• 1.

    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
  • 2.

    Chang MR, Taira CL, Paniago AM, Taira DL, Cunha RV, Wanke B, 2007. Study of 30 cases of histoplasmosis observed in the Mato Grosso do Sul State, Brazil. Rev Inst Med Trop Sao Paulo 49: 3739.

    • Search Google Scholar
    • Export Citation
  • 3.

    Hot A, Schmulewitz L, Viard JP, Lortholary O, 2007. Fever of unknown origin in HIV/AIDS patients. Infect Dis Clin North Am 21: 10131032.

  • 4.

    Dikshit B, Wanchu A, Sachdeva RK, Sharma A, Das R, 2009. Profile of hematological abnormalities of Indian HIV infected individuals. BMC Blood Disord 9: 5.

    • Search Google Scholar
    • Export Citation
  • 5.

    Russo R, Laguna F, Lopez-Velez R, Medrano FJ, Rosenthal E, Cacopardo B, Nigro L, 2003. Visceral leishmaniasis in those infected with HIV: clinical aspects and other opportunistic infections. Ann Trop Med Parasitol 97 (Suppl 1): 99105.

    • Search Google Scholar
    • Export Citation
  • 6.

    Srivastava P, Dayama A, Mehrotra S, Sundar S, 2011. Diagnosis of visceral leishmaniasis. Trans R Soc Trop Med Hyg 105: 16.

  • 7.

    Cota GF, de Sousa MR, Demarqui FN, Rabello A, 2012. The diagnostic accuracy of serologic and molecular methods for detecting visceral leishmaniasis in HIV infected patients: meta-analysis. PLoS Negl Trop Dis 6: e1665.

    • Search Google Scholar
    • Export Citation
  • 8.

    Chappuis F, Rijal S, Soto A, Menten J, Boelaert M, 2006. A meta-analysis of the diagnostic performance of the direct agglutination test and rK39 dipstick for visceral leishmaniasis. BMJ 333: 723.

    • Search Google Scholar
    • Export Citation
  • 9.

    Pedras MJ, de Gouvea Viana L, de Oliveira EJ, Rabello A, 2008. Comparative evaluation of direct agglutination test, rK39 and soluble antigen ELISA and IFAT for the diagnosis of visceral leishmaniasis. Trans R Soc Trop Med Hyg 102: 172178.

    • Search Google Scholar
    • Export Citation
  • 10.

    Schallig HD, Canto-Cavalheiro M, da Silva ES, 2002. Evaluation of the direct agglutination test and the rK39 dipstick test for the sero-diagnosis of visceral leishmaniasis. Mem Inst Oswaldo Cruz 97: 10151018.

    • Search Google Scholar
    • Export Citation
  • 11.

    ter Horst R, Tefera T, Assefa G, Ebrahim AZ, Davidson RN, Ritmeijer K, 2009. Field evaluation of rK39 test and direct agglutination test for diagnosis of visceral leishmaniasis in a population with high prevalence of human immunodeficiency virus in Ethiopia. Am J Trop Med Hyg 80: 929934.

    • Search Google Scholar
    • Export Citation
  • 12.

    Goswami RP, Rahman M, Guha SK, 2007. Utility of K39 strip test in visceral leishmaniasis (VL) and HIV co-infected patients: an early report from eastern India. J Assoc Physicians India 55: 154155.

    • Search Google Scholar
    • Export Citation
  • 13.

    Antinori S, Calattini S, Longhi E, Bestetti G, Piolini R, Magni C, Orlando G, Gramiccia M, Acquaviva V, Foschi A, Corvasce S, Colomba C, Titone L, Parravicini C, Cascio A, Corbellino M, 2007. Clinical use of polymerase chain reaction performed on peripheral blood and bone marrow samples for the diagnosis and monitoring of visceral leishmaniasis in HIV-infected and HIV-uninfected patients: a single-center, 8-year experience in Italy and review of the literature. Clin Infect Dis 44: 16021610.

    • Search Google Scholar
    • Export Citation
  • 14.

    Bossuyt PM, Reitsma JB, Bruns DE, Gatsonis CA, Glasziou PP, Irwig LM, Moher D, Rennie D, de Vet HC, Lijmer JG, 2003. The STARD statement for reporting studies of diagnostic accuracy: explanation and elaboration. The Standards for Reporting of Diagnostic Accuracy Group. Croat Med J 44: 639650.

    • Search Google Scholar
    • Export Citation
  • 15.

    Wortmann G, Sweeney C, Houng HS, Aronson N, Stiteler J, Jackson J, Ockenhouse C, 2001. Rapid diagnosis of leishmaniasis by fluorogenic polymerase chain reaction. Am J Trop Med Hyg 65: 583587.

