A Systematic Review of Toxocariasis: A Neglected But High-Prevalence Disease in Brazil

Paula Mayara Matos Fialho Departamento de SaĂșde Coletiva, Faculdade de CiĂȘncias MĂ©dicas, Universidade Estadual de Campinas, Campinas, SĂŁo Paulo, Brazil

Search for other papers by Paula Mayara Matos Fialho in
Current site
Google Scholar
PubMed
Close
and
Carlos Roberto Silveira CorrĂȘa Departamento de SaĂșde Coletiva, Faculdade de CiĂȘncias MĂ©dicas, Universidade Estadual de Campinas, Campinas, SĂŁo Paulo, Brazil

Search for other papers by Carlos Roberto Silveira CorrĂȘa in
Current site
Google Scholar
PubMed
Close
Restricted access

Toxocariasis is an anthropozoonosis that occurs in all parts of the world. In particular, this disease can often be found in developing countries and in regions, where basic sanitation conditions are poor. However, industrialized countries have reported seroprevalence rates as high as 14.2% in humans. The definitive hosts of the disease are dogs and cats, whereas humans are a paratenic host. To determine the burden of toxocariasis in Brazil, we followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines to conduct a systematic review of the literature. Using keywords and applying the established criteria, we identified 160 publications and selected 22 articles for further analysis. The seroprevalence of toxocariasis in various regions of the country ranged from 4.2% to 65.4%. The highest prevalence was found in the northeast region, although the majority of the studies identified were from the southeast region. The findings suggest the importance of raising awareness among health professionals and public authorities about the fact that toxocariasis is a health problem.

Author Notes

* Address correspondence to Paula Mayara Matos Fialho, Departamento de SaĂșde Coletiva, Faculdade de CiĂȘncias MĂ©dicas, Universidade Estadual de Campinas, Rua TessĂĄlia Vieira de Camargo, 126, Cidade UniversitĂĄria Zeferino Vaz, Campinas, SĂŁo Paulo 13083-887, Brazil. E-mail: paulamayara2@gmail.com
† These authors contributed equally to this work.

Financial support: We thank the Fundação de Amparo à Pesquisa do Estado de São Paulo (grant no. 2012/14134-6) for the PhD scholarship for PMMF.

Authors' addresses: Paula Mayara Matos Fialho and Carlos Roberto Silveira CorrĂȘa, Departamento de SaĂșde Coletiva, Faculdade de CiĂȘncias MĂ©dicas, Universidade Estadual de Campinas, Campinas, SĂŁo Paulo, Brazil, E-mails: paulamayara2@gmail.com and ccorrea@fcm.unicamp.br.

  • 1.

    Andrade LD, 2000. Aspectos clinico-epidemiológicos da toxocaríase humana. Rev Patol Trop 29: 147–159.

  • 2.

    Morimatsu Y, Akao N, Akiyoshi H, Kawazu T, Okabe Y, Aizawa H, 2006. A familial case of visceral larva migrans after ingestion of raw chicken livers: appearance of specific antibody in bronchoalveolar lavage fluid of the patients. Am J Trop Med Hyg 75: 303–306.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Choi D, Lim JH, Choi D-C, Paik SW, Kim S-H, Huh S, 2008. Toxocariasis and ingestion of raw cow liver in patients with eosinophilia. Korean J Parasitol 46: 139–143.

  • 4.

    Rubinsky-Elefant G, Hirata CE, Yamamoto JH, Ferreira MU, 2010. Human toxocariasis: diagnosis, worldwide seroprevalences and clinical expression of the systemic and ocular forms. Ann Trop Med Parasitol 104: 3–23.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Despommier D, 2003. Toxocariasis: clinical aspects, epidemiology, medical ecology, and molecular aspects. Clin Microbiol Rev 16: 265–272.

  • 6.

    Maizels RM, 2009. Exploring the immunology of parasitism—from surface antigens to the hygiene hypothesis. Parasitology 136 (Special Issue 12): 1549–1564.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Lumeng CN, Saltiel AR, 2011. Inflammatory links between obesity and metabolic disease. J Clin Invest 121: 2111–2117.

  • 8.

