PKDL and Other Dermal Lesions in HIV Co-infected Patients with Leishmaniasis: Review of Clinical Presentation in Relation to Immune Responses

PLoS Neglected Tropical Diseases

Volumn 8, Issue 11, 2014, Pages

  Zijlstra, Eduard E ^a  

^a Rotterdam Centre for Tropical Medicine   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 18; INTERLEUKIN 2;

ARTICLE; DISEASE COURSE; DISEASE TRANSMISSION; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENCE; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; MIXED INFECTION; PREVALENCE; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SKIN LEISHMANIASIS; ADULT; COMPLICATION; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; LEISHMANIA; LEISHMANIA DONOVANI; MALE; PARASITOLOGY; PATHOLOGY; SKIN; SKIN DISEASE; VISCERAL LEISHMANIASIS;

ADULT; COINFECTION; FEMALE; HIV INFECTIONS; HUMANS; IMMUNOCOMPETENCE; LEISHMANIA; LEISHMANIA DONOVANI; LEISHMANIASIS, CUTANEOUS; LEISHMANIASIS, DIFFUSE CUTANEOUS; LEISHMANIASIS, MUCOCUTANEOUS; LEISHMANIASIS, VISCERAL; MALE; SKIN; SKIN DISEASES;

EID: 84920402043     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0003258     Document Type: Article

References (133)

1. WHO (2014) Leishmaniasis fact sheet. Available: http://www.who.int/mediacentre/factsheets/fs375/en. Accessed 19 October 2014.
2. Reithinger R, Dujardin JC, Louzir H, Pirmez C, Alexander B, et al. (2007) Cutaneous leishmaniasis. Lancet Infect Dis 7: 581–596.
3. Zijlstra EE, Musa AM, Khalil EA, el-Hassan IM, el-Hassan AM, (2003) Post-kala-azar dermal leishmaniasis. Lancet Infect Dis 3: 87–98.
4. van Griensven J, Carrillo E, Lopez-Velez R, Lynen L, Moreno J, (2014) Leishmaniasis in immunosuppressed individuals. Clin Microbiol Infect 20: 286–299 doi:10.1111/469-0691.12556
5. Vinhal FA, Afonso-Cardoso SR, Silva AG, Pereira CG, Sousa W, et al. (2007) A typical presentation of cutaneous leishmaniasis after renal transplantation. Nephrol Dial Transplant 22: 3674.
6. Chusri S, Hortiwakul T, Silpapojakul K, Siriyasatien P, (2012) Consecutive cutaneous and visceral leishmaniasis manifestations involving a novel Leishmania species in two HIV patients in Thailand. Am J Trop Med Hyg 87: 76–80.
7. El Hassan AM, Khalil EA, Elamin WM, El Hassan LA, Ahmed ME, et al. (2013) Misdiagnosis and mistreatment of post-kala-azar dermal leishmaniasis. Case Rep Med 2013: 351579.
8. Desjeux P, Alvar J, (2003) Leishmania/HIV co-infections: epidemiology in Europe. Ann Trop Med Parasitol 97 Suppl 13–15.
9. Rosenthal E, Marty P, Poizot-Martin I, Reynes J, Pratlong F, et al. (1995) Visceral leishmaniasis and HIV-1 co-infection in southern France. Trans R Soc Trop Med Hyg 89: 159–162.
10. World Health Organization (2006) WHO Case definitions of HIV for surveillance and revised clinical staging and immunological classification of HIV-related disease in adults and children, http://www.who.int/hiv/pub/guidelines/hivstaging/en/, Accessed 19 October 2014
11. Alvar J, Aparicio P, Aseffa A, Den Boer M, Cañavate C, et al. (2008) The relationship between leishmaniasis and AIDS: the second 10 years. Clin Microbiol Rev 21: 334–359.
12. Bentwich Z, (2003) Concurrent infections that rise the HIV viral load. J HIV Ther 8: 72–75.
13. Rabello A, Orsini M, Disch J, (2003) Leishmania/HIV co-infection in Brazil: an appraisal. Ann Trop Med Parasitol 97 Suppl 117–28.
