Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-22T22:56:22.191Z Has data issue: false hasContentIssue false
  • English
  • Français

Epidemiology of soil-transmitted helminthiases-related mortality in Brazil

Published online by Cambridge University Press:  20 January 2017

FRANCISCO R. MARTINS-MELO ,
ALBERTO N. RAMOS JR ,
CARLOS H. ALENCAR ,
MAURICÉLIA S. LIMA  and
JORG HEUKELBACH
FRANCISCO R. MARTINS-MELO*
Affiliation:
Department of Community Health, School of Medicine, Federal University of Ceará, Fortaleza, Brazil Federal Institute of Education, Science and Technology of Ceará, Caucaia, Brazil
ALBERTO N. RAMOS JR
Affiliation:
Department of Community Health, School of Medicine, Federal University of Ceará, Fortaleza, Brazil
CARLOS H. ALENCAR
Affiliation:
Department of Community Health, School of Medicine, Federal University of Ceará, Fortaleza, Brazil
MAURICÉLIA S. LIMA
Affiliation:
Department of Community Health, School of Medicine, Federal University of Ceará, Fortaleza, Brazil São José Hospital for Infectious Diseases, Fortaleza, Brazil
JORG HEUKELBACH
Affiliation:
Department of Community Health, School of Medicine, Federal University of Ceará, Fortaleza, Brazil College of Public Health, Medical and Veterinary Sciences, Division of Tropical Health and Medicine, James Cook University, Townsville, Queensland, Australia
*
*Corresponding author: Federal Institute of Education, Science and Technology of Ceará, Rua Francisco da Rocha Martins, s/n, Pabussu, CEP 61609-090, Caucaia, Ceará, Brazil. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Soil-transmitted helminth (STH) infections are widely distributed in tropical and subtropical areas, including Brazil. We performed a nationwide population-based study including all deaths in Brazil from 2000 to 2011, in which STHs (ascariasis, trichuriasis and/or hookworm infection) were mentioned on death certificates, either as underlying or as associated causes of death. Epidemiological characteristics, time trends and spatial analysis of STH-related mortality were analysed. STHs was identified on 853/12 491 280 death certificates: 827 (97·0%) deaths related to ascariasis, 25 (2·9%) to hookworm infections, and 1 (0·1%) to trichuriasis. The average annual age-adjusted mortality rate was 0·34/1 000 000 inhabitants (95% confidence interval: 0·27–0·44). Females, children <10 years of age, indigenous ethnic groups and residents in the Northeast region had highest STH-related mortality rates. Nationwide mortality decreased significantly over time (annual percent change: −5·7%; 95% CI: −6·9 to −4·4), with regional differences. We identified spatial high-risk clusters for STH-related mortality mainly in the North, Northeast and South regions. Diseases of the digestive system and infectious/parasitic diseases were the most commonly associated causes of death mentioned in the STH-related deaths. Despite decreasing mortality in Brazil, a considerable number of deaths is caused by STHs, with ascariasis responsible for the vast majority. There were marked regional differences, affecting mainly children and vulnerable populations.

Keywords

soil-transmitted helminthiasisneglected tropical diseasesmortalityspatial analysistime trend analysisBrazil
Type
Research Article
Information
Parasitology , Volume 144 , Issue 5 , April 2017 , pp. 669 - 679
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

