Skip to main content Accessibility help
×
Home

Epidemiological, clinical and laboratory aspects of human visceral leishmaniasis (HVL) associated with human immunodeficiency virus (HIV) coinfection: a systematic review

  • Iolanda Graepp Fontoura (a1) (a2), David Soeiro Barbosa (a3), Antonio Marcus de Andrade Paes (a1) (a4), Floriacy Stabnow Santos (a2), Marcelino Santos Neto (a2), Volmar Morais Fontoura (a5), Jackson Mauricio Lopes Costa (a6) and Ana Lúcia Abreu Silva (a1) (a7)...
  • Please note a correction has been issued for this article.

Abstract

Coinfection with human visceral leishmaniasis (HVL) and human immunodeficiency virus (HIV) has become an emerging public health problem in several parts of the world, with high morbidity and mortality rates. A systematic review was carried out in the literature available in PubMed, Scielo and Lilacs related to HVL associated with HIV coinfection, seeking to analyze epidemiological, clinical and laboratory aspects. Of the 265 articles found, 15 articles were included in the qualitative analysis, which referred to the results of HVL treatment in patients coinfected with HIV. In the published articles between 2007 and 2015, 1171 cases of HVL/HIV coinfection were identified, 86% males, average age 34 years, liposomal amphotericin B was the most commonly used drug, cure rates 68 and 20% relapses and 19% deaths, five different countries, bone marrow was used in 10/15 manuscripts. HVL/HIV coinfection is a major challenge for public health, mainly due to the difficulty in establishing an accurate diagnosis, low response to treatment with high relapse rates and evolution to death. In addition, these two pathogens act concomitantly for the depletion of the immune system, contributing to worsening the clinical picture of these diseases, which requires effective surveillance and epidemiological control measures.

Copyright

Corresponding author

Author for correspondence: Iolanda Graepp Fontoura, E-mail: iolandagraepp@hotmail.com