14. World Health Organization (1997) Leishmania/HIV co-infection. Epidemiological analysis of 692 retrospective cases. Wkly Epidemiol Rec 72: 49–54.
15. Burza S, Mahajan R, Sanz MG, Sunyoto T, Kumar R, et al. (2014) HIV and Visceral Leishmaniasis Coinfection in Bihar, India: An Underrecognized and Underdiagnosed Threat Against Elimination. Clin Infect Dis 15: 552–555.
16. Scaglia M, Malfitano A, Douville H, Sacchi P, Gatti S, et al. (1996) Dermonodular and visceral leishmaniasis due to Leishmania infantum with a new isoenzyme pattern: report of a case involving a patient with AIDS. Clin Infect Dis 22: 376–377.
17. Gelanew T, Hurissa Z, Diro E, Kassahun A, Kuhls K, et al. (2011) Disseminated cutaneous leishmaniasis resembling post-kala-azar dermal leishmaniasis caused by Leishmania donovani in three patients co-infected with visceral leishmaniasis and human immunodeficiency virus/acquired immunodeficiency syndrome in Ethiopia. Am J Trop Med Hyg 84: 906–912.
18. Santos-Oliveira JR, Da-Cruz AM, Pires LH, Cupolillo E, Kuhls K, et al. (2011) Atypical lesions as a sign of cutaneous dissemination of visceral leishmaniasis in a human immunodeficiency virus-positive patient simultaneously infected by two viscerotropic Leishmania species. Am J Trop Med Hyg 85: 55–59.
19. Frade AF, Costa DL, Costa CH, Aquino D, Van Weyenburgh J, et al. (2011) TGFB1 and IL8 gene polymorphisms and susceptibility to visceral leishmaniasis. Infect Genet Evol 11: 912–916.
20. Katara GK, Ansari NA, Singh A, Ramesh V, Salotra P, (2012) Evidence for involvement of Th17 type responses in post kala azar dermal leishmaniasis (PKDL). PLoS Negl Trop Dis 6: e1703.
21. Katara GK, Raj A, R K, Avishek K, Kaushal H, et al. (2013) Analysis of localized immune responses reveals presence of Th17 and Treg cells in cutaneous leishmaniasis due to Leishmania tropica. BMC Immunology 14: 52.
22. Alexander J, Brombacher F, (2012) T helper1/T helper2 cells and resistance/susceptibility to Leishmania infection: is this paradigm still relevant? Front Immunol 1: 80 doi:10.3389/fimmu.2012.000803
23. Castellano LR, Llaguno M, Silva MV, Machado JR, Correia D, et al. (2011) Immunophenotyping of circulating T cells in a mucosal leishmaniasis patient coinfected with HIV. Rev Soc Bras Med Trop 44: 520–521.
24. Castellano LR, Filho DC, Algiro L, Dessein H, Prata A, et al. (2009) Th1/Th2 immune responses are associated with active cutaneous leishmaniasis and clinical cure is associated with strong interferon-gamma production. Hum Immunol 70: 383–390.
25. Gonzalez-Lombana C, Gimblet C, Bacellar O, Oliveira WW, Passos S, et al. (2013) IL-17 mediates immunopathology in the absence of IL-10 following Leishmania major infection. PLoS Pathog 9: e1003243.
26. Khalil EA, Khidir SA, Musa AM, Musa BY, Elfaki ME, et al. (2013) Post-Kala-Azar Dermal Leishmaniasis: A Paradigm of Paradoxical Immune Reconstitution Syndrome in Non-HIV/AIDS Patients. J Trop Med 2013: 275253.
27. Gasim S, Elhassan AM, Kharazmi A, Khalil EA, Ismail A, et al. (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: 523–529.
28. Ismail A, Gadir AF, Theander TG, Kharazmi A, El Hassan AM, (2006) Pathology of post-kala-azar dermal leishmaniasis: a light microscopical, immunohistochemical, and ultrastructural study of skin lesions and draining lymph nodes. J Cutan Pathol 33: 778–787.
29. Bixler S, Mattapallil JJ, (2013) Loss and dysregulation of Th17 cells during HIV infection. Clin Dev Immunol 2013: 852418.
