areas weremoved to the endemic areas for crop harvesting This led tooutbreaks of VL in many areas in the country which resultedin high morbidity and mortality [30]

Malaria is also one of the most public health problems inEthiopia The total land mass of the country is regarded asmalarious and about 68 of the total population is at risk ofmalaria infection [31] In this study the prevalence of malariawas 117 which is relatively lower than previous study donein the same study area (17) [22] The variation might bedue to difference in study participants The predominantPlasmodium species detected was P falciparum This was inagreement with other previous studies [22 32 33]

Visceral leishmaniasis-malaria coinfection was signifi-cantly higher in patients with the age groups of less thanfive years (119875 = 0004) followed by patients in the agegroups of fifteen to twenty-nine years This indicates thatchildren less than five years old are prone to acquire VL-malaria coinfections which might be associated with theirlow immune system On the other hand high prevalence ofVL-malaria coinfection within fifteen to twenty-nine yearsold might be associated with their daily activities Farmingis extensive in Metema due to the fact that young dailylaborers move to Metema from different areas for applicationof herbicide and for gathering of crops Because of hightemperature in this area daily activities are accomplishedespecially during night This may expose them to the bite ofmosquitoes and sand fly which means a more concentratedeffort should be given to educate these age groups about thisdisease and its vector

In this study majority of study subjects use their bednets However the prevalence of VL-malaria coinfection washigh in these subjects This might be due to improper andinfrequent use of their bed net or it might be due to lack ofimpregnating their bed nets regularly In the study area mostof study participants who were coinfected with VL-malariawere daily laborers followed by merchants This might beassociated with their daily activities which may expose themfor vector bite

This study is limited to the data obtained from the VLsuspected patients which may reduce the prevalence ofmalaria Moreover this study for VL diagnosis depends onlyon serological tests There is no microscopically confirmedparasitological data for VL To fill all these gaps there isa need for further study including all febrile patients withdifferent study design

In conclusion this study tries to see VL-malaria coin-fection for the first time and found 42 coinfection rateA significantly higher number of VL-malaria coinfectionswere showed in study subjects whose age was less thanfive years old Based on these findings we recommend thatmalaria screening be implemented for all VL patients wholive in malaria-endemic areas in order to promptly initiateantimalarial drug treatment Moreover to minimize thedisease burden health planners and administrators need to

Malaria Research and Treatment 5

Table 4 Associated factors of VL-malaria coinfection at Metema hospital Northwest Ethiopia 2014

Variables VL suspected cases119875 value

Not VL-malaria coinfected () VL-malaria coinfected ()Bed net useYes 279 (955) 13 (45) 0618No 89 (967) 3 (33)Sleep usuallyInside home 209 (963) 8 (37) 0592Outside home 158 (952) 8 (48)Lived in MetemaLess than 6 months 23 (958) 1 (42) 0999More than 6 months 345 (958) 15 (42)History of travelYes 170 (944) 10 (56) 0201No 198 (970) 6 (30)Seasonal migrant laborersYes 152 (962) 6 (38) 0762No 216 (956) 10 (44)

give intensive health education to increase the communityawareness about the two diseasesrsquo prevention and controlstrategies

Conflicts of Interest

The authors declared that they have no conflicts of interest

Authorsrsquo Contributions

GetachewFerede participated in conception anddesign of thestudy data collection and analysis interpretation of the find-ings drafting the paper and the write-up Ermias Diro SisayGetie Gebeyaw Getnet and Yegnasew Takele participated inconception and design of the study and interpretations of thefindings and reviewed the manuscript Yitayih Wondimenehand Anteneh Amsalu participated in conception and designof the study data analysis and interpretations of the findingsand reviewedmanuscript All authors reviewed and approvedthe final paper

Acknowledgments

The authors would like to acknowledge University of Gondarfor financial support and they also thank all the studyparticipants and all Metema hospital laboratory staffs fortheir cooperation during data collection

References

[1] RW Ashford P Desjeux and P deRaadt ldquoEstimation of popu-lation at risk of infection and number of cases of LeishmaniasisrdquoParasitology Today vol 8 no 3 pp 104-105 1992

[2] R SnowM Craig C Newton and R SteketeThePublic HealthBurden of Plasmodium Falciparum Malaria in Africa Derivingthe Numbers Forgarty International Center National Instituteof Health Bethesda MD USA 2003

[3] RW Snow C A Guerra AMNoor H YMyint and S I HayldquoThe global distribution of clinical episodes of Plasmodiumfalciparum malariardquo Nature vol 434 no 7030 pp 214ndash2172005

[4] World Health Organization World Malaria Report 2016httpappswhointirisbitstream1066525203819789241511711-engpdf

[5] J Lukes I L Mauricio G Schonian et al ldquoEvolutionary andgeographical history of the Leishmania donovani complex witha revision of current taxonomyrdquo Proceedings of the NationalAcademy of Sciences of the United States of America vol 104 no22 pp 9375ndash9380 2007

[6] H Gilles The Malaria Parasites Edward Arnold Bruce-Chwattrsquos Essential Malariology London UK 3rd edition 1993

[7] Tech Rep World Health Organization Vector Control forMalaria and Other Mosquito Born Diseases Technical ReportSeries Geneva 1995

[8] P Desjeux ldquoLeishmaniasis current situation and new perspec-tivesrdquo Comparative Immunology Microbiology and InfectiousDiseases vol 27 no 5 pp 305ndash318 2004

[9] World health Organization Malaria fact sheet [cited 2016]Available from httpwwwwhointithdiseasesmalariaen

[10] WHO World Malaria Report World Health organizationGeneva Switzerland 2010

[11] R E L Paul M Diallo and P T Brey ldquoMosquitoes and trans-mission ofmalaria parasites - Not just vectorsrdquoMalaria Journalvol 3 article no 39 2004

[12] Y Mueller D B Mbulamberi P Odermatt A Hoffmann LLoutan and F Chappuis ldquoRisk factors for in-hospital mortalityof visceral leishmaniasis patients in eastern Ugandardquo TropicalMedicine and International Health vol 14 no 8 pp 910ndash9172009

[13] J H Kolaczinski R Reithinger D T Worku et al ldquoRisk factorsof visceral leishmaniasis in East Africa A case-control study inPokot territory of Kenya and Ugandardquo International Journal ofEpidemiology vol 37 no 2 pp 344ndash352 2008

[14] P Beer A Harith L Deng S Semiao-Santos and B Chantal ldquoAkilling disease epidemic among displaced sudanese population

6 Malaria Research and Treatment

identified as visceral leishmaniasisrdquo The American Journal ofTropical Medicine and Hygiene vol 44 pp 283ndash289 1991

[15] C Sarker K ChowdhuryN SiddiquiM Jamal and S RahmanldquoClinical profile of kala-azar in adults as seen in Mymen-singh medical college hospital Mymensingh BangladeshrdquoMy-mensingh Medical Journal vol 12 pp 41ndash44 2003

