Volume 84, Issue 6
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



We report paired strains of parasites, one from the viscera and the other from skin lesions that were isolated from three patients with visceral leishmaniasis and disseminated cutaneous leishmaniasis that were co-infected with human immunodeficiency virus. The causative parasites were characterized by polymerase chain reaction–restriction length polymorphism of the ribosomal DNA internal transcribed spacer 1 and by a panel of multilocus microsatellite markers. We demonstrated that the causative agent was in all cases, irrespective of the phenotype of the disease. The paired strains from viscera and skin lesions of the same patients showed genetic identity across the 14 microsatellite markers investigated. These findings demonstrate that the skin lesions in these human immunodeficiency virus–positive patients with visceral leishmaniasis were caused by dissemination of viscerotropic parasites as a consequence of severe immunosuppression. However, in all three patients, rapid clearance of the skin lesions was observed after antimonial therapy.


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  1. Lyons S, Veeken H, Long J, , 2003. Visceral leishmaniasis and HIV in Tigray, Ethiopia. Trop Med Int Health 8: 733739.[Crossref] [Google Scholar]
  2. Haile T, Anderson SD, , 2006. Visceral leishmaniasis in northern Ethiopia. East Afr Med J 83: 389392.[Crossref] [Google Scholar]
  3. Mengistu G, Ayele B, , 2007. Visceral leishmaniasis and HIV co-infection in patients admitted to Gondar university hospital, northwest Ethiopia. Ethiopian J Health Develop 21: 5360. [Google Scholar]
  4. Alvar J, Aparicio P, Aseffa A, Den Boer M, Canavate C, Dedet JP, Gradoni L, Ter Horst R, Lopez-Velez R, Moreno J, , 2008. The relationship between leishmaniasis and AIDS: the second 10 years. Clin Microbiol Rev 21: 334359.[Crossref] [Google Scholar]
  5. Gonzalez-Beato MJ, Moyano B, Sanchez C, Gonzalez-Beato MT, Perez-Molina JA, Miralles P, Lazaro P, , 2000. Kaposi's sarcoma-like lesions and other nodules as cutaneous involvement in AIDS-related visceral leishmaniasis. Br J Dermatol 143: 13161318.[Crossref] [Google Scholar]
  6. Bosch RJ, Rodrigo AB, Sanchez P, de Galvez MV, Herrera E, , 2002. Presence of Leishmania organisms in specific and non-specific skin lesions in HIV-infected individuals with visceral leishmaniasis. Int J Dermatol 41: 670675.[Crossref] [Google Scholar]
  7. Ara M, Maillo C, Peon G, Clavel A, Cuesta J, Grasa MP, Carapeto FJ, , 1998. Visceral leishmaniasis with cutaneous lesions in a patient infected with human immunodeficiency virus. Br J Dermatol 139: 114117.[Crossref] [Google Scholar]
  8. Postigo C, Llamas R, Zarco C, Rubio R, Pulido F, Costa JR, Iglesias L, , 1997. Cutaneous lesions in patients with visceral leishmaniasis and HIV infection. J Infect 35: 265268.[Crossref] [Google Scholar]
  9. Hurissa Z, Gebre-Silassie S, Hailu W, Tefera T, Lalloo DG, Cuevas LE, Hailu A, , 2010. Clinical characteristics and treatment outcome of patients with visceral leishmaniasis and HIV co-infection in northwest Ethiopia. Trop Med Int Health 15: 848855.[Crossref] [Google Scholar]
  10. ter Horst R, Collin SM, Ritmeijer K, Bogale A, Davidson RN, , 2008. Concordant HIV infection and visceral leishmaniasis in Ethiopia: the influence of antiretroviral treatment and other factors on outcome. Clin Infect Dis 46: 17021709.[Crossref] [Google Scholar]
  11. Chaudhary RG, Bilimoria FE, Katare SK, , 2008. Diffuse cutaneous leishmaniasis: co-infection with human immunodeficiency virus (HIV). Indian J Dermatol Venereol Leprol 74: 641643.[Crossref] [Google Scholar]
  12. Gelanew T, Amogne W, Abebe T, Kuhls K, Hailu A, Schonian G, , 2010. A clinical isolate of Leishmania donovani with ITS1 sequence polymorphism as a cause of para-kala-azar dermal leishmaniasis in an Ethiopian human immunodeficiency virus-positive patient on highly active antiretroviral therapy. Br J Dermatol 163: 870874.[Crossref] [Google Scholar]
  13. Zijlstra EE, Musa AM, Khalil EA, el-Hassan IM, el-Hassan AM, , 2003. Post-kala-azar dermal leishmaniasis. Lancet Infect Dis 3: 8798.[Crossref] [Google Scholar]
  14. Chulay JD, Bryceson AD, , 1983. Quantitation of amastigotes of Leishmania donovani in smears of splenic aspirates from patients with visceral leishmaniasis. Am J Trop Med Hyg 32: 475479. [Google Scholar]
  15. Schonian G, Schweynoch C, Zlateva K, Oskam L, Kroon N, Graser Y, Presber W, , 1996. Identification and determination of the relationships of species and strains within the genus Leishmania using single primers in the polymerase chain reaction. Mol Biochem Parasitol 77: 1929.[Crossref] [Google Scholar]
  16. Schonian G, Nasereddin A, Dinse N, Schweynoch C, Schallig HD, Presber W, Jaffe CL, , 2003. PCR diagnosis and characterization of Leishmania in local and imported clinical samples. Diagn Microbiol Infect Dis 47: 349358.[Crossref] [Google Scholar]
  17. Kuhls K, Keilonat L, Ochsenreither S, Schaar M, Schweynoch C, Presber W, Schonian G, , 2007. Multilocus microsatellite typing (MLMT) reveals genetically isolated populations between and within the main endemic regions of visceral leishmaniasis. Microbes Infect 9: 334343.[Crossref] [Google Scholar]
  18. Gelanew T, Kuhls K, Hurissa Z, Weldegebreal T, Hailu W, Kassahun A, Abebe T, Hailu A, Schonian G, , 2010. Inference of population structure of Leishmania donovani strains isolated from different Ethiopian visceral leishmaniasis endemic areas. PLoS Negl Trop Dis 4: e889.[Crossref] [Google Scholar]
  19. Dieringer D, Schlötterer C, , 2003. Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite sets. Mol Ecol Notes 3: 167169.[Crossref] [Google Scholar]
  20. Kumar S, Tamura K, Nei M, , 2004. MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5: 150163.[Crossref] [Google Scholar]
  21. Couppie P, Clyti E, Sobesky M, Bissuel F, Del Giudice P, Sainte-Marie D, Dedet JP, Carme B, Pradinaud R, , 2004. Comparative study of cutaneous leishmaniasis in human immunodeficiency virus (HIV)-infected patients and non-HIV-infected patients in French Guiana. Br J Dermatol 151: 11651171.[Crossref] [Google Scholar]
  22. Turetz ML, Machado PR, Ko AI, Alves F, Bittencourt A, Almeida RP, Mobashery N, Johnson WD, Jr Carvalho EM, , 2002. Disseminated leishmaniasis: a new and emerging form of leishmaniasis observed in northeastern Brazil. J Infect Dis 186: 18291834.[Crossref] [Google Scholar]
  23. Barro-Traore F, Preney L, Traore A, Darie H, Tapsoba P, Bassole A, Sawadogo S, Niamba P, Grosshans E, Geniaux M, , 2008. Cutaneous leishmaniasis due to Leishmania major involving the bone marrow in an AIDS patient in Burkina Faso [in French]. Ann Dermatol Venereol 135: 380383.[Crossref] [Google Scholar]
  24. Jafari S, Hajiabdolbaghi M, Mohebali M, Hajjaran H, Hashemian H, , 2010. Disseminated leishmaniasis caused by Leishmania tropica in HIV-positive patients in the Islamic Republic of Iran. Mediterranean Health Journal 16: 30413044. [Google Scholar]
  25. Alvar J, Gutierrez-Solar B, Pachon I, Calbacho E, Ramirez M, Valles R, Guillen JL, Canavate C, Amela C, , 1996. AIDS and Leishmania infantum. New approaches for a new epidemiological problem. Clin Dermatol 14: 541546.[Crossref] [Google Scholar]
  26. Colebunders R, Depraetere K, Verstraeten T, Lambert J, Hauben E, Van Marck E, Maurer T, Banuls AL, Dujardin JC, , 1999. Unusual cutaneous lesions in two patients with visceral leishmaniasis and HIV infection. J Am Acad Dermatol 41: 847850.[Crossref] [Google Scholar]
  27. Antinori S, Longhi E, Bestetti G, Piolini R, Acquaviva V, Foschi A, Trovati S, Parravicini C, Corbellino M, Meroni L, , 2007. Post-kala-azar dermal leishmaniasis as an immune reconstitution inflammatory syndrome in a patient with acquired immune deficiency syndrome. Br J Dermatol 157: 10321036.[Crossref] [Google Scholar]
  28. Shelburne SA, Visnegarwala F, Darcourt J, Graviss EA, Giordano TP, White AC, Jr Hamill RJ, , 2005. Incidence and risk factors for immune reconstitution inflammatory syndrome during highly active antiretroviral therapy. AIDS 19: 399406.[Crossref] [Google Scholar]
  29. Boumis E, Chinello P, Della Rocca C, Paglia MG, Proietti MF, Petrosillo N, , 2006. Atypical disseminated leishmaniasis resembling post-kala-azar dermal leishmaniasis in an HIV-infected patient. Int J STD AIDS 17: 351353.[Crossref] [Google Scholar]
  30. al Jaser M, el-Yazigi A, Kojan M, Croft SL, , 1995. Skin uptake, distribution, and elimination of antimony following administration of sodium stibogluconate to patients with cutaneous leishmaniasis. Antimicrob Agents Chemother 39: 516519.[Crossref] [Google Scholar]
  31. Agostoni C, Dorigoni N, Malfitano A, Caggese L, Marchetti G, Corona S, Gatti S, Scaglia M, , 1998. Mediterranean leishmaniasis in HIV-infected patients: epidemiological, clinical, and diagnostic features of 22 cases. Infection 26: 9399.[Crossref] [Google Scholar]
  32. Pratlong F, Rioux JA, Marty P, Faraut-Gambarelli F, Dereure J, Lanotte G, Dedet JP, , 2004. Isoenzymatic analysis of 712 strains of Leishmania infantum in the south of France and relationship of enzymatic polymorphism to clinical and epidemiological features. J Clin Microbiol 42: 40774082.[Crossref] [Google Scholar]
  33. Kallel K, Pratlong F, Haouas N, Kaouech E, Belhadj S, Anane S, Dedet JP, Babba H, Chaker E, , 2008. Isoenzymatic variability of Leishmania infantum in Tunisia concerning 254 human strains. Acta Trop 106: 132136.[Crossref] [Google Scholar]
  34. Mahdi M, Elamin EM, Melville SE, Musa AM, Blackwell JM, Mukhtar MM, Elhassan AM, Ibrahim ME, , 2005. 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 5: 2933.[Crossref] [Google Scholar]
  35. Lewin S, Schonian G, El Tai N, Oskam L, Bastien P, Presber W, , 2002. Strain typing in Leishmania donovani by using sequence-confirmed amplified region analysis. Int J Parasitol 32: 12671276.[Crossref] [Google Scholar]
  36. El Tai NO, El Fari M, Mauricio I, Miles MA, Oskam L, El Safi SH, Presber WH, Schonian G, , 2001. Leishmania donovani: intraspecific polymorphisms of Sudanese isolates revealed by PCR-based analyses and DNA sequencing. Exp Parasitol 97: 3544.[Crossref] [Google Scholar]
  37. Alam MZ, Kuhls K, Schweynoch C, Sundar S, Rijal S, Shamsuzzaman AK, Raju BV, Salotra P, Dujardin JC, Schonian G, , 2009. Multilocus microsatellite typing (MLMT) reveals genetic homogeneity of Leishmania donovani strains in the Indian subcontinent. Infect Genet Evol 9: 2431.[Crossref] [Google Scholar]
  38. Mohamed HS, Ibrahim ME, Miller EN, Peacock CS, Khalil EA, Cordell HJ, Howson JM, El Hassan AM, Bereir RE, Blackwell JM, , 2003. Genetic susceptibility to visceral leishmaniasis in the Sudan: linkage and association with IL4 and IFNGR1. Genes Immun 4: 351355.[Crossref] [Google Scholar]
  39. Blackwell JM, Mohamed HS, Ibrahim ME, , 2004. Genetics and visceral leishmaniasis in the Sudan: seeking a link. Trends Parasitol 20: 268274.[Crossref] [Google Scholar]
  40. Stark D, Pett S, Marriott D, Harkness J, , 2006. Post-kala-azar dermal leishmaniasis due to Leishmania infantum in a human immunodeficiency virus type 1-infected patient. J Clin Microbiol 44: 11781180.[Crossref] [Google Scholar]
  41. Bittencourt A, Silva N, Straatmann A, Nunes VL, Follador I, Badaro R, , 2002. Post-kala-azar dermal leishmaniasis associated with AIDS. Braz J Infect Dis 6: 313316.[Crossref] [Google Scholar]
  42. Rihl M, Stoll M, Ulbricht K, Bange FC, Schmidt RE, , 2006. Successful treatment of post-kala-azar dermal leishmaniasis (PKDL) in a HIV infected patient with multiple relapsing leishmaniasis from western Europe. J Infect 53: e25e27.[Crossref] [Google Scholar]
  43. Ritmeijer K, Veeken H, Melaku Y, Leal G, Amsalu R, Seaman J, Davidson RN, , 2001. Ethiopian visceral leishmaniasis: generic and proprietary sodium stibogluconate are equivalent; HIV co-infected patients have a poor outcome. Trans R Soc Trop Med Hyg 95: 668672.[Crossref] [Google Scholar]
  44. Sepkowitz KA, , 2001. AIDS–the first 20 years. N Engl J Med 344: 17641772.[Crossref] [Google Scholar]
  45. el Hassan AM, Ghalib HW, Zijlstra EE, Eltoum IA, Satti M, Ali MS, Ali HM, , 1992. Post kala-azar dermal leishmaniasis in the Sudan: clinical features, pathology and treatment. Trans R Soc Trop Med Hyg 86: 245248.[Crossref] [Google Scholar]
  46. Ismail A, El Hassan AM, Kemp K, Gasim S, Kadaru AE, Moller T, Kharazmi A, Theander TG, , 1999. Immunopathology of post kala-azar dermal leishmaniasis (PKDL): T-cell phenotypes and cytokine profile. J Pathol 189: 615622.[Crossref] [Google Scholar]
  47. Ridolfo AL, Gervasoni C, Antinori S, Pizzuto M, Santambrogio S, Trabattoni D, Clerici M, Galli M, , 2000. Post-kala-azar dermal leishmaniasis during highly active antiretroviral therapy in an AIDS patient infected with Leishmania infantum . J Infect 40: 199202.[Crossref] [Google Scholar]
  48. Gasim S, Elhassan AM, Kharazmi A, Khalil EA, Ismail A, Theander TG, , 2000. The development of post-kala-azar dermal leishmaniasis (PKDL) is associated with acquisition of Leishmania reactivity by peripheral blood mononuclear cells (PBMC). Clin Exp Immunol 119: 523529.[Crossref] [Google Scholar]
  49. Lawn SD, Wilkinson RJ, , 2006. Immune reconstitution disease associated with parasitic infections following antiretroviral treatment. Parasite Immunol 28: 625633. [Google Scholar]

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  • Received : 27 Jan 2011
  • Accepted : 27 Feb 2011
  • Published online : 01 Jun 2011

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