30. Wolday D, Berhe N, Britton S, Akuffo H, (2000) HIV-1 alters T helper cytokines, interleukin-12 and interleukin-18 responses to the protozoan parasite Leishmania donovani. AIDS 14: 921–929.
31. Rodrigues MZ, Grassi MF, Mehta S, Zhang XQ, Gois LL, et al. (2011) Th1/Th2 cytokine profile in patients coinfected with HIV and Leishmania in Brazil. Clin Vaccine Immunol 18: 1765–1769.
32. Gois LL, Mehta S, Rodrigues MZ, (2013) Schooley RT, Badaro R, et al (2013) Decreased memory T-cell response and function in human immunodeficiency virus-infected patients with tegumentary leishmaniasis. Mem Inst Oswaldo Cruz 109: 9–14 doi:10.1590/0074-0276130174
33. Santos-Oliveira JR, Giacoia-Gripp CB, Alexandrino de Oliveira P, Amato VS, Lindoso JA, et al. (2010) High levels of T lymphocyte activation in Leishmania-HIV-1 co-infected individuals despite low HIV viral load. BMC Infect Dis 10: 358 doi:10.1186/1471-2334-10-358
34. Aukrust P, Liabakk ND, Müller F, Lien F, Esperik T, et al. (1994) Serum levels of tumor necrosis factor-alpha (TNF alpha) and soluble TNF receptors in human deficiency virus type 1 infections-correlations to clinical, immunolgic, and virologic parameters. J Infect Dis 169: 420–424.
35. Castellano LR, Llaguno M, Silva MV, Machado JR, Correia D, et al. (2011) Immunophenotyping of circulating T cells in a mucosal leishmaniasis patient coinfected with HIV. Revista da Sociedade Brasileira de Medicina Tropical 44: 520–521.
36. Zijlstra EE, Alvar J (2012) The Post-Kala-azar Dermal Leishmaniasis (PKDL) atlas: a manual for health workers. Geneva: World Health Organization.
37. Turetz ML, Machado AA, Ko AI, Bittencourt A, Almeida RP, et al. (2002) Disseminated leishmaniasis: a new and emerging form of leishmaniasis observed in northeastern Brazil. J Infect Dis 186: 1829–1834.
38. Couppié P, Clyti E, Sainte-Marie D, Dedet JP, Carme B, et al. (2004) Disseminated cutaneous leishmaniasis due to Leishmania guyanensis: case of a patient with 425 lesions. Am J Trop Med Hyg 71: 558–560.
39. World Health Organization (2010) WHO Technical report Series 949: Control of the leishmaniases. Geneva: WHO.
40. Diro E, Lynen L, Ritmeijer K, Boelaert M, Hailu A, et al. (2014) Visceral Leishmaniasis and HIV coinfection in East Africa. PLoS Negl Trop Dis 8: e2869 doi:10.1371/journal.pntd.0002869
41. Ritmeijer K, Dejenie A, Assefa Y, Hundie TB, Mesure J, et al. (2006) A comparison of miltefosine and sodium stibogluconate for treatment of visceral leishmaniasis in an Ethiopian population with high prevalence of HIV infection. Clin Infect Dis 43: 357–364.
42. Burza S, Sinha PK, Mahajan R, Sanz MG, Lima MA, et al. (2014) Post Kala-Azar dermal leishmaniasis following treatment with 20 mg/kg liposomal amphotericin B (Ambisome) for primary visceral leishmaniasis in Bihar, India. PLoS Negl Trop Dis 8: e2611 doi:10.1371/journal.pntd.0002611
43. Antinori S, Longhi E, Bestetti G, Piolini R, Acquaviva V, et al. (2007) Post-kala-azar dermal leishmaniasis as an immune reconstitution inflammatory syndrome in a patient with acquired immune deficiency syndrome. Br J Dermatol 157: 1032–1036.
44. Farooq U, Choudhary S, Chacon AH, Lebrun E, Shiman MI, et al. (2013) Post-kala-azar dermal leishmaniasis in HIV-infected patients with AIDS: a report of two cases diagnosed in the USA. Int J Dermatol 52: 1098–1104.