    Bergmann GG, Bergmann ML de A, Pinheiro E dos S, Moreira RB, Marques AC, Garlipp DC, Gaya DC, 2009. Índice de massa corporal: tendĂȘncia secular em crianças e adolescentes brasileiros. Rev Bras Cineantropometria Desempenho Hum 11: 280–285.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Terres NG, Pinheiro RT, Horta BL, Pinheiro KAT, Horta LL, 2006. PrevalĂȘncia e fatores associados ao sobrepeso e Ă  obesidade em adolescentes. Rev Saude Publica 40: 627–633.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Fialho PMM, CorrĂȘa CRS, 2014. ToxocarĂ­ase, asma e Ă­ndice de massa corporal em crianças e adolescentes em Campinas-SP, 1996 a 1998. Epidemiol E Serviços SaĂșde 23: 361–368.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Medronho RA, 2009. Epidemiologia. SĂŁo Paulo, Brazil: Atheneu.

  • 12.

    Smith H, Holland C, Taylor M, Magnaval J-F, Schantz P, Maizels R, 2009. How common is human toxocariasis? Towards standardizing our knowledge. Trends Parasitol 25: 182–188.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Lescano SZ, Chieffi PP, Amato Neto V, Ikai DK, Ribeiro MCSA, 2005. Anti-helmínticos na toxocaríase experimental: efeito na recuperação de larvas de Toxocara canis e na resposta humoral. J Bras Patol E Med Lab 41: 21–24.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Campos JĂșnior D, Elefant GR, de Melo e Silva EO, Gandolfi L, Jacob CMA, Tofeti A, Pratesi R, 2003. FreqĂŒĂȘncia de soropositividade para antĂ­genos de Toxocara canis em crianças de classes sociais diferentes. Rev Soc Bras Med Trop 36: 509–513.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Alonso JM, Bojanich MVI, Chamorro M, Gorodner JO, 2000. Toxocara seroprevalence in children from a subtropical city in Argentina. Rev Inst Med Trop Sao Paulo 42: 235–237.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Shields JA, 1984. Ocular toxocariasis. A review. Surv Ophthalmol 28: 361–381.

  • 17.

    Ajayi O, Duhlinska D, Agwale S, Njoku M, 2000. Frequency of human toxocariasis in Jos, Plateau State, Nigeria. Mem Inst Oswaldo Cruz 95: 147–149.

  • 18.

    Gueglio B, de Gentile L, Nguyen JM, Achard J, Chabasse D, Marjolet M, 1994. Epidemiologic approach to human toxocariasis in western France. Parasitol Res 80: 531–536.

  • 19.

    Lynch N, Hagel I, Vargas V, Rotundo A, Varela M, Di Prisco M, Hodgen AN, 1993. Comparable seropositivity for ascariasis and toxocariasis in tropical slum children. Parasitol Res 79: 547–550.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Baboolal S, Rawlins SC, 2002. Seroprevalence of toxocariasis in schoolchildren in Trinidad. Trans R Soc Trop Med Hyg 96: 139–143.

  • 21.

    Lee RM, Moore LB, Bottazzi ME, Hotez PJ, 2014. Toxocariasis in North America: a systematic review. PLoS Negl Trop Dis 8: e3116.

  • 22.

    Hotez PJ, 2008. Neglected infections of poverty in the United States of America. PLoS Negl Trop Dis 2: e256.

  • 23.

    Parise ME, Hotez PJ, Slutsker L, 2014. Neglected parasitic infections in the United States: needs and opportunities. Am J Trop Med Hyg 90: 783–785.

  • 24.