[16] A Nandy M Addy S K Guha A K Maji H M Chauahuriand P Chatterjee ldquoCo-existent kala-azar and malaria in IndiardquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 89 no 5 p 516 1995

[17] K Saha D Chattopadhya and D Kulpati ldquoConcomitant kala-azar malaria and progressive unstable indeterminate leprosy inan 8-year-old childrdquo Journal of Tropical Pediatrics vol 44 pp247-248 1998

[18] S Sah S Sharma and S Rani ldquoKala azar associated withmalariardquo Archives of Pathology amp Laboratory Medicine vol 126p 383 2002

[19] J Woodrow J Hartzell J Czarnik D Brett-Major and GWortmann ldquoCutaneous and presumed visceral leishmaniasisin a soldier deployed to Afghanistanrdquo International Journal ofGeneral Medicine vol 8 article 43 2006

[20] A K Ab Rahman and F H Abdullah ldquoVisceral leishmaniasis(kala-azar) andmalaria coinfection in an immigrant in the stateof TerengganuMalaysia A case reportrdquo Journal ofMicrobiologyImmunology and Infection vol 44 no 1 pp 72ndash76 2011

[21] S Yeromenesh W Yitayih W Habtamu and F GetachewldquoTrend analysis of visceral leishmaniasis in Metema HospitalNorthwest Ethiopiardquo Journal of Epidemiology and Public HealthReviews vol 1 pp 2471ndash8211 2016

[22] F Getachew W Abiyu G Alemtegna A Ali H Tarekegn AYenus et al ldquoPrevalence ofmalaria fromblood smears examina-tion a seven-year retrospective study from Metema HospitalNorthwest EthiopiardquoMalaria Research and Treatment vol 2013Article ID 704730 5 pages 2013

[23] M Siddig H Ghalib D Shillington E Petersen and S KhidirldquoVisceral leishmaniasis in Sudan Clinical featuresrdquoTropical andGeographical Medicine vol 42 pp 107ndash112 1990

[24] S Sundar S G Reed V P Singh P C K Kumar and H WMurray ldquoRapid accurate field diagnosis of Indian visceral leish-maniasisrdquo Lancet vol 351 no 9102 pp 563ndash565 1998

[25] E van den Bogaart M M Z Berkhout E R Adams et alldquoPrevalence features and risk factors for malaria co-infectionsamongst visceral leishmaniasis patients from Amudat hospitalUgandardquo PLoS Neglected Tropical Diseases vol 6 no 4 ArticleID e1617 2012

[26] S Bashaye N Nombela and D Argaw ldquoRisk factors forvisceral leishmaniasis in a new epidemic site in Amhara regionEthiopiardquo The American Journal of Tropical Medicine andHygiene vol 81 pp 34ndash39 2009

[27] B Bucheton M M Kheir S H El-Safi et al ldquoThe interplaybetween environmental and host factors during an outbreak ofvisceral leishmaniasis in eastern SudanrdquoMicrobes and Infectionvol 4 no 14 pp 1449ndash1457 2002

[28] A Hailu and D Frommel ldquoLeishmaniasis in Ethiopiardquo in TheEcology of Health and Disease in Ethiopia H Kloos and Z AZein Eds pp 375ndash388 Westview Press Boulder Colo USA1993

[29] YWondimeneh Y Takele A Atnafu G Ferede andDMuluyeldquoTrend analysis of visceral leishmaniasis at Addis Zemen healthcenter northwest Ethiopiardquo BioMed Research International vol2014 Article ID 545393 2014

[30] D Abyot K Solomon and AndargachewModule on Leishma-niasis for the Ethiopian Health Center Team Debub UniversitEthiopia 2005

[31] FMoH National Five Year Strategic Plan for Malaria Preventionand Control in Ethiopia 2006-2010 Ministry of Health AddisAbaba Ethiopia 2006

[32] Federal Republic of Ethiopia Ministry of HealthNational GuideLines Federal Republic of Ethiopia Ministry of Health AddisAbeba Ethiopia 3rd edition 2012

[33] K Karunamoorthi and M Bekele ldquoPrevalence of malaria fromperipheral blood smears examination a 1-year retrospectivestudy from the Serbo Health Center Kersa Woreda EthiopiardquoJournal of Infection and Public Health vol 2 no 4 pp 171ndash1762009

Submit your manuscripts athttpswwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 3: Visceral Leishmaniasis-Malaria Coinfection and Their ...downloads.hindawi.com/archive/2017/6816913.pdf · malaria.Individualswholiveintheurban8(5.3%)andrural 8(3.4%)werecoinfectedwithVL-malaria.5dailylaborers

Malaria Research and Treatment 3

Table 1 Sociodemographic characteristics of the study participants at Metema hospital Northwest Ethiopia 2014

Characteristic Frequency Percentage

Age (years)

lt5 6 165ndash14 20 5215ndash29 227 59130ndash44 99 258ge45 32 83

Gender Male 334 870Female 50 130

Residence Rural 234 609Urban 150 391

Occupational status

Farmer 267 695Merchant 12 31Driver 2 05

Civil servant 12 31Daily laborer 54 141Housewife 18 47Student 19 49

Educational status

Illiterate 230 599Only read and write 85 221Elementary school 45 117

High school 21 55Collegeuniversities 3 08

Table 2 Sociodemographic characteristics of the study participants in relation to VL-malaria coinfection at Metema Hospital NorthwestEthiopia 2014

VariablesVL suspected cases

119875 valueNot VL-malariacoinfected ()

VL-malariacoinfected ()

Age

lt5 4 (667) 2 (333)

00045ndash14 20 (100) 0 (0)15ndash29 218 (960) 9 (40)30ndash44 94 (950) 5 (50)ge45 32 (100) 0 (0)

Gender Male 319 (955) 15 (45) 0411Female 49 (980) 1 (20)

Residence Rural 226 (966) 8 (34) 0360Urban 142 (947) 8 (53)

Occupation status

Farmer 257 (963) 10 (37)

0384

Merchant 11 (917) 1 (83)Driver 2 (100) 0 (0)

Civil servant 12 (100) 0 (0)Daily laborer 49 (907) 5 (93)Housewife 18 (100) 0 (0)Student 19 (100) 0 (0)

Educational status

Illiterate 219 (952) 11 (48)

0181Only read and write 85 (100) 0 (0)Elementary school 42 (933) 3 (67)

High school 19 (905) 2 (95)Higher education 3 (100) 0 (0)

4 Malaria Research and Treatment

P falciparum40 (89)

P vivax5 (11)

Figure 1 Frequency of Plasmodium species at Metema hospitalNorthwest Ethiopia 2014

Table 3 Prevalence of VLmalaria and their coinfection amongVLsuspected patients at Metema hospital Northwest Ethiopia 2014