    • Search Google Scholar
    • Export Citation
  • 16.

    Gomes LI, Gonzaga FM, de Morais-Teixeira E, de Souza-Lima BS, Freire VV, Rabello A, 2012. Validation of quantitative real-time PCR for the in vitro assessment of antileishmanial drug activity. Exp Parasitol 131: 175179.

    • Search Google Scholar
    • Export Citation
  • 17.

    Musso O, Sommer P, Drouet E, Cotte L, Neyra M, Grimaud JA, Chevallier M, 1996. In situ detection of human cytomegalovirus DNA in gastrointestinal biopsies from AIDS patients by means of various PCR-derived methods. J Virol Methods 56: 125137.

    • Search Google Scholar
    • Export Citation
  • 18.

    dos Santos Marques LH, Gomes LI, da Rocha IC, da Silva TA, Oliveira E, Morais MH, Rabello A, Carneiro M, 2012. Low parasite load estimated by qPCR in a cohort of children living in urban area endemic for visceral leishmaniasis in Brazil. PLoS Negl Trop Dis 6: e1955.

    • Search Google Scholar
    • Export Citation
  • 19.

    Overbergh L, Valckx D, Waer M, Mathieu C, 1999. Quantification of murine cytokine mRNAs using real time quantitative reverse transcriptase PCR. Cytokine 11: 305312.

    • Search Google Scholar
    • Export Citation
  • 20.

    Harith AE, Kolk AH, Kager PA, Leeuwenburg J, Muigai R, Kiugu S, Kiugu S, Laarman JJ, 1986. A simple and economical direct agglutination test for serodiagnosis and sero-epidemiological studies of visceral leishmaniasis. Trans R Soc Trop Med Hyg 80: 583586.

    • Search Google Scholar
    • Export Citation
  • 21.

    Oliveira E, Saliba SW, Saliba JW, Rabello A, 2013. Validation of a direct agglutination test prototype kit for the diagnosis of visceral leishmaniasis. Trans R Soc Trop Med Hyg 107: 243247.

    • Search Google Scholar
    • Export Citation
  • 22.

    Hanley JA, McNeil BJ, 1982. The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143: 2936.

  • 23.

    Hanley JA, McNeil BJ, 1983. A method of comparing the areas under receiver operating characteristic curves derived from the same cases. Radiology 148: 839843.

    • Search Google Scholar
    • Export Citation
  • 24.

    Vercammen F, Berkvens D, Le Ray D, Jacquet D, Vervoort T, 1997. Development of a slide ELISA for canine leishmaniasis and comparison with four serological tests. Vet Rec 141: 328330.

    • Search Google Scholar
    • Export Citation
  • 25.

    Deborggraeve S, Boelaert M, Rijal S, De Doncker S, Dujardin JC, Herdewijn P, Buscher P, 2008. Diagnostic accuracy of a new Leishmania PCR for clinical visceral leishmaniasis in Nepal and its role in diagnosis of disease. Trop Med Int Health 13: 13781383.

    • Search Google Scholar
    • Export Citation
  • 26.

    Boelaert M, Aoun K, Liinev J, Goetghebeur E, Van der Stuyft P, 1999. The potential of latent class analysis in diagnostic test validation for canine Leishmania infantum infection. Epidemiol Infect 123: 499506.

    • Search Google Scholar
    • Export Citation
  • 27.

    Ogoina D, Obiako RO, Muktar HM, Adeiza M, Babadoko A, Hassan A, Bansi I, Iheonye H, Iyanda M, Tabi-Ajayi E, 2012. Morbidity and mortality patterns of hospitalised adult HIV/AIDS patients in the era of highly active antiretroviral therapy: a 4-year retrospective review from Zaria, northern Nigeria. AIDS Res Treat 2012: 940580.

    • Search Google Scholar
    • Export Citation
  • 28.

    Lins TB, Soares E de M, dos Santos FM, Mandacaru PM, Pina T, de Araujo Filho JA, 2012. Mycobacterium tuberculosis and human immunodeficiency virus coinfection in a tertiary care hospital in Midwestern Brazil. Infez Med 20: 108116.

    • Search Google Scholar
    • Export Citation
  • 29.

    World Health Organization, 2011. Global Health Sector Strategy on HIV/AIDS 2011–2015. Geneva: World Health Organization. Available at: http://whqlibdoc.who.int/publications/2011/9789241501651_eng.pdf. Accessed February 20, 2013.

    • Search Google Scholar
    • Export Citation
  • 30.