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

Andrade, E. C., Leite, I. C. G., Vieira, M. T., Abramo, C., Tibiriçá, S. H. C. and Silva, P. L. (2011). Prevalence of parasitic intestinal diseases in a quilombola community, in the Municipality of Bias Fortes, State of Minas Gerais, Brazil, 2008. Epidemiologia e Serviços de Saúde 20, 337–344.CrossRefGoogle Scholar
Anselin, L. (1995). Local indicators of spatial association–LISA. Geographical Analysis 27, 93–115.CrossRefGoogle Scholar
Assunção, R. M., Barreto, S. M., Guerra, H. L. and Sakurai, E. (1998). Maps of epidemiological rates: a Bayesian approach. Cadernos de Saúde Pública 14, 713–723.Google Scholar
Bethony, J., Brooker, S., Albonico, S. M., Geiger, M., Loukas, A., Diemert, D. and Hotez, P. J. (2006). Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. The Lancet 367, 1521–1532.Google Scholar
Bisanzio, D., Mutuku, F., Bustinduy, A. L., Mungai, P. L., Muchiri, E. M., King, C. H. and Kitron, U. (2014). Cross-sectional study of the burden of vector-borne and soil-transmitted polyparasitism in rural communities of Coast Province, Kenya. PLoS Neglected Tropical Diseases 8, e2992.Google Scholar
Brazilian Ministry of Health (2012). Integrated Strategic Action Plan for the Elimination of Leprosy, Filariasis, Schistosomiasis and Onchocerciasis as a Public Health Problem, Trachoma as a Cause of Blindness and Control of Geohelmintiases: Action Plan 2011–2015. Brazilian Ministry of Health, Brasília, Brazil. http://bvsms.saude.gov.br/bvs/publicacoes/plano_integrado_acoes_estrategicas_2011_2015.pdf Google Scholar
Brazilian Ministry of Health (2016). Informe Técnico – Campanha Nacional de Hanseníase, Verminoses, Tracoma e Esquistossomose 2016. Brazilian Ministry of Health, Brasília, Brazil.Google Scholar
Chammartin, F., Scholte, R. G., Guimarães, L. H., Tanner, M., Utzinger, J. and Vounatsou, P. (2013). Soil-transmitted helminth infection in South America: a systematic review and geostatistical meta-analysis. The Lancet Infectious Diseases 13, 507–518.Google Scholar
Chammartin, F., Guimarães, L. H., Scholte, R. G., Bavia, M. E., Utzinger, J. and Vounatsou, P. (2014). Spatio-temporal distribution of soil-transmitted helminth infections in Brazil. Parasites & Vectors 18, 440.Google Scholar
Cliff, A. D. and Ord, J. K. (1981). Spatial Processes: Models & Applications. Pion Ltd, London, UK.Google Scholar
Couto, L. D., Tibiriça, S. H., Pinheiro, I. O., Mitterofhe, A., Lima, A. C., Castro, M. F., Gonçalves, M., Silva, M. R., Guimarães, R. J., Rosa, F. M. and Coimbra, E. S. (2014). Neglected tropical diseases: prevalence and risk factors for schistosomiasis and soil-transmitted helminthiasis in a region of Minas Gerais State, Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 108, 363–371.Google Scholar
Ferreira, M. U., Ferreira, C. S. and Monteiro, C. A. (2000). Secular trends in child intestinal parasitic diseases in S. Paulo city, Brazil (1984–1996). Revista de Saúde Pública 34, 73–82.Google Scholar
Fonseca, E. O. L., Teixeira, M. G., Barreto, M. L., Carmo, E. H. and Costa, M. C. N. (2010). Prevalence and factors associated with geohelminth infections in children living in municipalities with low HDI in North and Northeast Brazil. Cadernos de Saúde Pública 26, 143–152.Google Scholar
Hotez, P. J., Brindley, P. J., Bethony, J. M., King, C. H., Pearce, E. J. and Jacobson, J. (2008). Helminth infections: the great neglected tropical diseases. Journal of Clinical Investigation 118, 1311–1321.Google Scholar
Hotez, P. J., Alvarado, M., Basáñez, M. G., Bolliger, I., Bourne, R., Boussinesq, M., Brooker, S. J., Brown, A. S., Buckle, G. and Budke, C. M. (2014). The global burden of disease study 2010: interpretation and implications for the neglected tropical diseases. PLoS Neglected Tropical Diseases 8, e2865.Google Scholar
Hurtado-Guerrero, A. F., Alencar, F. H. and Hurtado-Guerrero, J. C. (2005). Occurrence of enteroparasites in the elderly population of Nova Olinda do Norte, Amazonas, Brazil. Acta Amazonica 35, 487–490.CrossRefGoogle Scholar
Kim, H. J., Fay, M. P., Feuer, E. J. and Midthune, D. N. (2000). Permutation tests for joinpoint regression with applications to cancer rates. Statistics in Medicine 19, 335–351.3.0.CO;2-Z>CrossRefGoogle ScholarPubMed
Mandarino-Pereira, A., Souza, F. S., Lopes, C. W. G. and Pereira, M. J. S. (2010). Prevalence of parasites in soil and dog feces according to diagnostic tests. Veterinary Parasitology 170, 176–181.Google Scholar
Martins-Melo, F. R., Alencar, C. H., Ramos, A. N. Jr. and Heukelbach, J. (2012 a). Epidemiology of mortality related to Chagas’ disease in Brazil, 1999–2007. PLoS Neglected Tropical Diseases 6, e1508.CrossRefGoogle ScholarPubMed
Martins-Melo, F. R., Ramos, A. N. Jr., Alencar, C. H., Lange, W. and Heukelbach, J. (2012 b). Mortality of Chagas’ disease in Brazil: spatial patterns and definition of high-risk areas. Tropical Medicine & International Health 17, 1066–1075.Google Scholar
Martins-Melo, F. R., Ramos, A. N. Jr., Alencar, C. H. and Heukelbach, J. (2012 c). Multiple causes of death related to Chagas’ disease in Brazil, 1999 to 2007. Revista da Sociedade Brasileira de Medicina Tropical 45, 591–596.Google Scholar
Martins-Melo, F. R., Pinheiro, M. C. C., Ramos, A. N. Jr., Alencar, C. H., de Moraes Bezerra, F. S. M. and Heukelbach, J. (2015). Spatiotemporal patterns of schistosomiasis-related deaths, Brazil, 2000–2011. Emerging Infectious Diseases 21, 1820–1824.Google Scholar
Martins-Melo, F. R., Ramos, A. N. Jr., Alencar, C. H. and Heukelbach, J. (2016 a). Mortality from neglected tropical diseases in Brazil, 2000–2011. Bulletin of the World Health Organization 94, 103–110.Google Scholar
Martins-Melo, F. R., Ramos, A. N. Jr., Alencar, C. H. and Heukelbach, J. (2016 b). Trends and spatial patterns of mortality related to neglected tropical diseases in Brazil. Parasite Epidemiology and Control 1, 56–65.Google Scholar
Martins-Melo, F. R., Ramos, A. N. Jr., Cavalcanti, M. G., Alencar, C. H., and Heukelbach, J. (2016 c). Neurocysticercosis-related mortality in Brazil, 2000–2011: epidemiology of a neglected neurologic cause of death. Acta Tropica 153, 128–136.Google Scholar
Miranda, R. A., Xavier, F. B. and Menezes, R. C. (1998). Intestinal parasitism in a Parakanã indigenous community in southwestern Pará State, Brazil. Cadernos de Saúde Pública 14, 507–511.Google Scholar
Miranda, R. A., Xavier, F. B., Nascimento, J. R. L. and Menezes, R. C. (1999). Prevalence of intestinal parasitism in Tembé tribe indian settlements, Brazilian Eastern Amazon. Revista da Sociedade Brasileira de Medicina Tropical 32, 389–393.Google Scholar
Naing, C., Whittaker, M. A., Nyunt-Wai, V., Reid, S. A., Wong, S. F., Mak, J. W. and Tanner, M. (2013). Malaria and soil-transmitted intestinal helminth co-infection and its effect on anemia: a meta-analysis. Transactions of the Royal Society of Tropical Medicine and Hygiene 107, 672–683.Google Scholar
Prado, M. S., Barreto, M. L., Strina, A., Faria, J. A. S., Nobre, A. A. and Jesus, S. R. (2001). Prevalence and intensity of infection by intestinal parasites in school-aged children in the City of Salvador (Bahia State, Brazil). Revista da Sociedade Brasileira de Medicina Tropical 34, 99–101.Google Scholar
Pullan, R. L., Smith, J. L., Jasrasaria, R. and Brooker, S. J. (2014). Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasites & Vectors 7, 37.Google Scholar
Santo, A. H. (2007). Cysticercosis-related mortality in the State of São Paulo, Brazil, 1985–2004: a study using multiple causes of death. Cadernos de Saúde Pública 23, 2917–2927.Google Scholar
Scholte, R. G., Schur, N., Bavia, M. E., Carvalho, E. M., Chammartin, F., Utzinger, J. and Vounatsou, P. (2013). Spatial analysis and risk mapping of soil-transmitted helminth infections in Brazil, using Bayesian geostatistical models. Geospatial Health 8, 97–110.CrossRefGoogle ScholarPubMed
Scolari, C., Torti, C., Beltrame, A., Matteelli, A., Castelli, F., Gulletta, M., Ribas, M., Morana, S. and Urbani, C. (2000). Prevalence and distribution of soil-transmitted helminth (STH) infections in urban and indigenous schoolchildren in Ortigueira, State of Paraná, Brazil: implications for control. Tropical Medicine & International Health 5, 302–307.Google Scholar
Silva, N., Chan, M. and Bundy, D. (1997). Morbidity and mortality due to ascariasis: re-estimation and sensitivity analysis of global numbers at risk. Tropical Medicine & International Health 2, 513–518.Google Scholar
Silva, A. M. B., Bouth, R. C., Costa, K. S., Carvalho, D. C., Hirai, K. E., Prado, R. R., Araújo, S. G., Pereira, A. C. L. and Ribeiro, K. T. S. (2014). Occurrence of intestinal parasites in riverine communities in the City of Igarapé Miri, Pará State, Brazil. Revista Pan-Amazônica de Saúde 5, 45–51.CrossRefGoogle Scholar
Visser, S., Giatti, L. L., Carvalho, R. A. C. and Guerreiro, J. C. H. (2011). Study of the association between socio-environmental factors and the prevalence of intestinal parasitosis in the suburbs of the city of Manaus in the state of Amazonas, Brazil. Ciência & Saúde Coletiva 16, 3481–3492.CrossRefGoogle ScholarPubMed
Vos, T., Barber, R. M., Bell, B., Bertozzi-Villa, A., Biryukov, S., Bolliger, I., Charlson, F., Davis, A., Degenhardt, L., Dicker, D., Duan, L., Erskine, H., Feigin, V. L., Ferrari, A. J., Fitzmaurice, C., Fleming, T., Graetz, N., Guinovart, C., Haagsma, J., Hansen, G. M., Hanson, S. W., Heuton, K. R., Higashi, H., Kassebaum, N., Kyu, H., Laurie, E., Liang, X., Lofgren, K., Lozano, R. and MacIntyre, M. F. et al. (2016). Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015. The Lancet 388, 1545–1602.Google Scholar
World Health Organization (2012). Soil-Transmitted Helminthiases. Eliminating Soil-Transmitted Helminthiases as a Public Health Problem in Children: Progress Report 2001–2010 and Strategic Plan 2011–2020. World Health Organization, Geneva, Switzerland.Google Scholar
World Health Organization (2014). Statistical Classification of Diseases and Related Health Problems (ICD), 10th Revision. World Health Organization, Geneva, Switzerland. http://apps.who.int/classifications/icd10/browse/2010/en Google Scholar
World Health Organization (2016 a). Soil-transmitted Helminth Infections – Fact Sheet. World Health Organization, Geneva, Switzerland. http://www.who.int/mediacentre/factsheets/fs366/en/ Google Scholar
World Health Organization (2016 b). PCT databank – Soil-Transmitted Helminthiases. World Health Organization, Geneva, Switzerland. http://www.who.int/neglected_diseases/preventive_chemotherapy/sth/en/ Google Scholar
Supplementary material: File

Martins-Melo supplementary material

Tables S1-S3

Download Martins-Melo supplementary material(File)
File 131.1 KB