Variables and result VL () Malaria () VL-malariacoinfection ()

Negative 301 (784) 339 (883) 368 (958)Positive 83 (216) 45 (117) 16 (42)

hundred eighty (469) study participants have history oftravel fromMetema to any region of Ethiopia and vice versaOf these 10 (56) of them have VL-malaria coinfection Allstudy variables did not show statistical significance (Table 4)

4 Discussion

Visceral leishmaniasis and malaria coinfection may exist inendemic areas due to similarity in clinical manifestationsof the two diseases but their coinfection has been poorlyinvestigated In the present study the overall prevalenceof VL-malaria coinfection was 42 This is in agreementwith the study which is conducted in India 59 amongIndian patients with fever and splenomegaly [16] Howeverthis prevalence was lower as compared to study reported inUganda 19 [25]This variationmight be due to difference inthe VL and malaria prevalence which is 216 and 117 inthis study and 57 and 31 in Uganda respectively [25]

In this study prevalence of VL-malaria coinfection wasnonsignificantly higher in males than females A similarfinding was also reported in other studies [25ndash27]The higherprevalence rate might be due to the fact that males engage inactivities whichmake themmore prone to infectivemosquitoand sand fly bites as compared to females who are mostly athome and protected from such infective bites

Visceral leishmaniasis has been amajor health problem inNorthGondar especially in lowlands ofMetema andHumeraplains which are important endemic foci in Northwest ofEthiopia [28] In the present study its prevalence was 216which was consistent with the other study done in the same

study area 226 [21] however lower than the study inother areas of Ethiopia which was reported as 391 [29]The variation might be due to heterogeneity of the vectorsFollowing agricultural development in the region a largenumber of labor migrants from the different areas weremoved to the endemic areas for crop harvesting This led tooutbreaks of VL in many areas in the country which resultedin high morbidity and mortality [30]

Malaria is also one of the most public health problems inEthiopia The total land mass of the country is regarded asmalarious and about 68 of the total population is at risk ofmalaria infection [31] In this study the prevalence of malariawas 117 which is relatively lower than previous study donein the same study area (17) [22] The variation might bedue to difference in study participants The predominantPlasmodium species detected was P falciparum This was inagreement with other previous studies [22 32 33]

Visceral leishmaniasis-malaria coinfection was signifi-cantly higher in patients with the age groups of less thanfive years (119875 = 0004) followed by patients in the agegroups of fifteen to twenty-nine years This indicates thatchildren less than five years old are prone to acquire VL-malaria coinfections which might be associated with theirlow immune system On the other hand high prevalence ofVL-malaria coinfection within fifteen to twenty-nine yearsold might be associated with their daily activities Farmingis extensive in Metema due to the fact that young dailylaborers move to Metema from different areas for applicationof herbicide and for gathering of crops Because of hightemperature in this area daily activities are accomplishedespecially during night This may expose them to the bite ofmosquitoes and sand fly which means a more concentratedeffort should be given to educate these age groups about thisdisease and its vector

In this study majority of study subjects use their bednets However the prevalence of VL-malaria coinfection washigh in these subjects This might be due to improper andinfrequent use of their bed net or it might be due to lack ofimpregnating their bed nets regularly In the study area mostof study participants who were coinfected with VL-malariawere daily laborers followed by merchants This might beassociated with their daily activities which may expose themfor vector bite

This study is limited to the data obtained from the VLsuspected patients which may reduce the prevalence ofmalaria Moreover this study for VL diagnosis depends onlyon serological tests There is no microscopically confirmedparasitological data for VL To fill all these gaps there isa need for further study including all febrile patients withdifferent study design

In conclusion this study tries to see VL-malaria coin-fection for the first time and found 42 coinfection rateA significantly higher number of VL-malaria coinfectionswere showed in study subjects whose age was less thanfive years old Based on these findings we recommend thatmalaria screening be implemented for all VL patients wholive in malaria-endemic areas in order to promptly initiateantimalarial drug treatment Moreover to minimize thedisease burden health planners and administrators need to

Malaria Research and Treatment 5

Table 4 Associated factors of VL-malaria coinfection at Metema hospital Northwest Ethiopia 2014

Variables VL suspected cases119875 value

Not VL-malaria coinfected () VL-malaria coinfected ()Bed net useYes 279 (955) 13 (45) 0618No 89 (967) 3 (33)Sleep usuallyInside home 209 (963) 8 (37) 0592Outside home 158 (952) 8 (48)Lived in MetemaLess than 6 months 23 (958) 1 (42) 0999More than 6 months 345 (958) 15 (42)History of travelYes 170 (944) 10 (56) 0201No 198 (970) 6 (30)Seasonal migrant laborersYes 152 (962) 6 (38) 0762No 216 (956) 10 (44)

give intensive health education to increase the communityawareness about the two diseasesrsquo prevention and controlstrategies

Conflicts of Interest

The authors declared that they have no conflicts of interest

Authorsrsquo Contributions

GetachewFerede participated in conception anddesign of thestudy data collection and analysis interpretation of the find-ings drafting the paper and the write-up Ermias Diro SisayGetie Gebeyaw Getnet and Yegnasew Takele participated inconception and design of the study and interpretations of thefindings and reviewed the manuscript Yitayih Wondimenehand Anteneh Amsalu participated in conception and designof the study data analysis and interpretations of the findingsand reviewedmanuscript All authors reviewed and approvedthe final paper

Acknowledgments

The authors would like to acknowledge University of Gondarfor financial support and they also thank all the studyparticipants and all Metema hospital laboratory staffs fortheir cooperation during data collection

References

[1] RW Ashford P Desjeux and P deRaadt ldquoEstimation of popu-lation at risk of infection and number of cases of LeishmaniasisrdquoParasitology Today vol 8 no 3 pp 104-105 1992

[2] R SnowM Craig C Newton and R SteketeThePublic HealthBurden of Plasmodium Falciparum Malaria in Africa Derivingthe Numbers Forgarty International Center National Instituteof Health Bethesda MD USA 2003

[3] RW Snow C A Guerra AMNoor H YMyint and S I HayldquoThe global distribution of clinical episodes of Plasmodiumfalciparum malariardquo Nature vol 434 no 7030 pp 214ndash2172005

[4] World Health Organization World Malaria Report 2016httpappswhointirisbitstream1066525203819789241511711-engpdf

[5] J Lukes I L Mauricio G Schonian et al ldquoEvolutionary andgeographical history of the Leishmania donovani complex witha revision of current taxonomyrdquo Proceedings of the NationalAcademy of Sciences of the United States of America vol 104 no22 pp 9375ndash9380 2007

[6] H Gilles The Malaria Parasites Edward Arnold Bruce-Chwattrsquos Essential Malariology London UK 3rd edition 1993

[7] Tech Rep World Health Organization Vector Control forMalaria and Other Mosquito Born Diseases Technical ReportSeries Geneva 1995