    Brasil, Ministério da Saúde, 2011. Departamento de DST, Aids e Hepatites Virais. AIDS/DST. Boletim Epidemiológico 8: 1160. Available at: http://www.aids.gov.br/sites/default/files/anexos/publicacao/2011/50652/boletim_aids_2011_final_m_pdf_26659.pdf. Accessed February 20, 2013.

    • Search Google Scholar
    • Export Citation
  • 31.

    Zijlstra EE, Ali MS, el-Hassan AM, el-Toum IA, Satti M, Ghalib HW, Kager PA, 1992. Kala-azar: a comparative study of parasitological methods and the direct agglutination test in diagnosis. Trans R Soc Trop Med Hyg 86: 505507.

    • Search Google Scholar
    • Export Citation
  • 32.

    Boelaert M, Rijal S, Regmi S, Singh R, Karki B, Jacquet D, Chappuis F, Campino L, Desjeux P, Le Ray D, Koirala S, Van der Stuyft P, 2004. A comparative study of the effectiveness of diagnostic tests for visceral leishmaniasis. Am J Trop Med Hyg 70: 7277.

    • Search Google Scholar
    • Export Citation
  • 33.

    Rutjes AW, Reitsma JB, Coomarasamy A, Khan KS, Bossuyt PM, 2007. Evaluation of diagnostic tests when there is no gold standard. A review of methods. Health Technol Assess 11: iii51.

    • Search Google Scholar
    • Export Citation
  • 34.

    Bossolasco S, Gaiera G, Olchini D, Gulletta M, Martello L, Bestetti A, Bossi L, Germagnoli L, Lazzarin A, Uberti-Foppa C, Cinque P, 2003. Real-time PCR assay for clinical management of human immunodeficiency virus-infected patients with visceral leishmaniasis. J Clin Microbiol 41: 50805084.

    • Search Google Scholar
    • Export Citation
  • 35.

    World Health Organization, 2010. Control of the Leishmaniasis: Report of a Meeting of the WHO Expert Committee on the Control of Leishmaniases. WHO Technical Report Series No. 949. Geneva: World Health Organization.

    • Search Google Scholar
    • Export Citation
  • 36.

    Chappuis F, Rijal S, Singh R, Acharya P, Karki BM, Das ML, Bovier PA, Desjeux P, Le Ray D, Koirala S, Loutan L, 2003. Prospective evaluation and comparison of the direct agglutination test and an rK39-antigen-based dipstick test for the diagnosis of suspected kala-azar in Nepal. Trop Med Int Health 8: 277285.

    • Search Google Scholar
    • Export Citation
  • 37.

    Boelaert M, El-Safi S, Hailu A, Mukhtar M, Rijal S, Sundar S, Wasunna M, Aseffa A, Mbui J, Menten J, Desjeux P, Peeling RW, 2008. 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 102: 3240.

    • Search Google Scholar
    • Export Citation
  • 38.

    Ritmeijer K, Melaku Y, Mueller M, Kipngetich S, O'Keeffe C, Davidson RN, 2006. Evaluation of a new recombinant K39 rapid diagnostic test for Sudanese visceral leishmaniasis. Am J Trop Med Hyg 74: 7680.

    • Search Google Scholar
    • Export Citation
  • 39.

    Bourgeois N, Lachaud L, Reynes J, Rouanet I, Mahamat A, Bastien P, 2008. Long-term monitoring of visceral leishmaniasis in patients with AIDS: relapse risk factors, value of polymerase chain reaction, and potential impact on secondary prophylaxis. J Acquir Immune Defic Syndr 48: 1319.

    • Search Google Scholar
    • Export Citation
  • 40.

    Cruz I, Canavate C, Rubio JM, Morales MA, Chicharro C, Laguna F, Jimenez-Mejias M, Sirera G, Videla S, Alvar J, 2002. A nested polymerase chain reaction (Ln-PCR) for diagnosing and monitoring Leishmania infantum infection in patients co-infected with human immunodeficiency virus. Trans R Soc Trop Med Hyg 96 (Suppl 1): S185S189.

    • Search Google Scholar
    • Export Citation
  • 41.

    Piarroux R, Gambarelli F, Toga B, Dumon H, Fontes M, Dunan S, Quilici M, 1996. Interest and reliability of a polymerase chain reaction on bone-marrow samples in the diagnosis of visceral leishmaniasis in AIDS. AIDS 10: 452453.

    • Search Google Scholar
    • Export Citation
  • 42.

