• View in gallery
    Figure 1.

    Intrahistiocytic amastigote forms of Leishmania on a bone marrow specimen from the patient (May Grunwald Giemsa ×1,000).

  • 1.

    World Health Organization, 2007. Report of the Fifth Consultative Meeting on Leishmania/HIV Coinfection. Addis Ababa, Ethiopa: World Health Organization.

    • Search Google Scholar
    • Export Citation
  • 2.

    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.

    • Search Google Scholar
    • Export Citation
  • 3.

    Dedet JP, Roche B, Pratlong F, Cales-Quist D, Jouannelle J, Benichou JC, Huerre M, 1995. Diffuse cutaneous infection caused by a presumed monoxenous trypanosomatid in a patient infected with HIV. Trans R Soc Trop Med Hyg 89: 644646.

    • Search Google Scholar
    • Export Citation
  • 4.

    Noyes H, Pratlong F, Chance M, Ellis J, Lanotte G, Dedet JP, 2002. A previously unclassified trypanosomatid responsible for human cutaneous lesions in Martinique (French West Indies) is the most divergent member of the genus Leishmania ss. Parasitology 124: 1724.

    • Search Google Scholar
    • Export Citation
  • 5.

    Desbois N, Pratlong F, Quist D, Dedet JP, 2014. Leishmania (Leishmania) martiniquensis n. sp. (Kinetoplastida: Trypanosomatidae), description of the parasite responsible for cutaneous leishmaniasis in Martinique Island (French West Indies). Parasite 21: 12.

    • Search Google Scholar
    • Export Citation
  • 6.

    Liautaud B, Pape JW, DeHovitz JA, Thomas F, LaRoche AC, Verdier RI, Deschamps MM, Johnson WD, 1989. Pruritic skin lesions. A common initial presentation of acquired immunodeficiency syndrome. Arch Dermatol 125: 629632.

    • Search Google Scholar
    • Export Citation
  • 7.

    Mary C, Faraut F, Lascombe L, Dumon H, 2004. Quantification of Leishmania infantum DNA by a real-time PCR assay with high sensitivity. J Clin Microbiol 42: 52495255.

    • Search Google Scholar
    • Export Citation
  • 8.

    Zeledon R, 1992. Leishmaniasis in the Caribbean Islands. A review. Ann N Y Acad Sci 653: 154160.

  • 9.

    Garin YJ, Sulahian A, Meneceur P, Pratlong F, Prina E, Gangneux J, Dedet JP, Derouin F, 2001. Experimental pathogenicity of a presumed monoxenous trypanosomatid isolated from humans in a murine model. J Eukaryot Microbiol 48: 170176.

    • Search Google Scholar
    • Export Citation
  • 10.

    Courmes E, Escudie A, Fauran P, Monnerville A, 1966. First native case of human visceral leishmaniasis in Guadeloupe. Bull Soc Pathol Exot 59: 217226.

    • Search Google Scholar
    • Export Citation
  • 11.

    Cnudde F, Raccurt C, Boulard F, Terron-Aboud B, Nicolas M, Juminer B, 1994. Diffuse cutaneous leishmaniasis with visceral dissemination in an AIDS patient in Guadeloupe, West Indies. AIDS 8: 559560.

    • Search Google Scholar
    • Export Citation
  • 12.

    Kaplan JE, Benson C, Holmes KH, Brooks JT, Pau A, Masur H, 2009. Guidelines for prevention and treatment of opportunistic infections in HIV-infected adults and adolescents: recommendations from CDC, the National Institutes of Health, and the HIV Medicine Association of the Infectious Diseases Society of America. Recomm Rep 58: 1207.

    • Search Google Scholar
    • Export Citation
  • 13.

    Yanamandra U, Jairam A, Shankar S, Negi R, Guleria B, Nair V, 2011. Visceral leishmaniasis mimicking as second line anti retroviral therapy failure. Intern Med 50: 28552858.

    • Search Google Scholar
    • Export Citation
  • 14.

    Cruz I, Nieto J, Moreno J, Canavate C, Desjeux P, Alvar J, 2006. Leishmania/HIV co-infections in the second decade. Indian J Med Res 123: 357388.

  • 15.

    Cota GF, de Sousa MR, Rabello A, 2011. Predictors of visceral leishmaniasis relapse in HIV-infected patients: a systematic review. PLoS Negl Trop Dis 5: e1153.

    • Search Google Scholar
    • Export Citation
  • 16.

    Dedet JP, Gay F, Chatenay G, 1989. Isolation of Leishmania species from wild mammals in French Guiana. Trans R Soc Trop Med Hyg 83: 613615.

    • Search Google Scholar
    • Export Citation
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First Case of Visceral Leishmaniasis Caused by Leishmania martiniquensis

Bernard LiautaudDepartment of Tropical and Infectious Disease, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Department of Tropical and Infectious Disease, University Hospital of Avicenne, Bobigny, France; Parasitology and Mycology Laboratory, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Hematology Laboratory, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Hematology Unit, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; University Hospital of Montpellier, Unité Mixte de Recherche 5290, French National Reference Center for Leishmaniasis, Montpellier, France; Faculté des Antilles et de la Guyane, Institut National de la Santé et de la Recherche Medicale CIC1424 and EA4537, Martinique, French West Indies

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Nicolas VignierDepartment of Tropical and Infectious Disease, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Department of Tropical and Infectious Disease, University Hospital of Avicenne, Bobigny, France; Parasitology and Mycology Laboratory, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Hematology Laboratory, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Hematology Unit, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; University Hospital of Montpellier, Unité Mixte de Recherche 5290, French National Reference Center for Leishmaniasis, Montpellier, France; Faculté des Antilles et de la Guyane, Institut National de la Santé et de la Recherche Medicale CIC1424 and EA4537, Martinique, French West Indies

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Charline MiossecDepartment of Tropical and Infectious Disease, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Department of Tropical and Infectious Disease, University Hospital of Avicenne, Bobigny, France; Parasitology and Mycology Laboratory, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Hematology Laboratory, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Hematology Unit, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; University Hospital of Montpellier, Unité Mixte de Recherche 5290, French National Reference Center for Leishmaniasis, Montpellier, France; Faculté des Antilles et de la Guyane, Institut National de la Santé et de la Recherche Medicale CIC1424 and EA4537, Martinique, French West Indies

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Yves PlumelleDepartment of Tropical and Infectious Disease, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Department of Tropical and Infectious Disease, University Hospital of Avicenne, Bobigny, France; Parasitology and Mycology Laboratory, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Hematology Laboratory, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Hematology Unit, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; University Hospital of Montpellier, Unité Mixte de Recherche 5290, French National Reference Center for Leishmaniasis, Montpellier, France; Faculté des Antilles et de la Guyane, Institut National de la Santé et de la Recherche Medicale CIC1424 and EA4537, Martinique, French West Indies

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Moumini KoneDepartment of Tropical and Infectious Disease, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Department of Tropical and Infectious Disease, University Hospital of Avicenne, Bobigny, France; Parasitology and Mycology Laboratory, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Hematology Laboratory, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Hematology Unit, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; University Hospital of Montpellier, Unité Mixte de Recherche 5290, French National Reference Center for Leishmaniasis, Montpellier, France; Faculté des Antilles et de la Guyane, Institut National de la Santé et de la Recherche Medicale CIC1424 and EA4537, Martinique, French West Indies

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Delphine DeltaDepartment of Tropical and Infectious Disease, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Department of Tropical and Infectious Disease, University Hospital of Avicenne, Bobigny, France; Parasitology and Mycology Laboratory, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Hematology Laboratory, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Hematology Unit, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; University Hospital of Montpellier, Unité Mixte de Recherche 5290, French National Reference Center for Leishmaniasis, Montpellier, France; Faculté des Antilles et de la Guyane, Institut National de la Santé et de la Recherche Medicale CIC1424 and EA4537, Martinique, French West Indies

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Christophe RavelDepartment of Tropical and Infectious Disease, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Department of Tropical and Infectious Disease, University Hospital of Avicenne, Bobigny, France; Parasitology and Mycology Laboratory, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Hematology Laboratory, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Hematology Unit, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; University Hospital of Montpellier, Unité Mixte de Recherche 5290, French National Reference Center for Leishmaniasis, Montpellier, France; Faculté des Antilles et de la Guyane, Institut National de la Santé et de la Recherche Medicale CIC1424 and EA4537, Martinique, French West Indies

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André CabiéDepartment of Tropical and Infectious Disease, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Department of Tropical and Infectious Disease, University Hospital of Avicenne, Bobigny, France; Parasitology and Mycology Laboratory, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Hematology Laboratory, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Hematology Unit, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; University Hospital of Montpellier, Unité Mixte de Recherche 5290, French National Reference Center for Leishmaniasis, Montpellier, France; Faculté des Antilles et de la Guyane, Institut National de la Santé et de la Recherche Medicale CIC1424 and EA4537, Martinique, French West Indies

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Nicole DesboisDepartment of Tropical and Infectious Disease, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Department of Tropical and Infectious Disease, University Hospital of Avicenne, Bobigny, France; Parasitology and Mycology Laboratory, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Hematology Laboratory, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; Hematology Unit, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies; University Hospital of Montpellier, Unité Mixte de Recherche 5290, French National Reference Center for Leishmaniasis, Montpellier, France; Faculté des Antilles et de la Guyane, Institut National de la Santé et de la Recherche Medicale CIC1424 and EA4537, Martinique, French West Indies

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We report the first case of visceral leishmaniasis (VL) caused by Leishmania martiniquensis in the Caribbean, which until now, was known only to cause cutaneous leishmaniasis. The disease presented with fatigue, anemia, and hepatosplenomegaly in a 61-year-old man with human immunodeficiency virus (HIV) infection who was receiving antiretroviral therapy. Diagnosis was made by bone marrow biopsy. VL is life-threatening, and its emergence in the Caribbean is of concern.

Introduction

Intracellular protozoan of the Leishmania genus, mainly transmitted by sandflies, are the causative agents of leishmaniasis. More than 12 million people are currently infected worldwide.1 Among its different clinical presentations, visceral leishmaniasis (VL) is life-threatening. Human immunodeficiency virus (HIV) infection is one of the major risk factor for developing VL and reported in 2–12% of all cases.1,2

The new autochthonous and divergent L. (L.) martiniquensis n. sp. was first isolated in 1995; its taxonomical position was established in 2002, and it was named in 2014.35 This species is up to now restricted to Martinique and has been only reported in patients with cutaneous lesions. We report the first case of VL caused by this parasite in an immunocompromised HIV-infected patient.

Case Report

A 61-year-old heterosexual Caribbean male was diagnosed with acquired immunodeficiency syndrome (AIDS) prurigo in 2006.6 He worked as a painter and a coconut picker and seller. He was born and had always lived in Martinique, except from 1994 to 2001, when he had lived in Guadeloupe. He had traveled to northern Europe and Haiti. His sole medical history was hypertension. He had never used intravenous drugs. At the time of HIV diagnosis, no opportunistic infection was found. Immunological, virological, and therapeutic data are summarized in Table 1.

Table 1

Summary of biological and clinical data and history of treatment of a patient coinfected by HIV and autochthonous Leishmania in Martinique

  January of 2007 May of 2007 January of 2008 August of 2008 February of 2009 June of 2009 January of 2010 August of 2010 January of 2011 November of 2011 February of 2012 June of 2012 January of 2013 July of 2013
HIV-1 viral load (copies/mL) 1.6 × 106 485 49 40 < 40 < 40 < 20 < 20 < 20 27 < 20 < 20 < 20 < 20
CD4 count (/μL) 186 663 290 218 187 211 244 151 109 133 287 381 412 362
Lymphocytes (/μL) 1,280 2,210 1,285 1,830 1,367 949 833 939 1,624 2,409 2,613 2,061    
Total leukocytes (/μL) 4,580 5,530 4,200 3,650 5,350 4,130 3,110 2,730 5,230 3,610 5,920 7,250    
Hemoglobin (g/dL) 13 11 11 11 10 11 9 9 9 6 9 10 12 11
Platelet count (× 109/L) 166 214 206 220 250 216 201 152 241 111 273 300    
Clinical manifestations                   HSM and WL        
Others investigations                   BM+, bPCR+ bPCR− bPCR−   bPCR−
Serology IFA (retrospective) 1/640 1/640 1/320 1/320 1/320                  
Serology ELISA (retrospective) + +       +   +   +        
Red blood cells transfusion
Antibiotic SMX-TMP                 SMX-TMP      
cART   cART 1: ABC/3TC/LPV/r   cART 2: ABC/3TC/EFV    
Amphotericin B                   Yes      

ABC = abacavir; BM = bone marrow biopsy and aspiration; bPCR = blood Leishmania PCR; EFV = efavirenz; HSM = hepatosplenomegaly; LPV/r = lopinavir plus ritonavir; WL = weight lost; 3TC = lamivudine.

Combination antiretroviral therapy (cART) was introduced in May of 2007, with significant reduction of HIV viral load and increased CD4+ cell count 1 month later. However, at 1 year, although there was clinical improvement of prurigo and continued viral suppression, CD4 counts were decreasing. Genotypic testing for HIV-1 drug resistance on an initial sample had shown no transmitted resistance, and drug monitoring revealed normal absorption. Despite cART regimen switching in January of 2010, the CD4 counts continued to decline, and the patient remained virally suppressed (Table 1).

He progressively developed hepatosplenomegaly and a normochromic normocytic aregenerative anemia of < 10 g/dL. The patient had no fever but reported permanent fatigue. Sulfamethoxazole/trimethropin (SMX-TMP) toxicity was hypothesized because of a reduced serum folate level, but folinic acid supplementation failed to correct it. A bone marrow biopsy performed in November of 2011 revealed intrahistiocytic parasites consistent with the amastigote forms of Leishmania spp. (Figure 1).

Figure 1.
Figure 1.

Intrahistiocytic amastigote forms of Leishmania on a bone marrow specimen from the patient (May Grunwald Giemsa ×1,000).

Citation: The American Society of Tropical Medicine and Hygiene 92, 2; 10.4269/ajtmh.14-0205

The diagnosis was confirmed by Leishmania polymerase chain reaction (PCR) realized on whole blood with RV1/RV2 probes targeting a kinetoplastic DNA locus (145 bp).7 The molecular identification based on the ribosomal 18S RNA locus analysis gave a 100% identity with the sequence of the MHOM/MQ/92/MAR1 strain (GenBank accession number AF303938.1), a divergent Leishmania strain described for the first time in Martinique in 1995 and recently named L. martiniquensis.4,5 A retrospective analysis of several sera from our patient stored since 2007 detected high levels of antileishmanial antibodies by indirect immunofluorescence assay (IFA) and enzyme-linked immunosorbent assay (ELISA) using L. infantum antigen (Table 1). Immunoblot revealed two specific bands of 14 and 16 kDa, confirming the specificity of these antibodies.

The patient was treated with liposomal amphotericin B (4 mg/kg equal to 300 mg/day from day 1 to 5 and on days 10, 17, 24, 31, and 38 for a cumulative dose of 3 g) and also required a blood transfusion. Symptoms rapidly improved, with decreasing hepatosplenomegaly and disappearance of fatigue, and the patient remained asymptomatic more than 1 year later. Significant increases of hemoglobin level and CD4+ cell count above 350/mm3 followed as well as a negative blood Leishmania PCR 20 months later. The patient did not receive secondary prophylaxis.

Discussion

Leishmaniasis is endemic in Central and South America but rarely occurs in the Caribbean.8

The first cases of presumed autochthonous cutaneous leishmaniasis (CL) in Martinique were diagnosed based on direct examination of skin smears and consisted of localized CL in immunocompetent patients, except for one case of diffuse CL in an HIV-infected patient.3,4 More recently, seven additional CL cases (six of them were unpublished) were found to be caused by a new Leishmania species. None of these cases presented visceral dissemination. This parasite was identified by both molecular and isoenzymatic techniques and found to be a member of the Leishmania subgenus at the base of the phylogenetic tree.4 The new Leishmania taxon was recently described and named L. (L.) martiniquensis n. sp.5 Capacity of visceralization and dissemination has been shown in a murine model.9 This is the first reported case of VL caused by L. martiniquensis, which highlights the possibility of dissemination in immunocompromized patients of this new species as has been reported for other dermotropic leishmania.

VL is uncommon in the Caribbean. In Guadeloupe, three cases of possibly autochthonous VL have been observed. Two cases were presumed to be autochthonous based on epidemiological data but without species identification.10,11 In 2008, a third case of VL was diagnosed in Guadeloupe in an immunocompetent patient, but it was caused by L. infantum (unpublished data). No other autochthonous VL cases have been reported elsewhere in the Caribbean.8 Our patient most probably acquired leishmaniasis in Martinique, because L. martiniquensis has only been reported on this island, but late reactivation of an infection acquired in Guadeloupe or Haiti cannot be ruled out.

Although patients coinfected with VL and HIV commonly are very symptomatic,12 our patient was clinically well for a long time, but his immunological pattern mimicked that of failure of cART.13 Cases of VL initially presenting with isolated CD4+ cell count drops are uncommon.

VL/HIV coinfection is usually characterized by significantly lower cure rates of leishmaniasis and higher drug toxicity, relapse, and mortality rates than infection with VL in HIV-seronegative individuals.2,14 Although post-treatment increase in CD4+ cells is considered greatly predictive of relapse-free evolution,15 relapses have been reported in well-controlled HIV patients on cART, thus mandating prolonged follow-up.1,2 The patient has continued to do well with no relapse 1 year post-VL treatment.2

Research tracks have been paved to identify the parasitic cycle, sandfly vectors, and host reservoirs of Leishmania species in the Caribbean. Lutzomyia atroclavata has been identified in Martinique, Guadeloupe, and the Virgin Islands; black rats (Rattus rattus), mongooses (Herpestes auropunctatus), marsupials (Didelphis marsupialis), and canids are all potential animal reservoirs that should be investigated.8,16

The emergence of L. martiniquensis infection with the possibility of visceral extension could be of concern in the Caribbean region, where the prevalence of HIV infection is high.

ACKNOWLEDGMENTS

We are indebted to Brigitte Roche, who facilitated, in 1992, the identification of the first Leishmania MHOM/MQ/92/MAR1 strain. We are grateful to Ms. Marlene Ouka for technical assistance in management of stored sera samples and Patrick Hochedez and Vanessa Rouzier for reviewing the manuscript.

  • 1.

    World Health Organization, 2007. Report of the Fifth Consultative Meeting on Leishmania/HIV Coinfection. Addis Ababa, Ethiopa: World Health Organization.

    • Search Google Scholar
    • Export Citation
  • 2.

    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.

    • Search Google Scholar
    • Export Citation
  • 3.

    Dedet JP, Roche B, Pratlong F, Cales-Quist D, Jouannelle J, Benichou JC, Huerre M, 1995. Diffuse cutaneous infection caused by a presumed monoxenous trypanosomatid in a patient infected with HIV. Trans R Soc Trop Med Hyg 89: 644646.

    • Search Google Scholar
    • Export Citation
  • 4.

    Noyes H, Pratlong F, Chance M, Ellis J, Lanotte G, Dedet JP, 2002. A previously unclassified trypanosomatid responsible for human cutaneous lesions in Martinique (French West Indies) is the most divergent member of the genus Leishmania ss. Parasitology 124: 1724.

    • Search Google Scholar
    • Export Citation
  • 5.

    Desbois N, Pratlong F, Quist D, Dedet JP, 2014. Leishmania (Leishmania) martiniquensis n. sp. (Kinetoplastida: Trypanosomatidae), description of the parasite responsible for cutaneous leishmaniasis in Martinique Island (French West Indies). Parasite 21: 12.

    • Search Google Scholar
    • Export Citation
  • 6.

    Liautaud B, Pape JW, DeHovitz JA, Thomas F, LaRoche AC, Verdier RI, Deschamps MM, Johnson WD, 1989. Pruritic skin lesions. A common initial presentation of acquired immunodeficiency syndrome. Arch Dermatol 125: 629632.

    • Search Google Scholar
    • Export Citation
  • 7.

    Mary C, Faraut F, Lascombe L, Dumon H, 2004. Quantification of Leishmania infantum DNA by a real-time PCR assay with high sensitivity. J Clin Microbiol 42: 52495255.

    • Search Google Scholar
    • Export Citation
  • 8.

    Zeledon R, 1992. Leishmaniasis in the Caribbean Islands. A review. Ann N Y Acad Sci 653: 154160.

  • 9.

    Garin YJ, Sulahian A, Meneceur P, Pratlong F, Prina E, Gangneux J, Dedet JP, Derouin F, 2001. Experimental pathogenicity of a presumed monoxenous trypanosomatid isolated from humans in a murine model. J Eukaryot Microbiol 48: 170176.

    • Search Google Scholar
    • Export Citation
  • 10.

    Courmes E, Escudie A, Fauran P, Monnerville A, 1966. First native case of human visceral leishmaniasis in Guadeloupe. Bull Soc Pathol Exot 59: 217226.

    • Search Google Scholar
    • Export Citation
  • 11.

    Cnudde F, Raccurt C, Boulard F, Terron-Aboud B, Nicolas M, Juminer B, 1994. Diffuse cutaneous leishmaniasis with visceral dissemination in an AIDS patient in Guadeloupe, West Indies. AIDS 8: 559560.

    • Search Google Scholar
    • Export Citation
  • 12.

    Kaplan JE, Benson C, Holmes KH, Brooks JT, Pau A, Masur H, 2009. Guidelines for prevention and treatment of opportunistic infections in HIV-infected adults and adolescents: recommendations from CDC, the National Institutes of Health, and the HIV Medicine Association of the Infectious Diseases Society of America. Recomm Rep 58: 1207.

    • Search Google Scholar
    • Export Citation
  • 13.

    Yanamandra U, Jairam A, Shankar S, Negi R, Guleria B, Nair V, 2011. Visceral leishmaniasis mimicking as second line anti retroviral therapy failure. Intern Med 50: 28552858.

    • Search Google Scholar
    • Export Citation
  • 14.

    Cruz I, Nieto J, Moreno J, Canavate C, Desjeux P, Alvar J, 2006. Leishmania/HIV co-infections in the second decade. Indian J Med Res 123: 357388.

  • 15.

    Cota GF, de Sousa MR, Rabello A, 2011. Predictors of visceral leishmaniasis relapse in HIV-infected patients: a systematic review. PLoS Negl Trop Dis 5: e1153.

    • Search Google Scholar
    • Export Citation
  • 16.

    Dedet JP, Gay F, Chatenay G, 1989. Isolation of Leishmania species from wild mammals in French Guiana. Trans R Soc Trop Med Hyg 83: 613615.

    • Search Google Scholar
    • Export Citation

Author Notes

* Address correspondence to Nicolas Vignier, Department of Infectious and Tropical Diseases, University Hospital of Fort-de-France, 97200 Fort-de-France, Martinique, French West Indies. E-mail: vigniernicolas@yahoo.fr

Authors' addresses: Bernard Liautaud and Nicolas Vignier, Department of Infectious and Tropical Diseases, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies, E-mails: Bliautaud1@gmail.com and vigniernicolas@yahoo.fr. Charline Miossec and Nicole Desbois, Department of Parasitology and Mycology, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies, E-mails: charlinemiossec@hotmail.fr and nicole.desbois@chu-fortdefrance.fr. Yves Plumelle, Moumini Kone, and Delphine Delta, Department of Hematology, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies, E-mails: yves.plumelle@chu-fortdefrance.fr, mt.kone@chu-fortdefrance.fr, and delphine.delta@gmail.com. Christophe Ravel, Université Montpellier 1, Montpellier, France, and Regional University Hospital of Montpellier, UMR5290, French National Reference Center for Leishmaniasis University, Hospital of Montpellier, Montpellier, France, E-mail: christophe.ravel@univ-montp1.fr. André Cabié, Department of Infectious and Tropical Diseases and Inserm CIE802, University Hospital of Fort-de-France, Fort-de-France, Martinique, French West Indies, E-mail: andre.cabie@chu-fortdefrance.fr.

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