References

Hide All
Abass, E, Kang, C, Martinkovic, F, Semião-Santos, SJ, Sundar, S, Walden, P, Piarroux, R, el Harith, A, Lohoff, M and Steinhoff, U (2015) Heterogeneity of Leishmania donovani parasites complicates diagnosis of visceral leishmaniasis: comparison of different serological tests in three endemic regions. PLoS ONE 10, e0116408.
Alexandrino-de-Oliveira, P, Santos-Oliveira, JR, Dorval, MEC, Da-Costa Fdas, CB, Pereira, GROL, Cunha RVda Paniago, AMM and Da-Cruz, AM (2010) HIV/AIDS-associated visceral leishmaniasis in patients from an endemic area in central-west Brazil. Memórias do Instituto Oswaldo Cruz 105, 692697.
Almeida-Souza, F, Taniwaki, NN, Amaral, ACF, Souza Cda SFde Calabrese Kda, S and Abreu-Silva, AL (2016) Ultrastructural changes and death of Leishmania infantum promastigotes induced by Morinda citrifolia Linn. Fruit (Noni) juice treatment. Evidence-Based Complementary and Alternative Medicine 2016, 19.
Alvar, J, Aparicio, P, Aseffa, A, Den Boer, M, Cañavate, C, Dedet, J.-P, Gradoni, L, Ter Horst, R, López-Vélez, R and Moreno, J (2008) The relationship between leishmaniasis and AIDS: the second 10 years. Clinical Microbiology Reviews 21, 334359, Table of contents.
Barbosa Júnior, WL, Ramos de Araújo, PS, Dias de Andrade, L, Aguiar Dos Santos, AM, Lopes da Silva, MA, Dantas-Torres, F and Medeiros, Z (2015) Rapid tests and the diagnosis of visceral leishmaniasis and human immunodeficiency virus/acquired immunodeficiency syndrome coinfection. The American Journal of Tropical Medicine and Hygiene 93, 967969.
Belo, VS, Struchiner, CJ, Barbosa, DS, Nascimento, BWL, Horta, MAP, da Silva, ES and Werneck, GL (2014) Risk factors for adverse prognosis and death in American visceral leishmaniasis: a meta-analysis. PLoS Neglected Tropical Diseases 8, e2982.
Botelho, ACA and Natal, D (2009) Primeira descrição epidemiológica da leishmaniose visceral em Campo Grande, Estado de Mato Grosso do Sul. Revista da Sociedade Brasileira de Medicina Tropical 42, 503508.
Bourgeois, N, Lachaud, L, Reynes, J, Rouanet, I, Mahamat, A and Bastien, P (2008) Long-term monitoring of visceral leishmaniasis in patients with AIDS. JAIDS Journal of Acquired Immune Deficiency Syndromes 48, 1319.
Burza, S, Mahajan, R, Sinha, PK, van Griensven, J, Pandey, K, Lima, MA, Sanz, MG, Sunyoto, T, Kumar, S, Mitra, G, Kumar, R, Verma, N and Das, P (2014 a) Visceral leishmaniasis and HIV co-infection in Bihar, India: long-term effectiveness and treatment outcomes with liposomal Amphotericin B (AmBisome). PLoS Neglected Tropical Diseases 8, e3053.
Burza, S, Mahajan, R, Sanz, MG, Sunyoto, T, Kumar, R, Mitra, G and Lima, MA (2014 b) HIV and visceral leishmaniasis coinfection in Bihar, India: an underrecognized and underdiagnosed threat against elimination. Clinical Infectious Diseases 59, 552555.
Carvalho, FL, Aires, DLS, Segunda, ZF, Azevedo CMPESDe Corrêa RDGCF, de Aquino, DMC and Caldas, ADJM (2013) The epidemiological profile of HIV-positive individuals and HIV-leishmaniasis co-infection in a referral center in São Luis, Maranhão, Brazil. Ciência & saúde coletiva 18, 13051312.
Carvalho, RM, Nascimento, LF, R.M DC and L.F.C N (2014) Space-time description of dengue outbreaks in Cruzeiro, Sao Paulo, in 2006 and 2011. Revista da Associação Médica Brasileira (1992) 60, 565570.
Castelo Branco, PV, Soares, R.-EP, de Jesus, LCL, Moreira, VR, Alves, HJ, de Castro Belfort, MR, Silva, VLM and Ferreira Pereira, SR (2016) The antileishmanial drug miltefosine (Impavido®) causes oxidation of DNA bases, apoptosis, and necrosis in mammalian cells. Mutation Research/Genetic Toxicology and Environmental Mutagenesis 806, 3439.
Costa, DL, Rocha, RL, Carvalho RMa Lima-Neto, AS, Harhay, MO, Costa, CHN, Barral-Neto, M and Barral, AP (2013 a) Serum cytokines associated with severity and complications of kala-azar. Pathogens and Global Health 107, 7887.