[8] P Desjeux ldquoLeishmaniasis current situation and new perspec-tivesrdquo Comparative Immunology Microbiology and InfectiousDiseases vol 27 no 5 pp 305ndash318 2004

[9] World health Organization Malaria fact sheet [cited 2016]Available from httpwwwwhointithdiseasesmalariaen

[10] WHO World Malaria Report World Health organizationGeneva Switzerland 2010

[11] R E L Paul M Diallo and P T Brey ldquoMosquitoes and trans-mission ofmalaria parasites - Not just vectorsrdquoMalaria Journalvol 3 article no 39 2004

[12] Y Mueller D B Mbulamberi P Odermatt A Hoffmann LLoutan and F Chappuis ldquoRisk factors for in-hospital mortalityof visceral leishmaniasis patients in eastern Ugandardquo TropicalMedicine and International Health vol 14 no 8 pp 910ndash9172009

[13] J H Kolaczinski R Reithinger D T Worku et al ldquoRisk factorsof visceral leishmaniasis in East Africa A case-control study inPokot territory of Kenya and Ugandardquo International Journal ofEpidemiology vol 37 no 2 pp 344ndash352 2008

[14] P Beer A Harith L Deng S Semiao-Santos and B Chantal ldquoAkilling disease epidemic among displaced sudanese population

6 Malaria Research and Treatment

identified as visceral leishmaniasisrdquo The American Journal ofTropical Medicine and Hygiene vol 44 pp 283ndash289 1991

[15] C Sarker K ChowdhuryN SiddiquiM Jamal and S RahmanldquoClinical profile of kala-azar in adults as seen in Mymen-singh medical college hospital Mymensingh BangladeshrdquoMy-mensingh Medical Journal vol 12 pp 41ndash44 2003

[16] A Nandy M Addy S K Guha A K Maji H M Chauahuriand P Chatterjee ldquoCo-existent kala-azar and malaria in IndiardquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 89 no 5 p 516 1995

[17] K Saha D Chattopadhya and D Kulpati ldquoConcomitant kala-azar malaria and progressive unstable indeterminate leprosy inan 8-year-old childrdquo Journal of Tropical Pediatrics vol 44 pp247-248 1998

[18] S Sah S Sharma and S Rani ldquoKala azar associated withmalariardquo Archives of Pathology amp Laboratory Medicine vol 126p 383 2002

[19] J Woodrow J Hartzell J Czarnik D Brett-Major and GWortmann ldquoCutaneous and presumed visceral leishmaniasisin a soldier deployed to Afghanistanrdquo International Journal ofGeneral Medicine vol 8 article 43 2006

[20] A K Ab Rahman and F H Abdullah ldquoVisceral leishmaniasis(kala-azar) andmalaria coinfection in an immigrant in the stateof TerengganuMalaysia A case reportrdquo Journal ofMicrobiologyImmunology and Infection vol 44 no 1 pp 72ndash76 2011

[21] S Yeromenesh W Yitayih W Habtamu and F GetachewldquoTrend analysis of visceral leishmaniasis in Metema HospitalNorthwest Ethiopiardquo Journal of Epidemiology and Public HealthReviews vol 1 pp 2471ndash8211 2016

[22] F Getachew W Abiyu G Alemtegna A Ali H Tarekegn AYenus et al ldquoPrevalence ofmalaria fromblood smears examina-tion a seven-year retrospective study from Metema HospitalNorthwest EthiopiardquoMalaria Research and Treatment vol 2013Article ID 704730 5 pages 2013

[23] M Siddig H Ghalib D Shillington E Petersen and S KhidirldquoVisceral leishmaniasis in Sudan Clinical featuresrdquoTropical andGeographical Medicine vol 42 pp 107ndash112 1990

[24] S Sundar S G Reed V P Singh P C K Kumar and H WMurray ldquoRapid accurate field diagnosis of Indian visceral leish-maniasisrdquo Lancet vol 351 no 9102 pp 563ndash565 1998

[25] E van den Bogaart M M Z Berkhout E R Adams et alldquoPrevalence features and risk factors for malaria co-infectionsamongst visceral leishmaniasis patients from Amudat hospitalUgandardquo PLoS Neglected Tropical Diseases vol 6 no 4 ArticleID e1617 2012

[26] S Bashaye N Nombela and D Argaw ldquoRisk factors forvisceral leishmaniasis in a new epidemic site in Amhara regionEthiopiardquo The American Journal of Tropical Medicine andHygiene vol 81 pp 34ndash39 2009

[27] B Bucheton M M Kheir S H El-Safi et al ldquoThe interplaybetween environmental and host factors during an outbreak ofvisceral leishmaniasis in eastern SudanrdquoMicrobes and Infectionvol 4 no 14 pp 1449ndash1457 2002

[28] A Hailu and D Frommel ldquoLeishmaniasis in Ethiopiardquo in TheEcology of Health and Disease in Ethiopia H Kloos and Z AZein Eds pp 375ndash388 Westview Press Boulder Colo USA1993

[29] YWondimeneh Y Takele A Atnafu G Ferede andDMuluyeldquoTrend analysis of visceral leishmaniasis at Addis Zemen healthcenter northwest Ethiopiardquo BioMed Research International vol2014 Article ID 545393 2014

[30] D Abyot K Solomon and AndargachewModule on Leishma-niasis for the Ethiopian Health Center Team Debub UniversitEthiopia 2005

[31] FMoH National Five Year Strategic Plan for Malaria Preventionand Control in Ethiopia 2006-2010 Ministry of Health AddisAbaba Ethiopia 2006

[32] Federal Republic of Ethiopia Ministry of HealthNational GuideLines Federal Republic of Ethiopia Ministry of Health AddisAbeba Ethiopia 3rd edition 2012

[33] K Karunamoorthi and M Bekele ldquoPrevalence of malaria fromperipheral blood smears examination a 1-year retrospectivestudy from the Serbo Health Center Kersa Woreda EthiopiardquoJournal of Infection and Public Health vol 2 no 4 pp 171ndash1762009

Submit your manuscripts athttpswwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 4: Visceral Leishmaniasis-Malaria Coinfection and Their ...downloads.hindawi.com/archive/2017/6816913.pdf · malaria.Individualswholiveintheurban8(5.3%)andrural 8(3.4%)werecoinfectedwithVL-malaria.5dailylaborers

4 Malaria Research and Treatment

P falciparum40 (89)

P vivax5 (11)

Figure 1 Frequency of Plasmodium species at Metema hospitalNorthwest Ethiopia 2014

Table 3 Prevalence of VLmalaria and their coinfection amongVLsuspected patients at Metema hospital Northwest Ethiopia 2014

Variables and result VL () Malaria () VL-malariacoinfection ()

Negative 301 (784) 339 (883) 368 (958)Positive 83 (216) 45 (117) 16 (42)

hundred eighty (469) study participants have history oftravel fromMetema to any region of Ethiopia and vice versaOf these 10 (56) of them have VL-malaria coinfection Allstudy variables did not show statistical significance (Table 4)

4 Discussion

Visceral leishmaniasis and malaria coinfection may exist inendemic areas due to similarity in clinical manifestationsof the two diseases but their coinfection has been poorlyinvestigated In the present study the overall prevalenceof VL-malaria coinfection was 42 This is in agreementwith the study which is conducted in India 59 amongIndian patients with fever and splenomegaly [16] Howeverthis prevalence was lower as compared to study reported inUganda 19 [25]This variationmight be due to difference inthe VL and malaria prevalence which is 216 and 117 inthis study and 57 and 31 in Uganda respectively [25]

In this study prevalence of VL-malaria coinfection wasnonsignificantly higher in males than females A similarfinding was also reported in other studies [25ndash27]The higherprevalence rate might be due to the fact that males engage inactivities whichmake themmore prone to infectivemosquitoand sand fly bites as compared to females who are mostly athome and protected from such infective bites

Visceral leishmaniasis has been amajor health problem inNorthGondar especially in lowlands ofMetema andHumeraplains which are important endemic foci in Northwest ofEthiopia [28] In the present study its prevalence was 216which was consistent with the other study done in the same

study area 226 [21] however lower than the study inother areas of Ethiopia which was reported as 391 [29]The variation might be due to heterogeneity of the vectorsFollowing agricultural development in the region a largenumber of labor migrants from the different areas weremoved to the endemic areas for crop harvesting This led tooutbreaks of VL in many areas in the country which resultedin high morbidity and mortality [30]

Malaria is also one of the most public health problems inEthiopia The total land mass of the country is regarded asmalarious and about 68 of the total population is at risk ofmalaria infection [31] In this study the prevalence of malariawas 117 which is relatively lower than previous study donein the same study area (17) [22] The variation might bedue to difference in study participants The predominantPlasmodium species detected was P falciparum This was inagreement with other previous studies [22 32 33]

Visceral leishmaniasis-malaria coinfection was signifi-cantly higher in patients with the age groups of less thanfive years (119875 = 0004) followed by patients in the agegroups of fifteen to twenty-nine years This indicates thatchildren less than five years old are prone to acquire VL-malaria coinfections which might be associated with theirlow immune system On the other hand high prevalence ofVL-malaria coinfection within fifteen to twenty-nine yearsold might be associated with their daily activities Farmingis extensive in Metema due to the fact that young dailylaborers move to Metema from different areas for applicationof herbicide and for gathering of crops Because of hightemperature in this area daily activities are accomplishedespecially during night This may expose them to the bite ofmosquitoes and sand fly which means a more concentratedeffort should be given to educate these age groups about thisdisease and its vector

In this study majority of study subjects use their bednets However the prevalence of VL-malaria coinfection washigh in these subjects This might be due to improper andinfrequent use of their bed net or it might be due to lack ofimpregnating their bed nets regularly In the study area mostof study participants who were coinfected with VL-malariawere daily laborers followed by merchants This might beassociated with their daily activities which may expose themfor vector bite

This study is limited to the data obtained from the VLsuspected patients which may reduce the prevalence ofmalaria Moreover this study for VL diagnosis depends onlyon serological tests There is no microscopically confirmedparasitological data for VL To fill all these gaps there isa need for further study including all febrile patients withdifferent study design

In conclusion this study tries to see VL-malaria coin-fection for the first time and found 42 coinfection rateA significantly higher number of VL-malaria coinfectionswere showed in study subjects whose age was less thanfive years old Based on these findings we recommend thatmalaria screening be implemented for all VL patients wholive in malaria-endemic areas in order to promptly initiateantimalarial drug treatment Moreover to minimize thedisease burden health planners and administrators need to

Malaria Research and Treatment 5

Table 4 Associated factors of VL-malaria coinfection at Metema hospital Northwest Ethiopia 2014

Variables VL suspected cases119875 value

Not VL-malaria coinfected () VL-malaria coinfected ()Bed net useYes 279 (955) 13 (45) 0618No 89 (967) 3 (33)Sleep usuallyInside home 209 (963) 8 (37) 0592Outside home 158 (952) 8 (48)Lived in MetemaLess than 6 months 23 (958) 1 (42) 0999More than 6 months 345 (958) 15 (42)History of travelYes 170 (944) 10 (56) 0201No 198 (970) 6 (30)Seasonal migrant laborersYes 152 (962) 6 (38) 0762No 216 (956) 10 (44)

give intensive health education to increase the communityawareness about the two diseasesrsquo prevention and controlstrategies

Conflicts of Interest

The authors declared that they have no conflicts of interest

Authorsrsquo Contributions

GetachewFerede participated in conception anddesign of thestudy data collection and analysis interpretation of the find-ings drafting the paper and the write-up Ermias Diro SisayGetie Gebeyaw Getnet and Yegnasew Takele participated inconception and design of the study and interpretations of thefindings and reviewed the manuscript Yitayih Wondimenehand Anteneh Amsalu participated in conception and designof the study data analysis and interpretations of the findingsand reviewedmanuscript All authors reviewed and approvedthe final paper

Acknowledgments

The authors would like to acknowledge University of Gondarfor financial support and they also thank all the studyparticipants and all Metema hospital laboratory staffs fortheir cooperation during data collection

References

[1] RW Ashford P Desjeux and P deRaadt ldquoEstimation of popu-lation at risk of infection and number of cases of LeishmaniasisrdquoParasitology Today vol 8 no 3 pp 104-105 1992

[2] R SnowM Craig C Newton and R SteketeThePublic HealthBurden of Plasmodium Falciparum Malaria in Africa Derivingthe Numbers Forgarty International Center National Instituteof Health Bethesda MD USA 2003

[3] RW Snow C A Guerra AMNoor H YMyint and S I HayldquoThe global distribution of clinical episodes of Plasmodiumfalciparum malariardquo Nature vol 434 no 7030 pp 214ndash2172005

[4] World Health Organization World Malaria Report 2016httpappswhointirisbitstream1066525203819789241511711-engpdf

[5] J Lukes I L Mauricio G Schonian et al ldquoEvolutionary andgeographical history of the Leishmania donovani complex witha revision of current taxonomyrdquo Proceedings of the NationalAcademy of Sciences of the United States of America vol 104 no22 pp 9375ndash9380 2007

[6] H Gilles The Malaria Parasites Edward Arnold Bruce-Chwattrsquos Essential Malariology London UK 3rd edition 1993

[7] Tech Rep World Health Organization Vector Control forMalaria and Other Mosquito Born Diseases Technical ReportSeries Geneva 1995

[8] P Desjeux ldquoLeishmaniasis current situation and new perspec-tivesrdquo Comparative Immunology Microbiology and InfectiousDiseases vol 27 no 5 pp 305ndash318 2004

[9] World health Organization Malaria fact sheet [cited 2016]Available from httpwwwwhointithdiseasesmalariaen

[10] WHO World Malaria Report World Health organizationGeneva Switzerland 2010

[11] R E L Paul M Diallo and P T Brey ldquoMosquitoes and trans-mission ofmalaria parasites - Not just vectorsrdquoMalaria Journalvol 3 article no 39 2004

[12] Y Mueller D B Mbulamberi P Odermatt A Hoffmann LLoutan and F Chappuis ldquoRisk factors for in-hospital mortalityof visceral leishmaniasis patients in eastern Ugandardquo TropicalMedicine and International Health vol 14 no 8 pp 910ndash9172009

[13] J H Kolaczinski R Reithinger D T Worku et al ldquoRisk factorsof visceral leishmaniasis in East Africa A case-control study inPokot territory of Kenya and Ugandardquo International Journal ofEpidemiology vol 37 no 2 pp 344ndash352 2008

[14] P Beer A Harith L Deng S Semiao-Santos and B Chantal ldquoAkilling disease epidemic among displaced sudanese population

6 Malaria Research and Treatment

identified as visceral leishmaniasisrdquo The American Journal ofTropical Medicine and Hygiene vol 44 pp 283ndash289 1991

[15] C Sarker K ChowdhuryN SiddiquiM Jamal and S RahmanldquoClinical profile of kala-azar in adults as seen in Mymen-singh medical college hospital Mymensingh BangladeshrdquoMy-mensingh Medical Journal vol 12 pp 41ndash44 2003

[16] A Nandy M Addy S K Guha A K Maji H M Chauahuriand P Chatterjee ldquoCo-existent kala-azar and malaria in IndiardquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 89 no 5 p 516 1995

[17] K Saha D Chattopadhya and D Kulpati ldquoConcomitant kala-azar malaria and progressive unstable indeterminate leprosy inan 8-year-old childrdquo Journal of Tropical Pediatrics vol 44 pp247-248 1998

[18] S Sah S Sharma and S Rani ldquoKala azar associated withmalariardquo Archives of Pathology amp Laboratory Medicine vol 126p 383 2002

[19] J Woodrow J Hartzell J Czarnik D Brett-Major and GWortmann ldquoCutaneous and presumed visceral leishmaniasisin a soldier deployed to Afghanistanrdquo International Journal ofGeneral Medicine vol 8 article 43 2006

[20] A K Ab Rahman and F H Abdullah ldquoVisceral leishmaniasis(kala-azar) andmalaria coinfection in an immigrant in the stateof TerengganuMalaysia A case reportrdquo Journal ofMicrobiologyImmunology and Infection vol 44 no 1 pp 72ndash76 2011

[21] S Yeromenesh W Yitayih W Habtamu and F GetachewldquoTrend analysis of visceral leishmaniasis in Metema HospitalNorthwest Ethiopiardquo Journal of Epidemiology and Public HealthReviews vol 1 pp 2471ndash8211 2016

[22] F Getachew W Abiyu G Alemtegna A Ali H Tarekegn AYenus et al ldquoPrevalence ofmalaria fromblood smears examina-tion a seven-year retrospective study from Metema HospitalNorthwest EthiopiardquoMalaria Research and Treatment vol 2013Article ID 704730 5 pages 2013

[23] M Siddig H Ghalib D Shillington E Petersen and S KhidirldquoVisceral leishmaniasis in Sudan Clinical featuresrdquoTropical andGeographical Medicine vol 42 pp 107ndash112 1990

[24] S Sundar S G Reed V P Singh P C K Kumar and H WMurray ldquoRapid accurate field diagnosis of Indian visceral leish-maniasisrdquo Lancet vol 351 no 9102 pp 563ndash565 1998

[25] E van den Bogaart M M Z Berkhout E R Adams et alldquoPrevalence features and risk factors for malaria co-infectionsamongst visceral leishmaniasis patients from Amudat hospitalUgandardquo PLoS Neglected Tropical Diseases vol 6 no 4 ArticleID e1617 2012

[26] S Bashaye N Nombela and D Argaw ldquoRisk factors forvisceral leishmaniasis in a new epidemic site in Amhara regionEthiopiardquo The American Journal of Tropical Medicine andHygiene vol 81 pp 34ndash39 2009

[27] B Bucheton M M Kheir S H El-Safi et al ldquoThe interplaybetween environmental and host factors during an outbreak ofvisceral leishmaniasis in eastern SudanrdquoMicrobes and Infectionvol 4 no 14 pp 1449ndash1457 2002

[28] A Hailu and D Frommel ldquoLeishmaniasis in Ethiopiardquo in TheEcology of Health and Disease in Ethiopia H Kloos and Z AZein Eds pp 375ndash388 Westview Press Boulder Colo USA1993

[29] YWondimeneh Y Takele A Atnafu G Ferede andDMuluyeldquoTrend analysis of visceral leishmaniasis at Addis Zemen healthcenter northwest Ethiopiardquo BioMed Research International vol2014 Article ID 545393 2014

[30] D Abyot K Solomon and AndargachewModule on Leishma-niasis for the Ethiopian Health Center Team Debub UniversitEthiopia 2005

[31] FMoH National Five Year Strategic Plan for Malaria Preventionand Control in Ethiopia 2006-2010 Ministry of Health AddisAbaba Ethiopia 2006

[32] Federal Republic of Ethiopia Ministry of HealthNational GuideLines Federal Republic of Ethiopia Ministry of Health AddisAbeba Ethiopia 3rd edition 2012

[33] K Karunamoorthi and M Bekele ldquoPrevalence of malaria fromperipheral blood smears examination a 1-year retrospectivestudy from the Serbo Health Center Kersa Woreda EthiopiardquoJournal of Infection and Public Health vol 2 no 4 pp 171ndash1762009

Submit your manuscripts athttpswwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 5: Visceral Leishmaniasis-Malaria Coinfection and Their ...downloads.hindawi.com/archive/2017/6816913.pdf · malaria.Individualswholiveintheurban8(5.3%)andrural 8(3.4%)werecoinfectedwithVL-malaria.5dailylaborers

Malaria Research and Treatment 5

Table 4 Associated factors of VL-malaria coinfection at Metema hospital Northwest Ethiopia 2014

Variables VL suspected cases119875 value

Not VL-malaria coinfected () VL-malaria coinfected ()Bed net useYes 279 (955) 13 (45) 0618No 89 (967) 3 (33)Sleep usuallyInside home 209 (963) 8 (37) 0592Outside home 158 (952) 8 (48)Lived in MetemaLess than 6 months 23 (958) 1 (42) 0999More than 6 months 345 (958) 15 (42)History of travelYes 170 (944) 10 (56) 0201No 198 (970) 6 (30)Seasonal migrant laborersYes 152 (962) 6 (38) 0762No 216 (956) 10 (44)

give intensive health education to increase the communityawareness about the two diseasesrsquo prevention and controlstrategies

Conflicts of Interest

The authors declared that they have no conflicts of interest

Authorsrsquo Contributions

GetachewFerede participated in conception anddesign of thestudy data collection and analysis interpretation of the find-ings drafting the paper and the write-up Ermias Diro SisayGetie Gebeyaw Getnet and Yegnasew Takele participated inconception and design of the study and interpretations of thefindings and reviewed the manuscript Yitayih Wondimenehand Anteneh Amsalu participated in conception and designof the study data analysis and interpretations of the findingsand reviewedmanuscript All authors reviewed and approvedthe final paper

Acknowledgments

The authors would like to acknowledge University of Gondarfor financial support and they also thank all the studyparticipants and all Metema hospital laboratory staffs fortheir cooperation during data collection

References

[1] RW Ashford P Desjeux and P deRaadt ldquoEstimation of popu-lation at risk of infection and number of cases of LeishmaniasisrdquoParasitology Today vol 8 no 3 pp 104-105 1992

[2] R SnowM Craig C Newton and R SteketeThePublic HealthBurden of Plasmodium Falciparum Malaria in Africa Derivingthe Numbers Forgarty International Center National Instituteof Health Bethesda MD USA 2003

[3] RW Snow C A Guerra AMNoor H YMyint and S I HayldquoThe global distribution of clinical episodes of Plasmodiumfalciparum malariardquo Nature vol 434 no 7030 pp 214ndash2172005

[4] World Health Organization World Malaria Report 2016httpappswhointirisbitstream1066525203819789241511711-engpdf

[5] J Lukes I L Mauricio G Schonian et al ldquoEvolutionary andgeographical history of the Leishmania donovani complex witha revision of current taxonomyrdquo Proceedings of the NationalAcademy of Sciences of the United States of America vol 104 no22 pp 9375ndash9380 2007

[6] H Gilles The Malaria Parasites Edward Arnold Bruce-Chwattrsquos Essential Malariology London UK 3rd edition 1993

[7] Tech Rep World Health Organization Vector Control forMalaria and Other Mosquito Born Diseases Technical ReportSeries Geneva 1995

[8] P Desjeux ldquoLeishmaniasis current situation and new perspec-tivesrdquo Comparative Immunology Microbiology and InfectiousDiseases vol 27 no 5 pp 305ndash318 2004

[9] World health Organization Malaria fact sheet [cited 2016]Available from httpwwwwhointithdiseasesmalariaen

[10] WHO World Malaria Report World Health organizationGeneva Switzerland 2010

[11] R E L Paul M Diallo and P T Brey ldquoMosquitoes and trans-mission ofmalaria parasites - Not just vectorsrdquoMalaria Journalvol 3 article no 39 2004

[12] Y Mueller D B Mbulamberi P Odermatt A Hoffmann LLoutan and F Chappuis ldquoRisk factors for in-hospital mortalityof visceral leishmaniasis patients in eastern Ugandardquo TropicalMedicine and International Health vol 14 no 8 pp 910ndash9172009

[13] J H Kolaczinski R Reithinger D T Worku et al ldquoRisk factorsof visceral leishmaniasis in East Africa A case-control study inPokot territory of Kenya and Ugandardquo International Journal ofEpidemiology vol 37 no 2 pp 344ndash352 2008

[14] P Beer A Harith L Deng S Semiao-Santos and B Chantal ldquoAkilling disease epidemic among displaced sudanese population

6 Malaria Research and Treatment

identified as visceral leishmaniasisrdquo The American Journal ofTropical Medicine and Hygiene vol 44 pp 283ndash289 1991

[15] C Sarker K ChowdhuryN SiddiquiM Jamal and S RahmanldquoClinical profile of kala-azar in adults as seen in Mymen-singh medical college hospital Mymensingh BangladeshrdquoMy-mensingh Medical Journal vol 12 pp 41ndash44 2003

[16] A Nandy M Addy S K Guha A K Maji H M Chauahuriand P Chatterjee ldquoCo-existent kala-azar and malaria in IndiardquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 89 no 5 p 516 1995

[17] K Saha D Chattopadhya and D Kulpati ldquoConcomitant kala-azar malaria and progressive unstable indeterminate leprosy inan 8-year-old childrdquo Journal of Tropical Pediatrics vol 44 pp247-248 1998

[18] S Sah S Sharma and S Rani ldquoKala azar associated withmalariardquo Archives of Pathology amp Laboratory Medicine vol 126p 383 2002

[19] J Woodrow J Hartzell J Czarnik D Brett-Major and GWortmann ldquoCutaneous and presumed visceral leishmaniasisin a soldier deployed to Afghanistanrdquo International Journal ofGeneral Medicine vol 8 article 43 2006

[20] A K Ab Rahman and F H Abdullah ldquoVisceral leishmaniasis(kala-azar) andmalaria coinfection in an immigrant in the stateof TerengganuMalaysia A case reportrdquo Journal ofMicrobiologyImmunology and Infection vol 44 no 1 pp 72ndash76 2011

[21] S Yeromenesh W Yitayih W Habtamu and F GetachewldquoTrend analysis of visceral leishmaniasis in Metema HospitalNorthwest Ethiopiardquo Journal of Epidemiology and Public HealthReviews vol 1 pp 2471ndash8211 2016

[22] F Getachew W Abiyu G Alemtegna A Ali H Tarekegn AYenus et al ldquoPrevalence ofmalaria fromblood smears examina-tion a seven-year retrospective study from Metema HospitalNorthwest EthiopiardquoMalaria Research and Treatment vol 2013Article ID 704730 5 pages 2013

[23] M Siddig H Ghalib D Shillington E Petersen and S KhidirldquoVisceral leishmaniasis in Sudan Clinical featuresrdquoTropical andGeographical Medicine vol 42 pp 107ndash112 1990

[24] S Sundar S G Reed V P Singh P C K Kumar and H WMurray ldquoRapid accurate field diagnosis of Indian visceral leish-maniasisrdquo Lancet vol 351 no 9102 pp 563ndash565 1998

[25] E van den Bogaart M M Z Berkhout E R Adams et alldquoPrevalence features and risk factors for malaria co-infectionsamongst visceral leishmaniasis patients from Amudat hospitalUgandardquo PLoS Neglected Tropical Diseases vol 6 no 4 ArticleID e1617 2012

[26] S Bashaye N Nombela and D Argaw ldquoRisk factors forvisceral leishmaniasis in a new epidemic site in Amhara regionEthiopiardquo The American Journal of Tropical Medicine andHygiene vol 81 pp 34ndash39 2009

[27] B Bucheton M M Kheir S H El-Safi et al ldquoThe interplaybetween environmental and host factors during an outbreak ofvisceral leishmaniasis in eastern SudanrdquoMicrobes and Infectionvol 4 no 14 pp 1449ndash1457 2002

[28] A Hailu and D Frommel ldquoLeishmaniasis in Ethiopiardquo in TheEcology of Health and Disease in Ethiopia H Kloos and Z AZein Eds pp 375ndash388 Westview Press Boulder Colo USA1993

[29] YWondimeneh Y Takele A Atnafu G Ferede andDMuluyeldquoTrend analysis of visceral leishmaniasis at Addis Zemen healthcenter northwest Ethiopiardquo BioMed Research International vol2014 Article ID 545393 2014

[30] D Abyot K Solomon and AndargachewModule on Leishma-niasis for the Ethiopian Health Center Team Debub UniversitEthiopia 2005

[31] FMoH National Five Year Strategic Plan for Malaria Preventionand Control in Ethiopia 2006-2010 Ministry of Health AddisAbaba Ethiopia 2006

[32] Federal Republic of Ethiopia Ministry of HealthNational GuideLines Federal Republic of Ethiopia Ministry of Health AddisAbeba Ethiopia 3rd edition 2012

[33] K Karunamoorthi and M Bekele ldquoPrevalence of malaria fromperipheral blood smears examination a 1-year retrospectivestudy from the Serbo Health Center Kersa Woreda EthiopiardquoJournal of Infection and Public Health vol 2 no 4 pp 171ndash1762009

Submit your manuscripts athttpswwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 6: Visceral Leishmaniasis-Malaria Coinfection and Their ...downloads.hindawi.com/archive/2017/6816913.pdf · malaria.Individualswholiveintheurban8(5.3%)andrural 8(3.4%)werecoinfectedwithVL-malaria.5dailylaborers

6 Malaria Research and Treatment

identified as visceral leishmaniasisrdquo The American Journal ofTropical Medicine and Hygiene vol 44 pp 283ndash289 1991

[15] C Sarker K ChowdhuryN SiddiquiM Jamal and S RahmanldquoClinical profile of kala-azar in adults as seen in Mymen-singh medical college hospital Mymensingh BangladeshrdquoMy-mensingh Medical Journal vol 12 pp 41ndash44 2003

[16] A Nandy M Addy S K Guha A K Maji H M Chauahuriand P Chatterjee ldquoCo-existent kala-azar and malaria in IndiardquoTransactions of the Royal Society of Tropical Medicine andHygiene vol 89 no 5 p 516 1995

[17] K Saha D Chattopadhya and D Kulpati ldquoConcomitant kala-azar malaria and progressive unstable indeterminate leprosy inan 8-year-old childrdquo Journal of Tropical Pediatrics vol 44 pp247-248 1998

[18] S Sah S Sharma and S Rani ldquoKala azar associated withmalariardquo Archives of Pathology amp Laboratory Medicine vol 126p 383 2002

[19] J Woodrow J Hartzell J Czarnik D Brett-Major and GWortmann ldquoCutaneous and presumed visceral leishmaniasisin a soldier deployed to Afghanistanrdquo International Journal ofGeneral Medicine vol 8 article 43 2006

[20] A K Ab Rahman and F H Abdullah ldquoVisceral leishmaniasis(kala-azar) andmalaria coinfection in an immigrant in the stateof TerengganuMalaysia A case reportrdquo Journal ofMicrobiologyImmunology and Infection vol 44 no 1 pp 72ndash76 2011

[21] S Yeromenesh W Yitayih W Habtamu and F GetachewldquoTrend analysis of visceral leishmaniasis in Metema HospitalNorthwest Ethiopiardquo Journal of Epidemiology and Public HealthReviews vol 1 pp 2471ndash8211 2016

[22] F Getachew W Abiyu G Alemtegna A Ali H Tarekegn AYenus et al ldquoPrevalence ofmalaria fromblood smears examina-tion a seven-year retrospective study from Metema HospitalNorthwest EthiopiardquoMalaria Research and Treatment vol 2013Article ID 704730 5 pages 2013

[23] M Siddig H Ghalib D Shillington E Petersen and S KhidirldquoVisceral leishmaniasis in Sudan Clinical featuresrdquoTropical andGeographical Medicine vol 42 pp 107ndash112 1990

[24] S Sundar S G Reed V P Singh P C K Kumar and H WMurray ldquoRapid accurate field diagnosis of Indian visceral leish-maniasisrdquo Lancet vol 351 no 9102 pp 563ndash565 1998

[25] E van den Bogaart M M Z Berkhout E R Adams et alldquoPrevalence features and risk factors for malaria co-infectionsamongst visceral leishmaniasis patients from Amudat hospitalUgandardquo PLoS Neglected Tropical Diseases vol 6 no 4 ArticleID e1617 2012

[26] S Bashaye N Nombela and D Argaw ldquoRisk factors forvisceral leishmaniasis in a new epidemic site in Amhara regionEthiopiardquo The American Journal of Tropical Medicine andHygiene vol 81 pp 34ndash39 2009

[27] B Bucheton M M Kheir S H El-Safi et al ldquoThe interplaybetween environmental and host factors during an outbreak ofvisceral leishmaniasis in eastern SudanrdquoMicrobes and Infectionvol 4 no 14 pp 1449ndash1457 2002

[28] A Hailu and D Frommel ldquoLeishmaniasis in Ethiopiardquo in TheEcology of Health and Disease in Ethiopia H Kloos and Z AZein Eds pp 375ndash388 Westview Press Boulder Colo USA1993

[29] YWondimeneh Y Takele A Atnafu G Ferede andDMuluyeldquoTrend analysis of visceral leishmaniasis at Addis Zemen healthcenter northwest Ethiopiardquo BioMed Research International vol2014 Article ID 545393 2014

[30] D Abyot K Solomon and AndargachewModule on Leishma-niasis for the Ethiopian Health Center Team Debub UniversitEthiopia 2005

[31] FMoH National Five Year Strategic Plan for Malaria Preventionand Control in Ethiopia 2006-2010 Ministry of Health AddisAbaba Ethiopia 2006

[32] Federal Republic of Ethiopia Ministry of HealthNational GuideLines Federal Republic of Ethiopia Ministry of Health AddisAbeba Ethiopia 3rd edition 2012

[33] K Karunamoorthi and M Bekele ldquoPrevalence of malaria fromperipheral blood smears examination a 1-year retrospectivestudy from the Serbo Health Center Kersa Woreda EthiopiardquoJournal of Infection and Public Health vol 2 no 4 pp 171ndash1762009

Submit your manuscripts athttpswwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 7: Visceral Leishmaniasis-Malaria Coinfection and Their ...downloads.hindawi.com/archive/2017/6816913.pdf · malaria.Individualswholiveintheurban8(5.3%)andrural 8(3.4%)werecoinfectedwithVL-malaria.5dailylaborers

Submit your manuscripts athttpswwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom