Hostname: page-component-76fb5796d-x4r87 Total loading time: 0 Render date: 2024-04-27T02:07:04.329Z Has data issue: false hasContentIssue false
  • English
  • Français

Leishmania infantum: illness, transmission profile and risk factors for asymptomatic infection in an endemic metropolis in Brazil

Published online by Cambridge University Press:  29 November 2016

LETÍCIA HELENA DOS SANTOS MARQUES ,
IARA CAIXETA MARQUES DA ROCHA ,
ILKA AFONSO REIS ,
GISELE MACEDO RODRIGUES DA CUNHA ,
EDWARD OLIVEIRA ,
THAIS RIBEIRO PFEILSTICKER ,
VALDELAINE ETELVINA MIRANDA DE ARAÚJO ,
MARIA HELENA FRANCO MORAIS ,
ANA RABELLO  and
MARIÂNGELA CARNEIRO
LETÍCIA HELENA DOS SANTOS MARQUES
Affiliation:
Laboratório de Epidemiologia de Doenças Infecciosas e Parasitárias, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 31270-901, Belo Horizonte, MG, Brazil
IARA CAIXETA MARQUES DA ROCHA
Affiliation:
Laboratório de Epidemiologia de Doenças Infecciosas e Parasitárias, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 31270-901, Belo Horizonte, MG, Brazil Secretaria Municipal de Saúde, Prefeitura de Belo Horizonte, 30710-040, Belo Horizonte, MG, Brazil
ILKA AFONSO REIS
Affiliation:
Departamento de Estatística, Instituto de Ciências Exatas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
GISELE MACEDO RODRIGUES DA CUNHA
Affiliation:
Laboratório de Epidemiologia de Doenças Infecciosas e Parasitárias, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 31270-901, Belo Horizonte, MG, Brazil
EDWARD OLIVEIRA
Affiliation:
Laboratório de Pesquisas Clínicas, Centro de Pesquisas René Rachou, Fundação Oswaldo Cruz, 30190-002, Belo Horizonte, MG, Brazil
THAIS RIBEIRO PFEILSTICKER
Affiliation:
Laboratório de Epidemiologia de Doenças Infecciosas e Parasitárias, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 31270-901, Belo Horizonte, MG, Brazil
VALDELAINE ETELVINA MIRANDA DE ARAÚJO
Affiliation:
Ministério da Saúde, 70058-900, Esplanada dos Ministérios, DF, Brazil
MARIA HELENA FRANCO MORAIS
Affiliation:
Secretaria Municipal de Saúde, Prefeitura de Belo Horizonte, 30710-040, Belo Horizonte, MG, Brazil
ANA RABELLO
Affiliation:
Laboratório de Pesquisas Clínicas, Centro de Pesquisas René Rachou, Fundação Oswaldo Cruz, 30190-002, Belo Horizonte, MG, Brazil
MARIÂNGELA CARNEIRO*
Affiliation:
Laboratório de Epidemiologia de Doenças Infecciosas e Parasitárias, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 31270-901, Belo Horizonte, MG, Brazil Pós-Graduação em Ciências da Saúde: Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
*
*Corresponding author: Laboratório de Epidemiologia das Doenças Infecciosas e Parasitárias, Parasitologia, Instituto de Ciências Biológicas, Campus Pampulha, Universidade Federal de Minas Gerais, Avenida Antônio Carlos, 6627, CEP 31270-901, Belo Horizonte, MG, Brazil. E-mail: mcarneir@icb.ufmg.br
Get access Rights & Permissions [Opens in a new window]

Summary

To evaluate the distribution of asymptomatic infection by Leishmania infantum in a metropolis in Brazil with different relative risks (RRs) for disease and risk factors associated with the infection, an ecological study was conducted using a Bayesian approach to estimate the RR of human visceral leishmaniasis (HVL) based on cases between 2008 and 2011. The areas were categorized and selected according to disease incidence: low (area-1), medium (area-2) and high (area-3). Cross-sectional study enrolling 935 children was used to estimate the prevalence of infection by L. infantum. Volunteers from these three areas were tested for L. infantum infection by ELISA (rK39 and soluble antigens). Infection prevalence rates were estimated and compared with the RR of disease. Multilevel logistic regression model evaluated the relationship between infection and the analysed variables. The RR of HVL was distributed heterogeneously in the municipality. The infection prevalence rates were: 34·9% in area-1; 29·3% in area-2; and 33·6% in area-3, with no significant differences between these areas. The variables ‘Presence of backyards in the neighbourhood’ and ‘Younger children’ were associated with L. infantum infection. We conclude that infection by L. infantum affects a significant proportion of the infant population regardless of the RR of disease.

Keywords

visceral leishmaniasisasymptomatic infectioninfectionrelative riskBrazil
Type
Research Article
Information
Parasitology , Volume 144 , Issue 4 , April 2017 , pp. 546 - 556
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

ABEP (2012). Associação Brasileira de Empresas de Pesquisa. Vol. 2012. Available: http://www.abep.org/Default.aspx. Accessed April 2014.Google Scholar
Alonso, D. P., Ferreira, A. F., Ribolla, P. E., de Miranda Santos, I. K., do Socorro Pires e Cruz, M., Aecio de Carvalho, F., Abatepaulo, A. R., Lamounier Costa, D., Werneck, G. L., Farias, T. J., Soares, M. J. and Costa, C. H. (2007). Genotypes of the mannan-binding lectin gene and susceptibility to visceral leishmaniasis and clinical complications. Journal of Infectious Diseases 195, 1212–1217.CrossRefGoogle ScholarPubMed
Alvar, J., Velez, I. D., Bern, C., Herrero, M., Desjeux, P., Cano, J., Jannin, J. and den Boer, M. (2012). Leishmaniasis worldwide and global estimates of its incidence. PLoS ONE 7, e35671.CrossRefGoogle ScholarPubMed
Assuncao, R. M., Barreto, S. M., Guerra, H. L. and Sakurai, E. (1998). Maps of epidemiological rates: a Bayesian approach. Cadernos de saude publica 14, 713–723.Google Scholar
Assuncao, R. M., Reis, I. A. and Oliveira, C. D. (2001). Diffusion and prediction of Leishmaniasis in a large metropolitan area in Brazil with a Bayesian space-time model. Statistics in Medicine 20, 2319–2335.Google Scholar
Badaro, R., Jones, T. C., Lorenco, R., Cerf, B. J., Sampaio, D., Carvalho, E. M., Rocha, H., Teixeira, R. and Johnson, W. D. Jr. (1986). A prospective study of visceral leishmaniasis in an endemic area of Brazil. Journal of Infectious Diseases 154, 639–649.CrossRefGoogle Scholar
Besag, J., York, J. C. and Mollié, A. (1991). Bayesian image restoration, with two applications in spatial statistics (with discussion). Annals of the Institute of Statistical Mathematics 43, 1–59.CrossRefGoogle Scholar
Caldas, A. J., Costa, J. M., Silva, A. A., Vinhas, V. and Barral, A. (2002). Risk factors associated with asymptomatic infection by Leishmania chagasi in north-east Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 21–28.CrossRefGoogle ScholarPubMed
Carneiro, M., Moreno, E. C., Goncalves, A. V., Lambertucci, J. R. and Antunes, C. M. F. (2011). Visceral leishmaniasis: challenges in identifying subclinical Leishmania infection. Drug Development Research 72, 442–450.Google Scholar
Costa, C. H., Pereira, H. F. and Araujo, M. V. (1990). Visceral leishmaniasis epidemic in the State of Piaui, Brazil, 1980–1986. Revista de Saude Publica 24, 361–372.Google Scholar
Costa, C. H., Stewart, J. M., Gomes, R. B., Garcez, L. M., Ramos, P. K., Bozza, M., Satoskar, A., Dissanayake, S., Santos, R. S., Silva, M. R., Shaw, J. J., David, J. R. and Maguire, J. H. (2002). Asymptomatic human carriers of Leishmania chagasi . American Journal of Tropical Medicine and Hygiene 66, 334–337.CrossRefGoogle ScholarPubMed
Custodio, E., Gadisa, E., Sordo, L., Cruz, I., Moreno, J., Nieto, J., Chicharro, C., Aseffa, A., Abraham, Z., Hailu, T. and Canavate, C. (2012). Factors associated with Leishmania asymptomatic infection: results from a cross-sectional survey in highland northern Ethiopia. PLoS Neglected Tropical Diseases 6, e1813.Google Scholar
de Almeida, A. S., Medronho Rde, A. and Werneck, G. L. (2011). Identification of risk areas for visceral leishmaniasis in Teresina, Piaui State, Brazil. American Journal of Tropical Medicine and Hygiene 84, 681–687.Google Scholar
de Araujo, V. E., Morais, M. H., Reis, I. A., Rabello, A. and Carneiro, M. (2012). Early clinical manifestations associated with death from visceral leishmaniasis. PLoS Neglected Tropical Diseases 6, e1511.Google Scholar
de Araujo, V. E., Pinheiro, L. C., Almeida, M. C., de Menezes, F. C., Morais, M. H., Reis, I. A., Assuncao, R. M. and Carneiro, M. (2013). Relative risk of visceral leishmaniasis in Brazil: a spatial analysis in urban area. PLoS Neglected Tropical Diseases 7, e2540.Google Scholar
de Gouvea Viana, L., de Assis, T. S., Orsini, M., da Silva, A. R., de Souza, G. F., Caligiorne, R., da Silva, A. C., Peruhype-Magalhaes, V., Marciano, A. P., Martins-Filho, O. A. and Rabello, A. (2008). Combined diagnostic methods identify a remarkable proportion of asymptomatic Leishmania (Leishmania) chagasi carriers who present modulated cytokine profiles. Transactions of the Royal Society of Tropical Medicine and Hygiene 102, 548–555.Google Scholar
dos Santos Marques, L. H., Gomes, L. I., da Rocha, I. C., da Silva, T. A., Oliveira, E., Morais, M. H., Rabello, A. and 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 Neglected Tropical Diseases 6, e1955.Google Scholar
Elnaiem, D. E., Schorscher, J., Bendall, A., Obsomer, V., Osman, M. E., Mekkawi, A. M., Connor, S. J., Ashford, R. W. and Thomson, M. C. (2003). Risk mapping of visceral leishmaniasis: the role of local variation in rainfall and altitude on the presence and incidence of kala-azar in eastern Sudan. American Journal of Tropical Medicine and Hygiene 68, 10–17.CrossRefGoogle ScholarPubMed
Gavgani, A. S., Hodjati, M. H., Mohite, H. and Davies, C. R. (2002). Effect of insecticide-impregnated dog collars on incidence of zoonotic visceral leishmaniasis in Iranian children: a matched-cluster randomised trial. Lancet 360, 374–379.CrossRefGoogle ScholarPubMed
Goldstein, H. (1995). Multilevel Statistical Models. Edward Arnold/Halstead, Londres/Nova York.Google Scholar
Gouvea, M. V., Werneck, G. L., Costa, C. H. and de Amorim Carvalho, F. A. (2007). Factors associated to Montenegro skin test positivity in Teresina, Brazil. Acta Tropica 104, 99–107.Google Scholar
Ho, M., Leeuwenburg, J., Mbugua, G., Wamachi, A. and Voller, A. (1983). An enzyme-linked immunosorbent assay (ELISA) for field diagnosis of visceral leishmaniasis. American Journal of Tropical Medicine and Hygiene 32, 943–946.Google Scholar
Hosmer, D. W. Jr. and Lemeshow, S. (1989). Applied Logisitic Regression. John Wiley & Sons, New York, NY.Google Scholar
Karplus, T. M., Jeronimo, S. M., Chang, H., Helms, B. K., Burns, T. L., Murray, J. C., Mitchell, A. A., Pugh, E. W., Braz, R. F., Bezerra, F. L. and Wilson, M. E. (2002). Association between the tumor necrosis factor locus and the clinical outcome of Leishmania chagasi infection. Infection and Immunity 70, 6919–6925.Google Scholar
Maciel, B. L., Lacerda, H. G., Queiroz, J. W., Galvao, J., Pontes, N. N., Dimenstein, R., McGowan, S. E., Pedrosa, L. F. and Jeronimo, S. M. (2008). Association of nutritional status with the response to infection with Leishmania chagasi . American Journal of Tropical Medicine and Hygiene 79, 591–598.Google Scholar
Maia, Z., Viana, V., Muniz, E., Goncalves, L. O., Mendes, C. M., Mehta, S. R. and Badaro, R. (2016). Risk factors associated with Human Visceral Leishmaniasis in an urban area of Bahia, Brazil. Vector Borne and Zoonotic Diseases 16, 368–376.Google Scholar
Margonari, C., Freitas, C. R., Ribeiro, R. C., Moura, A. C., Timbo, M., Gripp, A. H., Pessanha, J. E. and Dias, E. S. (2006). Epidemiology of visceral leishmaniasis through spatial analysis, in Belo Horizonte municipality, state of Minas Gerais, Brazil. Memorias do Instituto Oswaldo Cruz 101, 31–38.Google Scholar
Marzochi, M. C., Marzochi, K. B. and Carvalho, R. W. (1994). Visceral leishmaniasis in Rio de Janeiro. Parasitology Today 10, 37–40.Google Scholar
Moreno, E. C., Melo, M. N., Lambertucci, J. R., Serufo, J. C., Andrade, A. S., Antunes, C. M., Genaro, O. and Carneiro, M. (2006). Diagnosing human asymptomatic visceral leishmaniasis in an urban area of the State of Minas Gerais, using serological and molecular biology techniques. Revista da Sociedade Brasileira de Medicina Tropical 39, 421–427.Google Scholar
Moreno, E. C., Goncalves, A. V., Chaves, A. V., Melo, M. N., Lambertucci, J. R., Andrade, A. S., Negrao-Correa, D., de Figueiredo Antunes, C. M. and Carneiro, M. (2009). Inaccuracy of enzyme-linked immunosorbent assay using soluble and recombinant antigens to detect asymptomatic infection by Leishmania infantum . PLoS Neglected Tropical Diseases 3, e536.CrossRefGoogle ScholarPubMed
Nascimento Mdo, D., Souza, E. C., da Silva, L. M., Leal Pda, C., Cantanhede Kde, L., Bezerra, G. F. and Viana, G. M. (2005). Prevalence of infection by Leishmania chagasi using ELISA (rK39 and CRUDE) and the Montenegro skin test in an endemic leishmaniasis area of Maranhao, Brazil. Cadernos de saude publica 21, 1801–1807.Google Scholar
Oliveira, C. D., Diez-Roux, A., Cesar, C. C. and Proietti, F. A. (2006). A case-control study of microenvironmental risk factors for urban visceral leishmaniasis in a large city in Brazil, 1999–2000. Revista Panamericana de Salud Publica 20, 369–376.CrossRefGoogle Scholar
PBH (2014). Prefeitura Municipal de Belo Horizonte. Informaçoes sobre Leishmaniose Visceral. Available: http://portalpbh.pbh.gov.br/pbh/ecp/comunidade.do?evento=portlet&pIdPlc=ecpTaxonomiaMenuPortal&app=saude&lang=pt_BR&pg=5571&tax=12768. Last Accessed July 2014.Google Scholar
Romero, G. A. and Boelaert, M. (2010). Control of visceral leishmaniasis in latin america-a systematic review. PLoS Neglected Tropical Diseases 4, e584.Google Scholar
Romero, H. D., Silva Lde, A., Silva-Vergara, M. L., Rodrigues, V., Costa, R. T., Guimaraes, S. F., Alecrim, W., Moraes-Souza, H. and Prata, A. (2009). Comparative study of serologic tests for the diagnosis of asymptomatic visceral leishmaniasis in an endemic area. American Journal of Tropical Medicine and Hygiene 81, 27–33.Google Scholar
Saraiva, L., Andrade Filho, J. D., Falcao, A. L., de Carvalho, D. A., de Souza, C. M., Freitas, C. R., Gomes Lopes, C. R., Moreno, E. C. and Melo, M. N. (2011). Phlebotominae fauna (Diptera: Psychodidae) in an urban district of Belo Horizonte, Brazil, endemic for visceral leishmaniasis: characterization of favored locations as determined by spatial analysis. Acta Tropica 117, 137–145.CrossRefGoogle Scholar
Silva, L. A., Romero, H. D., Nogueira Nascentes, G. A., Costa, R. T., Rodrigues, V. and Prata, A. (2011). Antileishmania immunological tests for asymptomatic subjects living in a visceral leishmaniasis-endemic area in Brazil. American Journal of Tropical Medicine and Hygiene 84, 261–266.Google Scholar
Singh, S., Kumari, V. and Singh, N. (2002). Predicting kala-azar disease manifestations in asymptomatic patients with latent Leishmania donovani infection by detection of antibody against recombinant K39 antigen. Clinical and Diagnostic Laboratory Immunology 9, 568–572.Google Scholar
Souza, V. M. M., Julião, F. S., Neves, R. C. S., Magalhães, P. B., Bisinotto, T. V., Lima, A. S., Oliveira, S. S. and Moreira Júnior, E. D. (2008). Ensaio comunitário para avaliação da efetividade de estratégias de prevenção e controle da leishmaniose visceral humana no Município de Feira de Santana, Estado da Bahia, Brasil. Epidemiologia e Serviços de Saúde 17, 97–106.Google Scholar
Supplementary material: PDF

Dos Santos Marques supplementary material

Dos Santos Marques supplementary material 1

Download Dos Santos Marques supplementary material(PDF)
PDF 19.2 KB