Costa, DJ, Carvalho RMde, A, Abbehusen, M, Teixeira, C, Pitombo, M, Trigo, J, Nascimento, F, Amorim, L, Abreu-Silva, AL, do Socorro Pires Cruz, M, Miranda, JC, Fukutani, K, de Oliveira, CI, Barral, A, Barral-Netto, M and Brodskyn, C (2013 b) Experimental infection of dogs with Leishmania and saliva as a model to study canine visceral leishmaniasis. PLoS ONE 8, e60535.
Cota, GF, de Sousa, MR and Rabello, A (2011) Predictors of visceral leishmaniasis relapse in HIV-infected patients: a systematic review. PLoS Neglected Tropical Diseases 5, e1153.
Cota, GF, de Sousa, MR, Demarqui, FN and Rabello, A (2012) The diagnostic accuracy of serologic and molecular methods for detecting visceral leishmaniasis in HIV infected patients: meta-analysis. PLoS Neglected Tropical Diseases 6, e1665.
Cota, GF, de Sousa, MR, Fereguetti, TO and Rabello, A (2013 a) Efficacy of anti-leishmania therapy in visceral leishmaniasis among HIV infected patients: a systematic review with indirect comparison. PLoS Neglected Tropical Diseases 7, e2195.
Cota, GF, de Sousa, MR, de Freitas Nogueira, BM, Gomes, LI, Oliveira, E, Assis, TSM, de Mendonça, ALP, Pinto, BF, Saliba, JW and Rabello, A (2013 b) Comparison of parasitological, serological, and molecular tests for visceral leishmaniasis in HIV-infected patients: a cross-sectional delayed-type study. The American Journal of Tropical Medicine and Hygiene 89, 570577.
Cota, GF, de Sousa, MR, de Mendonça, ALP, Patrocinio, A, Assunção, LS, de Faria, SR and Rabello, A (2014) Leishmania-HIV co-infection: clinical presentation and outcomes in an urban area in Brazil. PLoS Neglected Tropical Diseases 8, e2816.
Coura-Vital, W, Araújo VEMde Reis, IA, Amancio, FF, Reis, AB and Carneiro, M (2014) Prognostic factors and scoring system for death from visceral leishmaniasis: an historical cohort study in Brazil. PLoS Neglected Tropical Diseases 8, e3374.
Coutinho, JVSC, Santos, FSD Ribeiro, RDSP Oliveira, IBB Dantas, VB Santos, ABFS and Tauhata, JR (2017) Leishmaniose visceral e leishmaniose-HIV coinfecção: estudo comparativo. Revista da Sociedade Brasileira de Medicina Tropical 50(5), 670674.
Craft, N, Ezra, N and Ochoa, M (2010) Human immunodeficiency virus and leishmaniasis. Journal of Global Infectious Diseases 2, 248.
Das, S, Halder, A, Rabidas, VN, Mandal, A and Das, P (2014) Specific noninvasive detection of Leishmania donovani in desquamated buccal cell swab samples from human visceral Leishmaniasis-HIV coinfected patients. Journal of Clinical Microbiology 52, 12381241.
de Albuquerque, LCP, Mendonça, IR, Cardoso, PN, Baldaçara, LR, Borges, MRMM, Borges J da C and Pranchevicius MC da S (2014) HIV/AIDS-related visceral leishmaniasis: a clinical and epidemiological description of visceral leishmaniasis in northern Brazil. Revista da Sociedade Brasileira de Medicina Tropical 47, 3846.
de Almeida e Cavalcanti, AT, Medeiros, Z, Lopes, F, de Andrade, LD, Ferreira, V de M, Magalhães, V and Miranda-Filho D de, B (2012) Diagnosing visceral leishmaniasis and HIV/AIDS co-infection: a case series study in Pernambuco, Brazil. Revista do Instituto de Medicina Tropical de São Paulo 54, 4347.
de Almeida Pachioni, J, Magalhães JG, Lima, EJC, Bueno Lde, M, Barbosa, JF, de Sá, MM and Rangel-Yagui, CO (2013) Alkylphospholipids – a promising class of chemotherapeutic agents with a broad pharmacological spectrum. Journal of Pharmacy & Pharmaceutical Sciences: A Publication of the Canadian Society for Pharmaceutical Sciences, Société canadienne des sciences pharmaceutiques 16, 742759.
de Araújo, VEM, Morais, MHF, Reis, IA, Rabello, A and Carneiro, M (2012) Early clinical manifestations associated with death from visceral leishmaniasis. PLoS Neglected Tropical Diseases 6, e1511.
de Souza, GF, Biscione, F, Greco, DB and Rabello, A (2012 a). Slow clinical improvement after treatment initiation in Leishmania/HIV coinfected patients. Revista da Sociedade Brasileira de Medicina Tropical 45, 147150.
de Souza, VAF, Cortez LRPde, B, Dias, RA, Amaku, M, Ferreira Neto, JS, Kuroda RBdos, S and Ferreira, F (2012 b). Space-time cluster analysis of American visceral leishmaniasis in Bauru, São Paulo State, Brazil. Cadernos de Saúde Pública 28, 19491964.
Diro, E, Lynen, L, Mohammed, R, Boelaert, M, Hailu, A and van Griensven, J (2014 a) High parasitological failure rate of visceral leishmaniasis to sodium stibogluconate among HIV co-infected adults in Ethiopia. PLoS Neglected Tropical Diseases 8, e2875.
Diro, E, Lynen, L, Ritmeijer, K, Boelaert, M, Hailu, A and van Griensven, J (2014 b) Visceral leishmaniasis and HIV coinfection in East Africa. PLoS Neglected Tropical Diseases 8, e2869.
Diro, E, Ritmeijer, K, Boelaert, M, Alves, F, Mohammed, R, Abongomera, C, Ravinetto, R, De Crop, M, Fikre, H, Adera, C, Colebunders, R, van Loen, H, Menten, J, Lynen, L, Hailu, A and van Griensven, J (2015) Use of pentamidine as secondary prophylaxis to prevent visceral leishmaniasis relapse in HIV infected patients, the first twelve months of a prospective Cohort study. PLoS Neglected Tropical Diseases 9, e0004087.
Druzian, AF, de Souza, AS, de Campos, DN, Croda, J, Higa, MG, Dorval, MEC, Pompilio, MA, de Oliveira, PA and Paniago, AMM (2015) Risk factors for death from visceral leishmaniasis in an Urban Area of Brazil. PLoS Neglected Tropical Diseases 9, e0003982.
Dupnik, KM, Nascimento EL, Rodrigues-neto, JF, Keesen, T, Duarte, I and Jeronimo, SMB (2011) New challenges in the epidemiology and treatment of visceral leishmaniasis in periurban areas. Drug Development Research 72, 451462.
Fontoura, IG, Fontoura, VM and Nascimento, LFC (2016) Análise espacial da ocorrência de leishmaniose visceral no estado do Tocantins, Brasil. Ambiente e Agua – an Interdisciplinary Journal of Applied Science 11, 1088.
Galvão, TF, Pansani, TSA and Harrad, D (2015) Principais itens para relatar Revisões sistemáticas e Meta-análises: a recomendação PRISMA. Epidemiologia e Serviços de Saúde 24, 335342.
Granthon, AC, Braga, MV, Rodrigues, JCF, Cammerer, S, Lorente, SO, Gilbert, IH, Urbina, JA and de Souza, W (2007) Alterations on the growth and ultrastructure of Leishmania chagasi induced by squalene synthase inhibitors. Veterinary Parasitology 146, 2534.
Herrador, Z, Gherasim, A, Jimenez, BC, Granados, M, San Martín, JV and Aparicio, P (2015) Epidemiological changes in leishmaniasis in Spain according to hospitalization-based records, 1997–2011: raising awareness towards leishmaniasis in non-HIV patients. PLoS Neglected Tropical Diseases 9, e0003594.
Hurissa, Z, Gebre-Silassie, S, Hailu, W, Tefera, T, Lalloo, DG, Cuevas, LE and Hailu, A (2010) Clinical characteristics and treatment outcome of patients with visceral leishmaniasis and HIV co-infection in northwest Ethiopia. Tropical Medicine & International Health 15, 848855.
Inocêncio, RdL, Romero, GAS, Dorval, ME, Cruz, I, Cavalcante, C, Dujardin, JC, van Assche, T, Cos, P and Maes, L (2011) Drug susceptibility of Leishmania infantum (syn. Leishmania chagasi) isolates from Brazilian HIV-positive and HIV-negative patients. Journal of Antimicrobial Chemotherapy 66, 677679.
Lima, IP, Müller, MC, Holanda, TA, Harhay, M, Costa, CHN and Costa, DL (2013) Human immunodeficiency virus/Leishmania infantum in the first foci of urban American visceral leishmaniasis: clinical presentation from 1994 to 2010. Revista da Sociedade Brasileira de Medicina Tropical 46, 156160.
Lindoso, JA, Cota, GF, da Cruz, AM, Goto, H, Maia-Elkhoury, ANS, Romero, GAS, de Sousa-Gomes, ML, Santos-Oliveira, JR and Rabello, A (2014) Visceral leishmaniasis and HIV coinfection in Latin America. PLoS Neglected Tropical Diseases 8, e3136.
Lindoso, JAL, Cunha, MA, Queiroz, I, Valente, CH and Moreira, (2016) Leishmaniasis-HIV coinfection: current challenges. HIV/AIDS – Research and Palliative Care 8, 147156.
Machado, CJS, Silva, EG and Vilani, RM (2016) O uso de um instrumento de política de saúde pública controverso: a eutanásia de cães contaminados por leishmaniose no Brasil. Saúde e Sociedade 25, 247258.
Mahajan, R, Das, P, Isaakidis, P, Sunyoto, T, Sagili, KD, Lima, MA, Mitra, G, Kumar, D, Pandey, K, Van, geertruyden J.-P, Boelaert, M and Burza, S (2015) Combination treatment for visceral leishmaniasis patients coinfected with human immunodeficiency virus in India. Clinical Infectious Diseases 61, 12551262.
Marques, N, Cabral, S, , R, Coelho, F, Oliveira, J, Saraiva da Cunha, JG and Meliço Silvestre, A (2007) Visceral leishmaniasis and HIV infection in the HAART era. Acta Medica Portuguesa 20, 291298.
Martins-Melo, FR, Lima Mda, S, Alencar, CH, Ramos, AN and Heukelbach, J (2014) Epidemiological patterns of mortality due to visceral leishmaniasis and HIV/AIDS co-infection in Brazil, 2000–2011. Transactions of the Royal Society of Tropical Medicine and Hygiene 108, 338347.
Menon, SS, Rossi, R, Nshimyumukiza, L and Zinszer, K (2016) Decentralized control of human visceral leishmaniasis in endemic urban areas of Brazil: a literature review. Tropical Medicine and Health 44, 9.
Ministério da Saúde (2014) Manual de vigilância e controle da leishmaniose visceral. 1a. (ed. Ministério da Saúde, S. de V. em S.D. de V.) and Transmissíveis.). Brazil: Ministério da Saúde, Brasília-Distrito Federal, pp. 122.
Ministério da Saúde (2015) Manual de recomendações para diagnóstico, tratamento e acompanhamento de pacientes com a coinfecção Leishmania-HIV. 1a. (ed. Brasília, Ministério da Saúde, S. de V. em S.D. de V.) and Transmissíveis.). Brazil: Ministério da Saúde, Brasília-Distrito Federal, pp. 109.
Molina, I, Falco, V, Crespo, M, Riera, C, Ribera, E, Curran, A, Carrio, J, Diaz, M, Villar del Saz, S, Fisa, R, Lopez-Chejade, P, Ocana, I and Pahissa, A (2007) Efficacy of liposomal amphotericin B for secondary prophylaxis of visceral leishmaniasis in HIV-infected patients. Journal of Antimicrobial Chemotherapy 60, 837842.
Nascimento, ET, Moura, MLN, Queiroz, JW, Barroso, AW, Araujo, AF, Rego, EF, Wilson, ME, Pearson, RD and Jeronimo, SM (2011) The emergence of concurrent HIV-1/AIDS and visceral leishmaniasis in Northeast Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 105, 298300.
Ritmeijer, K, ter Horst, R, Chane, S, Aderie, EM, Piening, T, Collin, SM and Davidson, RN (2011) Limited effectiveness of high-dose liposomal Amphotericin B (AmBisome) for treatment of visceral leishmaniasis in an Ethiopian population with high HIV prevalence. Clinical Infectious Diseases 53, e152e158.
Santos-Oliveira, JR, Giacoia-Gripp, CBW, Alexandrino de Oliveira, P, Amato, VS, Lindoso, JÂL, Goto, H, Oliveira-Neto, MP, Mattos, MS, Grinsztejn, B, Morgado, MG and Da-Cruz, AM (2010) High levels of T lymphocyte activation in Leishmania-HIV-1 co-infected individuals despite low HIV viral load. BMC Infectious Diseases 10, 358.
Santos-Oliveira, JR, Regis, EG, Leal, CRB, Cunha, RV, Bozza, PT and Da-Cruz, AM (2011) Evidence that lipopolisaccharide may contribute to the cytokine storm and cellular activation in patients with visceral leishmaniasis. PLoS Neglected Tropical Diseases 5, e1198.
Santos-Oliveira, JR, Regis, EG, Giacoia-Gripp, CBW, Valverde, JG, Alexandrino-de-Oliveira, P, Lindoso, JÂL, Goto, H, Oliveira-Neto, MP, Guerra, JO, Grinsztejn, B, Jerônimo, SB, Morgado, MG and Da-Cruz, AM (2013) Microbial translocation induces an intense proinflammatory response in patients with visceral leishmaniasis and HIV type 1 coinfection. The Journal of Infectious Diseases 208, 5766.
Shamseer, L, Moher, D, Clarke, M, Ghersi, D, Liberati, A, Petticrew, M, Shekelle, P and Stewart, LA (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ 349, g7647g7647.
Silva, LA, Romero, HD, Fagundes, A, Nehme, N, Fernandes, O, Rodrigues, V, Costa, RT and Prata, A (2013) Use of the polymerase chain reaction for the diagnosis of asymptomatic leishmania infection in a visceral leishmaniasis-endemic area. Revista do Instituto de Medicina Tropical de São Paulo 55, 101104.
Sinha, PK, van Griensven, J, Pandey, K, Kumar, N, Verma, N, Mahajan, R, Kumar, P, Kumar, R, Das, P, Mitra, G, Flevaud, L, Ferreyra, C, Remartinez, D, Pece, M and Palma, PP (2011) Liposomal Amphotericin B for visceral leishmaniasis in human immunodeficiency virus-coinfected patients: 2-year treatment outcomes in Bihar, India. Clinical Infectious Diseases 53, e91e98.
Távora, LGF, Nogueira, MB and Gomes, ST (2015) Visceral Leishmaniasis/HIV co-infection in northeast Brazil: evaluation of outcome. The Brazilian Journal of Infectious Diseases: An Official Publication of the Brazilian Society of Infectious Diseases 19, 651656.
Van Griensven, J, Carrillo, E, López-Vélez, R, Lynen, L and Moreno, J (2014 a) Leishmaniasis in immunosuppressed individuals. Clinical Microbiology and Infection: The Official Publication of the European Society of Clinical Microbiology and Infectious Diseases 20, 286299.
Van Griensven, J, Diro, E, Lopez-Velez, R, Ritmeijer, K, Boelaert, M, Zijlstra, EE, Hailu, A and Lynen, L (2014 b). A screen-and-treat strategy targeting visceral leishmaniasis in HIV-infected individuals in endemic east African countries: the way forward? PLoS Neglected Tropical Diseases 8, e3011.
Van Griensven, J, Zijlstra, EE and Hailu, A (2014 c) Visceral leishmaniasis and HIV coinfection: time for concerted action. PLoS Neglected Tropical Diseases 8, e3023.
Viana, GMDC, Silva, MACND, Garcia, JVDS, Guimarães, HD, Júnior, A, Farias, G and Galvão, CDS (2017) Epidemiological profile of patients co-infected with visceral leishmaniasis and HIV/AIDS in Northeast, Brazil. Revista da Sociedade Brasileira de Medicina Tropical 50(5), 613620.
Wang, H, Wolock, TM, Carter, A, Nguyen, G, Kyu, HH, Gakidou, E, and Coates, MM (2016) Estimates of global, regional, and national incidence, prevalence, and mortality of HIV, 1980–2015: the Global Burden of Disease Study 2015. The Lancet HIV, 3(8), e361e387.
Whitehead, PJ, Drummond, AEE, Walker, MF and Parry, RH (2013) Interventions to reduce dependency in personal activities of daily living in community-dwelling adults who use homecare services: protocol for a systematic review. Systematic Reviews 2, 49.
World Health Organization (2010) Control of the Leishmaniases: Report of a Meeting of the WHO Expert Committee on the Control of Leishmaniases. Geneva, Switzerland.
World Health Organization (2015) Visceral Leishmaniasis: Control Strategies and Epidemiological Situation Update in East Africa. Geneva, Switzerland.

Keywords

Type Description Title
WORD
Supplementary materials

Graepp Fontoura et al. supplementary material
Table A

 Word (17 KB)
17 KB

Epidemiological, clinical and laboratory aspects of human visceral leishmaniasis (HVL) associated with human immunodeficiency virus (HIV) coinfection: a systematic review

  • Iolanda Graepp Fontoura (a1) (a2), David Soeiro Barbosa (a3), Antonio Marcus de Andrade Paes (a1) (a4), Floriacy Stabnow Santos (a2), Marcelino Santos Neto (a2), Volmar Morais Fontoura (a5), Jackson Mauricio Lopes Costa (a6) and Ana Lúcia Abreu Silva (a1) (a7)...
  • Please note a correction has been issued for this article.

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed

A correction has been issued for this article: