A review of visceral leishmaniasis during the conflict in South Sudan and the consequences for East African countries

Parasites and Vectors

Volumn 9, Issue 1, 2016, Pages

  Al Salem, Waleed ^a   Herricks, Jennifer R ^b,c   Hotez, Peter J ^b,c,d,e  

^a MINISTRY OF HEALTH   (Saudi Arabia)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c RICE UNIVERSITY   (United States)

^d TEXAS CHILDREN S HOSPITAL   (United States)

^e BAYLOR UNIVERSITY   (United States)

Author keywords

Civil war; Conflict zone; East Africa; Leishmania donovani; Phlebotomus orientalis; Refugees; South Sudan; Visceral leishmaniasis

Indexed keywords

AMPHOTERICIN B; AMPHOTERICIN B LIPID COMPLEX; ANTIMONY; ANTIRETROVIRUS AGENT; DEOXYCHOLIC ACID; INSECTICIDE; MILTEFOSINE; PENTAMIDINE; PENTAVALENT ANTIMONIAL; UNCLASSIFIED DRUG;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; AGGLUTINATION TEST; BED NET; CORRELATION ANALYSIS; DRUG EFFICACY; EAST AFRICAN; ENDEMIC DISEASE; EPIDEMIC; HEALTH CARE ACCESS; HEALTH CARE COST; HEALTH CARE POLICY; HEALTH CARE SYSTEM; HEALTH SERVICE; HEALTH SURVEY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOAFFINITY CHROMATOGRAPHY; INFECTION PREVENTION; KENYA; LETHALITY; MALNUTRITION; MIGRATION; MIXED INFECTION; POST KALA AZAR DERMAL LEISHMANIASIS; PRACTICE GUIDELINE; PUBLIC HEALTH; REFUGEE; RESOURCE ALLOCATION; REVIEW; SEROLOGY; SOMALIA; SOUTH SUDAN; SYSTEMATIC REVIEW; TREATMENT RESPONSE; UGANDA; VISCERAL LEISHMANIASIS; WAR; REFUGEE CAMP; WARFARE;

HUMANS; LEISHMANIASIS, VISCERAL; REFUGEE CAMPS; SOUTH SUDAN; WARFARE;

EID: 84983356566     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/s13071-016-1743-7     Document Type: Review

References (93)

1. Hotez PJ. Combating the next lethal epidemic. Science. 2015;348(6232):296-7.
2. Jacobson RL. Leishmaniasis in an era of conflict in the Middle East. Vector Borne Zoonotic Dis. 2011;11(3):247-58.
3. Naghavi M, Wang H, Lozano R, Davis A, Liang X, Zhou M, et al. Global, regional, and national age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2015;385(9963):117-71.
4. Murray CJ, Barber RM, Foreman KJ, Ozgoren AA, Abd-Allah F, Abera SF, et al. Global, regional, and national disability-adjusted life years (DALYs) for 306 diseases and injuries and healthy life expectancy (HALE) for 188 countries, 1990-2013: quantifying the epidemiological transition. Lancet. 2015;386(10009):2145-91.
5. Alvar J, Velez ID, Bern C, Herrero M, Desjeux P, Cano J, et al. Leishmaniasis worldwide and global estimates of its incidence. PLoS One. 2012;7(5):e35671.
6. Litt E, Baker MC, Molyneux D. Neglected tropical diseases and mental health: a perspective on comorbidity. Trends Parasitol. 2012;28(5):195-201.
7. Hotez PJ. Stigma: the stealth weapon of the NTD. PLoS Negl Trop Dis. 2008;2(4):e230.
8. Gorski S, Wiercinska-Drapalo A. Visceral leishmaniasis as a threat for non-endemic countries. Wiad Parazytol. 2009;55(3):195-200. In Polish.
9. World Health Organization. Control of the leishmaniasis. In: WHO Technical Report Series, Vol. 9492010. Geneva: Report of the meeting of the WHO Expert Committee on the Control of Leishmaniases; 2010. 22-26.
10. Anjili CO, Ngumbi PM, Kaburi JC, Irungu LW. The phlebotomine sandfly fauna (Diptera: Psychodidae) of Kenya. J Vector Borne Dis. 2011;48(4):183-9.
11. Elnaiem DE. Ecology and control of the sand fly vectors of Leishmania donovani in East Africa, with special emphasis on Phlebotomus orientalis. J Vector Ecol. 2011;36 Suppl 1:S23-31.
12. Gebre-Michael T, Malone JB, Balkew M, Ali A, Berhe N, Hailu A, Herzi AA. Mapping the potential distribution of Phlebotomus martini and P. orientalis (Diptera: Psychodidae), vectors of kala-azar in East Africa by use of geographic information systems. Acta Trop. 2004;90(1):73-86.
13. Mahdi M, Elamin EM, Melville SE, Musa AM, Blackwell JM, Mukhtar MM, et al. Sudanese mucosal leishmaniasis: isolation of a parasite within the Leishmania donovani complex that differs genotypically from L. donovani causing classical visceral leishmaniasis. Infect Genet Evol. 2005;5(1):29-33.
14. Zijlstra EE, Khalil EA, Kager PA, El-Hassan AM. Post-kala-azar dermal leishmaniasis in the Sudan: clinical presentation and differential diagnosis. Br J Dermatol. 2000;143(1):136-43.
15. Dereure J, El-Safi SH, Bucheton B, Boni M, Kheir MM, Davoust B, et al. Visceral leishmaniasis in eastern Sudan: parasite identification in humans and dogs; host-parasite relationships. Microbes Infect. 2003;5(12):1103-8.
16. Reithinger R, Brooker S, Kolaczinski JH. Visceral leishmaniasis in eastern Africa-current status. Trans R Soc Trop Med Hyg. 2007;101(12):1169-70.
17. Marlet MV, Sang DK, Ritmeijer K, Muga RO, Onsongo J, Davidson RN. Emergence or re-emergence of visceral leishmaniasis in areas of Somalia, north-eastern Kenya, and south-eastern Ethiopia in 2000-01. Trans R Soc Trop Med Hyg. 2003;97(5):515-18.
18. Zijlstra EE, el-Hassan AM. Leishmaniasis in Sudan. Visceral leishmaniasis. Trans R Soc Trop Med Hyg. 2001;95 Suppl 1:S27-58.
19. Kassahun A, Sadlova J, Dvorak V, Kostalova T, Rohousova I, Frynta D, et al. Detection of Leishmania donovani and L. tropica in Ethiopian wild rodents. Acta Trop. 2015;145:39-44.
20. Seblova V, Volfova V, Dvorak V, Pruzinova K, Votypka J, Kassahun A, et al. Phlebotomus orientalis sand flies from two geographically distant Ethiopian localities: biology, genetic analyses and susceptibility to Leishmania donovani. PLoS Negl Trop Dis. 2013;7(4):e2187.
21. Elnaiem DA, Hassan HK, Ward RD. Associations of Phlebotomus orientalis and other sandflies with vegetation types in the eastern Sudan focus of kala-azar. Med Vet Entomol. 1999;13(2):198-203.
22. Elnaiem DE, Hassan HK, Osman OF, Maingon RD, Killick-Kendrick R, Ward RD. A possible role for Phlebotomus (Anaphlebotomus) rodhaini (Parrot, 1930) in transmission of Leishmania donovani. Parasit Vectors. 2011;4:238.
23. Elnaiem DA, Hassan HK, Ward RD. Phlebotomine sandflies in a focus of visceral leishmaniasis in a border area of eastern Sudan. Ann Trop Med Parasitol. 1997;91(3):307-18.
24. Burki T. East African countries struggle with visceral leishmaniasis. Lancet. 2009;374(9687):371-2.
25. Abbasi I, Aramin S, Hailu A, Shiferaw W, Kassahun A, Belay S, et al. Evaluation of PCR procedures for detecting and quantifying Leishmania donovani DNA in large numbers of dried human blood samples from a visceral leishmaniasis focus in Northern Ethiopia. BMC Infect Dis. 2013;13:153.
26. Gelanew T, Kuhls K, Hurissa Z, Weldegebreal T, Hailu W, Kassahun A, et al. Inference of population structure of Leishmania donovani strains isolated from different Ethiopian visceral leishmaniasis endemic areas. PLoS Negl Trop Dis. 2010;4(11):e889.
27. Nackers F, Mueller YK, Salih N, Elhag MS, Elbadawi ME, Hammam O, et al. Determinants of visceral leishmaniasis: A case-control study in Gedaref State, Sudan. PLoS Negl Trop Dis. 2015;9(11):e0004187.
28. Yared S, Deribe K, Gebreselassie A, Lemma W, Akililu E, Kirstein OD, et al. Risk factors of visceral leishmaniasis: a case control study in north-western Ethiopia. Parasit Vectors. 2014;7:470.
29. Argaw D, Mulugeta A, Herrero M, Nombela N, Teklu T, Tefera T, et al. Risk factors for visceral leishmaniasis among residents and migrants in Kafta-Humera, Ethiopia. PLoS Negl Trop Dis. 2013;7(11):e2543.
30. Gadisa E, Tsegaw T, Abera A, Elnaiem DE, den Boer M, Aseffa A, Jorge A. Eco-epidemiology of visceral leishmaniasis in Ethiopia. Parasit Vectors. 2015;8:381.
31. Wasunna M, Musa A, Hailu A, Khalil EA, Olobo J, Juma R, et al. The Leishmaniasis East Africa Platform (LEAP): strengthening clinical trial capacity in resource-limited countries to deliver new treatments for visceral leishmaniasis. Trans R Soc Trop Med Hyg. 2016;110(6):321-3.
32. Leta S, Dao TH, Mesele F, Alemayehu G. Visceral leishmaniasis in Ethiopia: an evolving disease. PLoS Negl Trop Dis. 2014;8(9):e3131.
33. Elnaiem DA, Hassan MM, Maingon R, Nureldin GH, Mekawi AM, Miles M, Ward RD. The Egyptian mongoose, Herpestes ichneumon, is a possible reservoir host of visceral leishmaniasis in eastern Sudan. Parasitology. 2001;122(Pt 5):531-6.
34. Alvar J, Bashaye S, Argaw D, Cruz I, Aparicio P, Kassa A, et al. Kala-azar outbreak in Libo Kemkem, Ethiopia: epidemiologic and parasitologic assessment. Am J Trop Med Hyg. 2007;77(2):275-82.
35. Mueller YK, Kolaczinski JH, Koech T, Lokwang P, Riongoita M, Velilla E, et al. Clinical epidemiology, diagnosis and treatment of visceral leishmaniasis in the Pokot endemic area of Uganda and Kenya. Am Trop Med Hyg. 2014;90(1):33-9.
36. Kolaczinski JH, Reithinger R, Worku DT, Ocheng A, Kasimiro J, Kabatereine N, Brooker S. Risk factors of visceral leishmaniasis in East Africa: a case-control study in Pokot territory of Kenya and Uganda. Int J Epidemiol. 2008;37(2):344-52.
37. Boussery G, Boelaert M, van Peteghem J, Ejikon P, Henckaerts K. Visceral leishmaniasis (kala-azar) outbreak in Somali refugees and Kenyan shepherds, Kenya. Emerg Infect Dis. 2001;7(3 Suppl):603-4.
38. Schaefer KU, Kurtzhals JA, Sherwood JA, Githure JI, Kager PA, Muller AS. Epidemiology and clinical manifestations of visceral and cutaneous leishmaniasis in Baringo District, Rift Valley, Kenya. A literature review. Trop Geogr Med. 1994;46(3):129-33.
39. Marlet MV, Wuillaume F, Jacquet D, Quispe KW, Dujardin JC, Boelaert M. A neglected disease of humans: a new focus of visceral leishmaniasis in Bakool, Somalia. Trans R Soc Trop Med Hyg. 2003;97(6):667-71.
40. Schaefer KU, Schoone GJ, Gachihi GS, Muller AS, Kager PA, Meredith SE. Visceral leishmaniasis: use of the polymerase chain reaction in an epidemiological study in Baringo District, Kenya. Trans R Soc Trop Med Hyg. 1995;89(5):492-5.
41. Mugasa CM, Deborggraeve S, Schoone GJ, Laurent T, Leeflang MM, Ekangu RA, et al. Accordance and concordance of PCR and NASBA followed by oligochromatography for the molecular diagnosis of Trypanosoma brucei and Leishmania. Trop Med Int Health. 2010;15(7):800-5.
42. Raguenaud ME, Jansson A, Vanlerberghe V, Deborggraeve S, Dujardin JC, Orfanos G, et al. Epidemiology and clinical features of patients with visceral leishmaniasis treated by an MSF clinic in Bakool region, Somalia, 2004-2006. PLoS Negl Trop Dis. 2007;1(1):e85.
43. Rumunu J, Brooker S, Hopkins A, Chane F, Emerson P, Kolaczinski J. Southern Sudan: an opportunity for NTD control and elimination? Trends Parasitol. 2009;25(7):301-7.
44. Wakabi W. Peace has come to southern Sudan, but challenges remain. Lancet. 2006;368(9538):829-30.
45. Abubakar A, Ruiz-Postigo JA, Pita J, Lado M, Ben-Ismail R, Argaw D, Alvar J. Visceral leishmaniasis outbreak in South Sudan 2009-2012: epidemiological assessment and impact of a multisectoral response. PLoS Negl Trop Dis. 2014;8(3):e2720.
46. World Health Organization. Summary of visceral leishmaniasis (VL) or kala-azar (KA) Outbreak situation in South Sudan. 2015. http://www.who.int/hac/crises/ssd/sitreps/south-sudan-kala-azar-september2014.pdf. Accessed 15 Jan 2016.
47. United Nations High Commissioner for Refugees (UNHCR). 2015 UNHCR country operations profile-South Sudan. 2015. http://www.unhcr.org/south-sudan.html. Accessed 15 Jan 2016.
48. South Sudan Situation, Regional Overview UNHCR 2015.
49. MSF. South Sudan: Tackling a deadly outbreak of tropical disease. 2015.
50. Ahmad K. War and gerbils compound Afghan leishmaniasis epidemic. Lancet Infect Dis. 2002;2(5):268.
51. Hailu A, Berhe N, Yeneneh H. Visceral leishmaniasis in Gambela, western Ethiopia. Ethiop Med J. 1996;34(1):33-42.
52. Mengesha B, Endris M, Takele Y, Mekonnen K, Tadesse T, Feleke A, Diro E. Prevalence of malnutrition and associated risk factors among adult visceral leishmaniasis patients in Northwest Ethiopia: a cross sectional study. BMC Res Notes. 2014;7:75.
53. Johnson RN, Ngumbi PM, Gachihi GS, Mwanyumba JP, Mbugua J, Mosonik N, et al. A new focus of kala-azar due to Leishmania donovani sensu lato in Kenya. Trans R Soc Trop Med Hyg. 1993;87(2):142-4.
54. Fendall NR, McKinnon JA. Kalaazar in the Baringo District of Kenya; progress report. J Trop Med Hyg. 1956;59(9):208-12.
55. Fendall NR. The spread of kala-azar in Kenya. East Afr Med J. 1961;38:417-19.
56. el-Hassan AM, Hashim FA, Ali MS, Ghalib HW, Zijlstra EE. Kala-azar in western Upper Nile province in the southern Sudan and its spread to a nomadic tribe from the north. Trans R Soc Trop Med Hyg. 1993;87(4):395-8.
57. Musa SA, el Rabaa FM, Abdel-Nour OM. Studies on phlebotomine sandflies in an active focus of leishmaniasis in the Sudan. Parassitologia. 1991;33(Suppl):55-62.
58. Widaa SO, Ahmed KA, Bari AA, Ali MM, Ibrahim MA, Bashir MA, et al. Sandflies (Diptera: Psychodidae) in a focus of visceral leishmaniasis in White Nile, Sudan. Memo Inst Oswaldo Cruz. 2012;107(4):470-5.
59. Ahmed MA, Suleman SM, Kordofani AA, Mustafa MD. Outbreak of visceral leishmaniasis in the western bank of the White Nile-Sudan, report and clinical study. East Afr Med J. 1988;65(12):824-8.
60. Fuller GK, Lemma A, Haile T, Gemeda N. Kala-azar in Ethiopia: survey of south-west Ethiopia. The leishmanin skin test and epidemiological studies. Ann Trop Med Parasitol. 1979;73(5):417-30.
61. Tamazug R. Ethiopia camps nearing capacity as S. Sudan refugee number tops. 2015;133:000.
62. Zijlstra EE, Musa AM, Khalil EA, El-Hassan IM, El-Hassan AM. Post-kala-azar dermal leishmaniasis. Lancet Infect Dis. 2003;3(2):87-98.
63. Desjeux P, Ghosh RS, Dhalaria P, Strub-Wourgaft N, Zijlstra EE. Report of the post kala-azar dermal leishmaniasis (PKDL) consortium meeting, New Delhi, India, 27-29 June 2012. Parasit Vectors. 2013;6:196.
64. Addy M, Nandy A. Ten years of kala-azar in west Bengal, Part I. Did post-kala-azar dermal leishmaniasis initiate the outbreak in 24-Parganas? Bull World Health Organ. 1992;70(3):341-6.
65. Kirk R, Lewis DJ. Studies in leishmaniasis in the Anglo-Egyptian Sudan. XI. Phlebotomus in relation to leishmaniasis in the Sudan. Trans R Soc Trop Med Hyg. 1955;49(3):229-40.
66. Rahman KM, Islam S, Rahman MW, Kenah E, Ghalib CM, Zahid MM, et al. Increasing incidence of post-kala-azar dermal leishmaniasis in a population-based study in Bangladesh. Clin Infect Dis. 2010;50(1):73-6.
67. Inbar E, Lawyer P, Sacks D, Podini D. The potential use of forensic DNA methods applied to sand fly blood meal analysis to identify the infection reservoirs of anthroponotic visceral leishmaniasis. PLoS Negl Trop Dis. 2016;10(5):e0004706.
68. El Hassan AM, Khalil EA. Post-kala-azar dermal leishmaniasis: does it play a role in the transmission of Leishmania donovani in the Sudan? Trop Medi Int Health. 2001;6(9):743-4.
69. Ganguly S, Das NK, Barbhuiya JN, Chatterjee M. Post-kala-azar dermal leishmaniasis - an overview. Int J Dermatol. 2010;49(8):921-31.
70. Mukhopadhyay D, Mukherjee S, Ghosh S, Roy S, Saha B, Das NK, Chatterjee M. A male preponderance in patients with Indian post kala-azar dermal leishmaniasis is associated with increased circulating levels of testosterone. Int J Dermatol. 2016;55(5):e250-5.
71. Mukhopadhyay D, Dalton JE, Kaye PM, Chatterjee M. Post kala-azar dermal leishmaniasis: an unresolved mystery. Trends Parasitol. 2014;30(2):65-74.
72. Ismail A, Khalil EA, Musa AM, El Hassan IM, Ibrahim ME, Theander TG, El Hassan AM. The pathogenesis of post kala-azar dermal leishmaniasis from the field to the molecule: does ultraviolet light (UVB) radiation play a role? Med Hypotheses. 2006;66(5):993-9.
73. Bhattacharyya T, Boelaert M, Miles MA. Comparison of visceral leishmaniasis diagnostic antigens in African and Asian Leishmania donovani reveals extensive diversity and region-specific polymorphisms. PLoS Negl Trop Dis. 2013;7(2):e2057.
74. Bhattacharyya T, Bowes DE, El-Safi S, Sundar S, Falconar AK, Singh OP, et al. Significantly lower anti-Leishmania IgG responses in Sudanese versus Indian visceral leishmaniasis. PLoS Negl Trop Dis. 2014;8(2):e2675.
75. de Ruiter CM, van der Veer C, Leeflang MM, Deborggraeve S, Lucas C, Adams ER. Molecular tools for diagnosis of visceral leishmaniasis: systematic review and meta-analysis of diagnostic test accuracy. J Clin Microbiol. 2014;52(9):3147-55.
76. Adams ER, Gomez MA, Scheske L, Rios R, Marquez R, Cossio A, et al. Sensitive diagnosis of cutaneous leishmaniasis by lesion swab sampling coupled to qPCR. Parasitology. 2014;141(14):1891-7.
77. Adams ER, Versteeg I, Leeflang MM. Systematic review into diagnostics for post-kala-azar dermal leishmaniasis (PKDL). J Trop Med. 2013;2013:150746.
78. Diro E, Lynen L, Ritmeijer K, Boelaert M, Hailu A, van Griensven J. Visceral leishmaniasis and HIV coinfection in East Africa. PLoS Negl Trop Dis. 2014;8(6):e2869.
79. Diro E, van Griensven J, Mohammed R, Colebunders R, Asefa M, Hailu A, Lynen L. Atypical manifestations of visceral leishmaniasis in patients with HIV in north Ethiopia: a gap in guidelines for the management of opportunistic infections in resource poor settings. Lancet Infect Dis. 2015;15(1):122-9.
80. Alvar J, Aparicio P, Aseffa A, Den Boer M, Canavate C, Dedet JP, et al. The relationship between leishmaniasis and AIDS: the second 10 years. Clin Microbiol Rev. 2008;21(2):334-59.
81. Collin S, Davidson R, Ritmeijer K, Keus K, Melaku Y, Kipngetich S, Davies C. Conflict and kala-azar: determinants of adverse outcomes of kala-azar among patients in southern Sudan. Clin Infect Dis. 2004;38(5):612-19.
82. UNICEF. Child malnutrition emergency in South Sudan. 2014.
83. Singh S, Sharma U, Mishra J. Post-kala-azar dermal leishmaniasis: recent developments. Int J Dermatol. 2011;50(9):1099-108.
84. Boelaert M, El-Safi S, Hailu A, Mukhtar M, Rijal S, Sundar S, et al. Diagnostic tests for kala-azar: a multi-centre study of the freeze-dried DAT, rK39 strip test and KAtex in East Africa and the Indian subcontinent. Trans R Soc Trop Med Hyg. 2008;102(1):32-40.
85. Diro E, Techane Y, Tefera T, Assefa Y, Kebede T, Genetu A, et al. Field evaluation of FD-DAT, rK39 dipstick and KATEX (urine latex agglutination) for diagnosis of visceral leishmaniasis in northwest Ethiopia. Trans R Soc Trop Med Hyg. 2007;101(9):908-14.
86. El-Safi SH, Abdel-Haleem A, Hammad A, El-Basha I, Omer A, Kareem HG, et al. Field evaluation of latex agglutination test for detecting urinary antigens in visceral leishmaniasis in Sudan. East Mediterr Health J. 2003;9(4):844-55.
87. Maia Z, Lirio M, Mistro S, Mendes CM, Mehta SR, Badaro R. Comparative study of rK39 Leishmania antigen for serodiagnosis of visceral leishmaniasis: systematic review with meta-analysis. PLoS Negl Trop Dis. 2012;6(1):e1484.
88. Beyrer C, Villar JC, Suwanvanichkij V, Singh S, Baral SD, Mills EJ. Neglected diseases, civil conflicts, and the right to health. Lancet. 2007;370(9587):619-27.
89. Mondal D, Huda MM, Karmoker MK, Ghosh D, Matlashewski G, Nabi SG, Kroeger A. Reducing visceral leishmaniasis by insecticide impregnation of bed-nets, Bangladesh. Emerg Infect Dis. 2013;19(7):1131-4.
90. Chowdhury R, Huda MM, Kumar V, Das P, Joshi AB, Banjara MR, et al. The Indian and Nepalese programmes of indoor residual spraying for the elimination of visceral leishmaniasis: performance and effectiveness. Ann Trop Med Parasitol. 2011;105(1):31-5.
91. Elnaiem DA, Elnahas AM, Aboud MA. Protective efficacy of lambdacyhalothrin-impregnated bednets against Phlebotomus orientalis, the vector of visceral leishmaniasis in Sudan. Med Vet Entomol. 1999;13(3):310-14.
92. Ritmeijer K, Davies C, van Zorge R, Wang SJ, Schorscher J, Dongu'du SI, Davidson RN. Evaluation of a mass distribution programme for fine-mesh impregnated bednets against visceral leishmaniasis in eastern Sudan. Trop Med Intern Health. 2007;12(3):404-14.
93. Meheus F, Abuzaid AA, Baltussen R, Younis BM, Balasegaram M, Khalil EAG, et al. The economic burden of visceral leishmaniasis in Sudan: an assessment of provider and household costs. Am J Trop Med Hyg. 2013;89(6):1146-53.