    Campino L, Cortes S, Pires R, Oskam L, Abranches P, 2000. Detection of Leishmania in immunocompromised patients using peripheral blood spots on filter paper and the polymerase chain reaction. Eur J Clin Microbiol Infect Dis 19: 396398.

    • Search Google Scholar
    • Export Citation
  • 43.

    Nuzum E, White F 3rd, Thakur C, Dietze R, Wages J, Grogl M, Berman J, 1995. Diagnosis of symptomatic visceral leishmaniasis by use of the polymerase chain reaction on patient blood. J Infect Dis 171: 751754.

    • Search Google Scholar
    • Export Citation
 
 
 
 

 

 

 

 

 

 

 

 

 

Comparison of Parasitological, Serological, and Molecular Tests for Visceral Leishmaniasis in HIV-Infected Patients: A Cross-Sectional Delayed-Type Study

View More View Less
  • Eduardo de Menezes Hospital, Fundação Hospitalar do Estado de Minas Gerais (FHEMIG), Belo Horizonte, Minas Gerais, Brazil; Post Graduation Program in Adult Health Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil; Laboratório de Pesquisas Clínicas, Centro de Pesquisas René Rachou, Fundação Oswaldo Cruz (FIOCRUZ), Belo Horizonte, Minas Gerais, Brazil

The aim of this study was to evaluate the accuracy of invasive and non-invasive tests for diagnosis of visceral leishmaniasis (VL) in a large series of human immunodeficiency virus (HIV)-infected patients. In this delayed-type cross-sectional study, 113 HIV-infected symptomatic patients were evaluated by an adjudication committee after clinical follow-up to establish the presence or absence of VL as the target condition (reference test). The index tests were recombinant K39 antigen-based immunochromatographic test (rK39), indirect fluorescent antibody test (IFAT), prototype kit of direct agglutination test (DAT-LPC), and real-time polymerase chain reaction (qPCR) in peripheral blood. Compared with parasitological test and adjudication committee diagnosis or latent class model analyses, IFAT and rk39 dipstick test presented the lowest sensitivity. DAT-LPC exhibited good overall performance, and there was no statistical difference between DAT-LPC and qPCR diagnosis accuracy. Real-time PCR emerges as a less invasive alternative to parasitological examination for confirmation of cases not identified by DAT.

Author Notes

* Address correspondence to Gláucia Fernandes Cota, Avenida Augusto de Lima, 1715, Barro Preto, CEP: 30190002, Belo Horizonte, Minas Gerais, Brazil. E-mail: glauciacota@uol.com.br

Financial support: This work was supported by Fundação de Amparo à Pesquisa de Minas Gerais (FAPEMIG), Belo Horizonte, Minas Gerais, Brazil (Grant APQ-01562-11 to A.R.); FAPEMIG also provided scientific initiation scholarship for the undergraduate students A.L.P.d.M. and B.F.P. Financial support was also available from PDTIS-FIOCRUZ (Rede de Plataformas Tecnológicas do Programa de Desenvolvimento Tecnológico em Insumos para Saúde) [RID06] and National Counsel of Technological and Scientific Development (CNPq) Grant 311641/2009-1. A.R. is a research fellow of CNPq (304881/2009-0).

Authors' addresses: Gláucia Fernandes Cota, Eduardo de Menezes Hospital, Fundação Hospitalar do Estado de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil, and Laboratório de Pesquisas Clínicas, Centro de Pesquisas René Rachou, Fundação Oswaldo Cruz, Belo Horizonte, Minas Gerais, Brazil, E-mail: glauciacota@uol.com.br. Marcos Roberto de Sousa, Post Graduation Program in Adult Health Sciences, Universidade Federal de Minas Gerai, Belo Horizonte, Minas Gerais, Brazil, E-mail: sousa.mr@uol.com.br. Betânia Mara de Freitas Nogueira and Andréa Laender Pessoa de Mendonça, Eduardo de Menezes Hospital, Fundação Hospitalar do Estado de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil, E-mails: betaniamfn@hotmail.com and andrea.laender@yahoo.com.br. Luciana Inácia Gomes, Edward Oliveira, Tália Santana Machado Assis, Bruna Fernandes Pinto, Juliana Wilke Saliba, and Ana Rabello, Laboratório de Pesquisas Clínicas, Centro de Pesquisas René Rachou, Fundação Oswaldo Cruz, Belo Horizonte, Minas Gerais, Brazil, E-mails: lgomes@cpqrr.fiocruz.br, edwardjo@cpqrr.fiocruz.br, talia@cpqrr.fiocruz.br, bruna.fernandes@cpqrr.fiocruz.br, julianawilke@yahoo.com.br, and ana@cpqrr.fiocruz.br.

Save