45. Gilad J, Borer A, Hallel-Halevy D, Riesenberg K, Alkan M, et al. (2001) Post-kala-azar dermal leishmaniasis manifesting after initiation of highly active anti-retroviral therapy in a patient with human immunodeficiency virus infection. Isr Med Assoc J 3: 451–452.
46. Ramos A, Cruz I, Munez E, Salas C, Fernandez A, et al. (2008) Post-kala-azar dermal Leishmaniasis and uveitis in an HIV-positive patient. Infection 36: 184–186.
47. 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: 1178–1180.
48. Boumis E, Chinello P, Della Rocca C, Paglia MG, Proietti MF, et al. (2006) Atypical disseminated leishmaniasis resembling post-kala-azar dermal leishmaniasis in an HIV-infected patient. Int J STD AIDS 17: 351–353.
49. Bittencourt A, Silva N, Straatmann A, Nunes VL, Follador I, et al. (2002) Post-kala-azar dermal leishmaniasis associated with AIDS. Braz J Infect Dis 6: 313–316.
50. Colebunders R, Depraetere K, Verstraeten T, Lambert J, Hauben E, et al. (1999) Unusual cutaneous lesions in two patients with visceral leishmaniasis and HIV infection. J Am Acad Dermatol 41: 847–850.
51. Shah S, Shah A, Prajapati S, Bilimoria F, (2010) Post-kala-azar dermal leishmaniasis in HIV-positive patients: A study of two cases. Indian J Sex Transm Dis 31: 42–44.
52. Catorze G, Alberto J, Afonso A, Vieira R, Cortes S, et al. (2006) [Leishmania infantum/HIV co-infection: cutaneous lesions following treatment of visceral leishmaniasis]. Ann Dermatol Venereol 133: 39–42.
53. 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: e25–27.
54. Belay AD, Asafa Y, Mesure J, Davidson RN, (2006) Successful miltefosine treatment of post-kala-azar dermal leishmaniasis occurring during antiretroviral therapy. Ann Trop Med Parasitol 100: 223–227.
55. Alsina-Gibert M, López-Lerma I, Martinez-Chamorro E, Herrero-Mateu C, (2006) Cutaneous manifestations of visceral leishmaniasis resistant to liposomal amphotericin B in an HIV-positive patient. Arch Dermatol 142: 787–789.
56. Guffanti M, Gaiera G, Bossolasco S, Ceserani N, Ratti D, et al. (2008) Post-Kala-Azar dermal leishmaniasis in an HIV-1-infected woman: recovery after amphotericin B following failure of oral miltefosine. Am J Trop Med Hyg 79: 715–718.
57. González-Beato MJ, Moyano B, Sánchez C, González-Beato MT, Pérez-Molina JA, et al. (2000) Kaposi's sarcoma-like lesions and other nodules as cutaneous involvement in AIDS-related visceral leishmaniasis. Br J Dermatol 143: 1316–1318.
58. Calza L, D'Antuono A, Marinacci G, Manfredi R, Colangeli V, et al. (2004) Disseminated cutaneous leishmaniasis after visceral disease in a patient with AIDS. J Am Acad Dermatol 50: 461–465.
59. Silva ED, Andrade LD, Araujo PS, Silveira VM, Padilha CE, et al. (2013) Case study of a patient with HIV-AIDS and visceral leishmaniasis co-infection in multiple episodes. Rev Inst Med Trop Sao Paulo 55: 425–428.
60. 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: 670–675.
61. Mondain-Miton V, Toussaint-Gari M, Hofman P, Marty P, Carles M, et al. (1995) Atypical leishmaniasis in a patient infected with human immunodeficiency virus. Clin Infect Dis 21: 663–665.
62. Postigo C, Llamas R, Zarco C, Rubio R, Pulido F, et al. (1997) Cutaneous lesions in patients with visceral leishmaniasis and HIV infection. J Infect 35: 265–268.
63. Pasquau F, Ena J, Sanchez R, Cuadrado JM, Amador C, et al. (2005) Leishmaniasis as an opportunistic infection in HIV-infected patients: determinants of relapse and mortality in a collaborative study of 228 episodes in a Mediterreanean region. Eur J Clin Microbiol Infect Dis 24: 411–418.
64. Cnudde F, Raccurt C, Boulard F, Terron-Aboud B, Nicolas M, et al. (1994) Diffuse cutaneous leishmaniasis with visceral dissemination in an AIDS patient in Guadeloupe, West Indies. AIDS 8: 559–560.
65. Ara M, Maillo C, Peon G, Clavel A, Cuesta J, et al. (1998) Visceral leishmaniasis with cutaneous lesions in a patient infected with human immunodeficiency virus. Br J Dermatol 139: 114–117.
66. Rosatelli JB, Souza CS, Soares FA, Foss NT, Roselino AM, (1998) Generalized cutaneous leishmaniasis in acquired immunodeficiency syndrome. J Eur Acad Dermatol Venereol 10: 229–232.
67. Pourahmad M, Hooshmand F, Rahiminejad M, (2009) Cutaneous leishmaniasis associated with visceral leishmaniasis in a case of acquired immunodeficiency syndrome (AIDS). Int J Dermatol 48: 59–61.
68. Bualert L, Charungkiattikul W, Thongsuksai P, Mungthin M, Siripattanapipong S, et al. (2012) Autochthonous disseminated dermal and visceral leishmaniasis in an AIDS patient, southern Thailand, caused by Leishmania siamensis. Am J Trop Med Hyg 86: 821–824.
69. Gobels K, Feldt T, Oette M, Richter J, Harms G, et al. (2003) Visceral leishmaniasis presenting as subcutaneous nodules in a HIV-positive patient. Eur J Clin Microbiol Infect Dis 22: 329–331.
70. Carnaúba D, JrKonishi CT, Petri V, Martinez IC, Shimizu L, et al. (2009) Atypical disseminated leishmaniasis similar to post-kala-azar dermal leishmaniasis in a Brazilian AIDS patient infected with Leishmania (Leishmania) infantum chagasi: a case report. Int J Infect Dis 13: e504–507.
71. Puig L, Pradinaud R, (2003) Leishmania and HIV co-infection: dermatological manifestations. Ann Trop Med Parasitol 97 Suppl 1107–114 doi:10.1016/j.ijid.2009.01.022
72. Rubio FA, Robayna G, Herranz P, Torres E, Peña JM, et al. (1997) Leishmaniasis presenting as a psoriasifrom eruption in AIDS. Br J Dermatol 136: 792–794.
73. Kumar P, Sharma PK, Jain RK, Gautam RK, Bhardwaj M, et al. (2007) Oral ulcer as an unusual feature of visceral leishmaniasis in an AIDS patient. Indian J Med Sci 61: 97–101.
74. Amato VS, Nicodemo AC, Amato JG, Boulos M, Neto VA, (2000) Mucocutaneous leishmaniasis associated with HIV infection treated successfully with liposomal amphotericin B (AmBisome). J Antimicrob Chemother 46: 341–342.
75. Barrio J, Lecona M, Cosin J, Olalquiaga FJ, Hernanz JM, et al. (1996) Leishmania infection occurring in herpes zoster lesions in an HIV-positive patient. Br J Dermatol 134: 164–166.
76. Espana A, Hermida JM, Montilla P, Buzon L, (1990) [Cutaneous and systemic leishmaniasis with a herpesvirus infection in an AIDS patient]. Rev Clin Esp 187: 437.
77. Del Giudice P, (1996) Leishmania infection occurring in herpes zoster lesions in an HIV positive patient. Br J Dermatol 135: 1005–1006.
78. Gallego MA, Aguilar A, Plaza S, Gomez JM, Burgos F, et al. (1996) Kaposi's sarcoma with an intense parasitization by Leishmania. Cutis 57: 103–105.
79. Castellano VM, Rodriguez-Peralto JL, Alonso S, Gomez-De la Fuente E, Ibarrola C, (1999) Dermatofibroma parasitized by Leishmania in HIV infection: a new morphologic expression of dermal Kala Azar in an immunodepressed patient. J Cutan Pathol 26: 516–519.
80. Perrin C, Taillan B, Hofman P, Mondain V, Lefichoux Y, et al. (1995) Atypical cutaneous histological features of visceral leishmaniasis in acquired immunodeficiency syndrome. Am J Dermatopathol 17: 145–150.
81. Daudén E, Peñas PF, Rios L, Jimenez M, Fraga J, et al. (1996) Leishmaniasis presenting as a dermatomyositis-like eruption in AIDS. J Am Acad Dermatol 35: 316–319.
82. Karram S, Lova A, Hamam H, Habib RH, Khalifeh I, (2012) Transepidermal elimination in cutaneous leishmaniasis: a multiregional study. J Cutan Pathol 39: 406–412.
83. Taillan B, Marty P, Schneider S, Telle H, Fuzibet JG, et al. (1992) Visceral leishmaniasis involving a cutaneous Kaposi's sarcoma lesion and free areas of skin. Eur J Med 1: 255.
84. Yebra M, Segovia J Manzano L, Vargas JA, Bernaldo de Quirós, et al. (1988) Disseminated-to-skin kala-azar and the acquired immunodeficiency syndrome. Ann Intern Med 108: 490–491.
85. Ndiaye PB, Develoux M, Dieng MT, Huerre M, (1996) [Diffuse cutaneous leishmaniasis and acquired immunodeficiency syndrome in a Senegalese patient]. Bull Soc Pathol Exot 89: 282–286.
86. Guiguemde RT, Sawadogo OS, Bories C, Traore KL, Nezien D, et al. (2003) Leishmania major and HIV co-infection in Burkina Faso. Trans R Soc Trop Med Hyg 97: 168–169.
87. Mattos M, Caiza A, Fernandes O, Goncalves AJ, Pirmez C, et al. (1998) American cutaneous leishmaniasis associated with HIV infection: report of four cases. J Eur Acad Dermatol Venereol 10: 218–225.
88. Couppié P, Clyti E, Sobesky M, Bissuel F, Del Giudice P, et al. (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: 1165–1171.
89. Guerra JA, Coelho LI, Pereira FR, Siqueira AM, Ribeiro RL, et al. (2011) American tegumentary leishmaniasis and HIV-AIDS association in a tertiary care center in the Brazilian Amazon. Am J Trop Med Hyg 85: 524–527.
90. Niamba P, Traoré, Goumbri-Lompo O, Labrèze C, Traoré-Barro F, et al. (2006) [Cutaneous leishmania in HIV patient in Ouagadougou: clinical and therapeutic aspects]. Ann Dermatol Venereol 133: 537–542.
91. Lindoso JA, Barbosa RN, Posada-Vergara MP, Duarte MI, Oyafuso LK, et al. (2009) Unusual manifestations of tegumentary leishmaniasis in AIDS patients from the New World. Br J Dermatol 160: 311–318.
92. Lartey M, Adusei L, Hanson-Nortey L, Addy J, (2006) Coinfection of Cutaneous Leishmaniasis and HIV Infection. Ghana Med J 40: 110–112.
93. Pérez C, Solias Y, Rodriguez G, (2006) [Diffuse cutaneous leishmaniasis in a patient with AIDS]. Biomedica 26: 485–497.
94. Goto H, Lauletta Lindoso JA, (2012) Cutaneous and mucocutaneous leishmaniasis. Infect Dis Clin North Am 26: 293–307.
95. Nogueira-Castañon MC, Pereira CA, Furtado T, (1996) Unusual association of American cutaneous leishmaniasis and acquired immunodeficiency syndrome. Int J Dermatol 35: 295–297.
96. Mehta V, Balachandran C, Rao R, Dil SK, Indusri L, (2009) Diffuse cutaneous leishmaniasis in HIV. Dermatol Online J 15: 9.
97. Chaudhary RG, Bilimoria FE, Katare SK, (2008) Diffuse cutaneous leishmaniasis: co-infection with human immunodeficiency virus (HIV). Indian J Dermatol Venereol Leprol 74: 641–643.
98. Khandelwal K, Bumb RA, Mehta RD, Kaushal H, Lezama-Davila C, et al. (2011) A patient presenting with diffuse cutaneous leishmaniasis (DCL) as a first indicator of HIV infection in India. Am J Trop Med Hyg 85: 64–65.
99. Soni P, Prasad N, Khandelwal K, Ghiya BC, Mehta RD, et al. (2011) Unresponsive cutaneous leishmaniasis and HIV co-infection: report of three cases. Indian J Dermatol Venereol Leprol 77: 251.
100. Niamba P, Goumbri-Lompo O, Traore A, Barro-Traore F, Soudre RT, (2007) Diffuse cutaneous leishmaniasis in an HIV-positive patient in western Africa. Australas J Dermatol 48: 32–34.
101. Schraner C, Hasse B, Hasse U, Baumann D, Faeh A, et al. (2005) Successful treatment with miltefosine of disseminated cutaneous leishmaniasis in a severely immunocompromised patient infected with HIV-1. Clin Infect Dis 40: e120–124.
102. Durand I, Beylot-Barry M, Weill FX, Doutre MS, Beylot C, (1998) [Disseminated cutaneous leishmaniasis revealing human immunodeficiency virus infection]. Ann Dermatol Venereol 125: 268–270.
103. 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. East Mediterr Health J 16: 340–343.
104. Purohit HM, Shah AN, Amin BK, Shevkani MR, (2012) Diffuse cutaneous leishmaniasis - A rare cutaneous presentation in an HIV-positive patient. Indian J Sex Transm Dis 33: 62–64.
105. Barro-Traore F, Preney L, Traore A, Darie H, Tapsoba P, et al. (2008) [Cutaneous leishmaniasis due to Leishmania major involving the bone marrow in an AIDS patient in Burkina Faso]. Ann Dermatol Venereol 135: 380–383.
106. Balkhair A, Ben Abid F, (2008) Gastric and cutaneous dissemination of visceral leishmaniasis in a patient with advanced HIV. Int J Infect Dis 12: 111–113.
107. Vazquez-Pineiro T, Fernandez Alvarez JM, Gonzalo Lafuente JC, Cano J, Gimeno M, et al. (1998) Visceral leishmaniasis: a lingual presentation in a patient with HIV infection. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 86: 179–182.
108. Gonzalez-Anglada MI, Pena JM, Barbado FJ, Gonzalez JJ, Redondo C, et al. (1994) Two cases of laryngeal leishmaniasis in patients infected with HIV. Eur J Clin Microbiol Infect Dis 13: 509–511.
109. Milián MA, Bagán JV, Jiménez Y, Pérez A, Scully C, (2002) Oral leishmaniasis in a HIV-positive patient. Report of a case involving the palate. Oral Dis 8: 59–61.
110. Ehlert N, Seilmaier M, Guggemos W, Löscher T, Meurer A, et al. (2013) [Severe oral mucositis in a patient with HIV infection]. Dtsch Med Wochenschr 138: 1601–1605 doi:10.1055/s-0033-1343296
111. Nigro L, Montineri A, La Rosa R, Zuccarello M, Iacobello C, et al. (2003) Visceral leishmaniasis and HIV co-infection: a rare case of pulmonary and oral localization. Infez Med 11: 93–96.
112. Banuls J, Boix V, Portilla J, Silvestre JF, (1995) Leishmaniasis as a cause of oral disease in HIV infection. AIDS 9: 96–98.
113. de Souza e Souza I, Naiff RD, Guimarães TC, Naiff MF, Cupolillo E, et al. (1998) American cutaneous leishmaniasis due to Leishmania (Viannia) guyanensis as an initial clinical presentation of human immunodeficiency virus infection. J Eur Acad Dermatol Venereol 10: 214–217.
114. Machado ES, Braga Mda P, Da Cruz AM, Coutinho SG, Vieira AR, et al. (1992) Disseminated American muco-cutaneous leishmaniasis caused by Leishmania braziliensis braziliensis in a patient with AIDS: a case report. Mem Inst Oswaldo Cruz 87: 487–492.
115. Madeddu G, Fiori ML, Ena P, Riu F, Lovigu C, et al. (2014) Mucocutaneous leishmaniasis as presentation of HIV infection in Sardinia, insular Italy. Parasitol Int 63: 35–36.
116. Sampaio RN, Salaro CP, Resende P, de Paula CD, (2002) [American cutaneous leishmaniasis associated with HIV/AIDS: report of four clinical cases]. Rev Soc Bras Med Trop 35: 651–654.
117. Lopez-Velez R, Perez-Molina JA, Guerrero A, Baquero F, Villarrubia J, et al. (1998) Clinicoepidemiologic characteristics, prognostic factors, and survival analysis of patients coinfected with human immunodeficiency virus and Leishmania in an area of Madrid, Spain. Am J Trop Med Hyg 58: 436–443.
118. Miralles ES, Nunez M, Hilara Y, Harto A, Moreno R, et al. (1994) Mucocutaneous leishmaniasis and HIV. Dermatology 189: 275–277.
119. Sanchez P, Bosch RJ, de Galvez MV, Rodrigo AB, Herrera E, (2001) Mucocutaneous leishmaniasis in a patient with the human immunodeficiency virus. Int J STD AIDS 12: 687–689.
120. Alvar J, Ballesteros J, Soler R, Benito A, van Eys G, et al. (1990) Mucocutaneous leishmaniasis due to Leishmania (Leishmania) infantum: biochemical characterization. Am J Trop Med Hyg 43: 614–618.
121. Shelburne SA, 3rdHamill RJ, (2003) The immune reconstitution inflammatory syndrome. AIDS Rev 5: 67–79.
122. Lawn SD, Wilkinson RJ, (2006) Immune reconstitution disease associated with parasitic infections following antiretroviral treatment. Parasite Immunol 28: 625–633.
123. Ridolfo AL, Gervasoni C, Antinori S, Pizzuto M, Santambrogio S, et al. (2000) Post-kala-azar dermal leishmaniasis during highly active antiretroviral therapy in an AIDS patient infected with Leishmania infantum. J Infect 40: 199–202.
124. de la Rosa R, Pineda JA, Delgado J, Macias J, Morillas F, et al. (2001) Influence of highly active antiretroviral therapy on the outcome of subclinical visceral leishmaniasis in human immunodeficiency virus-infected patients. Clin Infect Dis 32: 633–635.
125. Berry A, Abraham B, Dereure J, Pinzani V, Bastien P, et al. (2004) Two case reports of symptomatic leishmaniasis in AIDS patients concomitant with immune reconstitution due to antiretroviral therapy. Scand J Infect Dis 36: 225–227.
126. Jimenez-Exposito MJ, Alonso-Villaverde C, Sarda P, Masana L, (1999) Visceral leishmaniasis in HIV-infected patients with non-detectable HIV-1 viral load after highly active antiretroviral therapy. AIDS 13: 152–153.
127. Albrecht H, Sobottka I, Emminger C, Jablonowski H, Just G, et al. (1996) Visceral leishmaniasis emerging as an important opportunistic infection in HIV-infected persons living in areas nonendemic for Leishmania donovani. Arch Pathol Lab Med 120: 189–198.
128. Albrecht H, (1998) Leishmaniosis-new perspectives on an underappreciated opportunistic infection. AIDS 12: 2225–2226.
129. Blanche P, Gombert B, Rivoal O, Abad S, Salmon D, et al. (2002) Uveitis due to Leishmania major as part of HAART-induced immune restitution syndrome in a patient with AIDS. Clin Infect Dis 34: 1279–1280.
130. Posada-Vergara MP, Lindoso JA, Tolezano JE, Pereira-Chioccola VL, Silva MV, et al. (2005) Tegumentary leishmaniasis as a manifestation of immune reconstitution inflammatory syndrome in 2 patients with AIDS. J Infect Dis 192: 1819–1822.
131. Sinha S, Fernandez G, Kapila R, Lambert WC, Schwartz RA, (2008) Diffuse cutaneous leishmaniasis associated with the immune reconstitution inflammatory syndrome. Int J Dermatol 47: 1263–1270.
132. Chrusciak-Talhari A, Ribeiro-Rodrigues R, Talhari C, Silva RM, JrFerreira LC, et al. (2009) Tegumentary leishmaniasis as the cause of immune reconstitution inflammatory syndrome in a patient co-infected with human immunodeficiency virus and Leishmania guyanensis. Am J Trop Med Hyg 81: 559–564.
133. Kérob D, Bouaziz JD, Sarfati C, Pavie J, Vignon-Pennamen MD, et al. (2006) First case of cutaneous reconstitution inflammatory syndrome associated with HIV infection and leishmaniasis. Clin Infect Dis 43: 664–666.