    Marchioro AA, Colli CM, Ferreira ÉC, Viol BM, AraĂșjo SM, Falavigna-Guilherme AL, 2014. Risk factors associated with toxoplasmosis and toxocariasis in populations of children from nine cities in southern Brazil. J Helminthol 89: 428–432.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Cassenote AJF, de Abreu Lima AR, Pinto Neto JM, Rubinsky-Elefant G, 2014. Seroprevalence and modifiable risk factors for Toxocara spp. in Brazilian schoolchildren. PLoS Negl Trop Dis 8: e2830.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Negri EC, SantarĂ©m VA, Rubinsky-Elefant G, Giuffrida R, 2013. Anti-Toxocara spp. antibodies in an adult healthy population: serosurvey and risk factors in Southeast Brazil. Asian Pac J Trop Biomed 3: 211–216.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Guilherme EV, Marchioro AA, Araujo SM, Falavigna DL, Adami C, Falavigna-Guilherme G, Rubinsky-Elefant G, Falavigna-Guilherme AL, 2013. Toxocariasis in children attending a Public Health Service Pneumology Unit in Paraná State, Brazil. Rev Inst Med Trop Sao Paulo 55: 189–192.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Schoenardie ER, Scaini CJ, Brod CS, Pepe MS, Villela MM, McBride AJA, Borsuk S, Berne MEA, 2013. Seroprevalence of Toxocara infection in children from southern Brazil. J Parasitol 99: 537–539.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Prestes-Carneiro LE, Rubinsky-Elefant G, Ferreira AW, Araujo PR, Troiani C, Zago SC, Kaiahara M, Sasso L, Iha A, Vaz A, 2013. Seroprevalence of toxoplasmosis, toxocariasis and cysticercosis in a rural settlement, São Paulo State, Brazil. Pathog Glob Health 107: 88–95.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Manini MP, Marchioro AA, Colli CM, Nishi L, Falavigna-Guilherme AL, 2012. Association between contamination of public squares and seropositivity for Toxocara spp. in children. Vet Parasitol 188: 48–52.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Mattia S, Colli CM, Adami CM, Guilherme GF, Nishi L, Rubinsky-Elefant G, Marchioro AA, Gomes ML, Falavigna-Guilherme AL, 2012. Seroprevalence of Toxocara infection in children and environmental contamination of urban areas in Paraná State, Brazil. J Helminthol 86: 440–445.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Fragoso RP, Monteiro MBM, Lemos EM, Pereira FEL, 2011. Anti-Toxocara antibodies detected in children attending elementary school in Vitoria, State of Espírito Santo, Brazil: prevalence and associated factors. Rev Soc Bras Med Trop 44: 461–466.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Marchioro AA, Colli CM, Mattia S, Paludo ML, de Melo GC, Adami CM, Pelloso SM, Guilherme ALF, 2011. Avaliação eosinofĂ­lica e soropositividade para anticorpos IgG anti-Toxocara em crianças atendidas pelo Sistema Único de SaĂșde. Rev Paul Pediatr 29: 80–84.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    SantarĂ©m VA, Leli FNC, Rubinsky-Elefant G, Giuffrida R, 2011. Protective and risk factors for toxocariasis in children from two different social classes of Brazil. Rev Inst Med Trop Sao Paulo 53: 66–72.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Correa CRS, Bismarck CM, 2010. Toxocariasis: incidence, prevalence and the time serum remains positive in school children from Campinas, SP, Brazil. J Trop Pedriatrics 56: 215–216.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Colli CM, Rubinsky-Elefant G, Paludo ML, Falavigna DLM, Guilherme EV, Mattia S, Araujo SM, Ferreira É, Previdelli ITS, Falavigna-Guilherme AL, 2010. Serological, clinical and epidemiological evaluation of toxocariasis in urban areas of south Brazil. Rev Inst Med Trop Sao Paulo 52: 69–74.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Prestes-Carneiro LE, Souza DHP, Moreno GC, Troiani C, SantarĂ©m V, Zago SCS, Miguel NA, Freitas SBZ, Faria R, Martini L, Rubinsky-Elefant G, Iha A, Vaz AJ, 2009. Toxocariasis/cysticercosis seroprevalence in a long-term rural settlement, SĂŁo Paulo, Brazil. Parasitology 136: 681–689.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Prestes-Carneiro LE, SantarĂ©m V, Zago SCS, Miguel NA, Zambelli S de F, Villas R, Vaz AJ, Rubinsky-Elefant G, 2008. Sero-epidemiology of toxocariasis in a rural settlement in SĂŁo Paulo state, Brazil. Ann Trop Med Parasitol 102: 347–356.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Mendonça LR, Figueiredo CA, Esquivel R, Fiaccone RL, Pontes-de-Carvalho L, Cooper P, Barreto ML, Alcantara-Neves NM, 2013. Seroprevalence and risk factors for Toxocara infection in children from an urban large setting in northeast Brazil. Acta Trop 128: 90–95.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    Mendonça LR, Veiga RV, Dattoli VCC, Figueiredo CA, Fiaccone R, Santos J, Cruz ÁA, Rodrigues LC, Cooper PJ, Pontes-de-Carvalho LC, Barreto ML, Alcantara-Neves NM, 2012. Toxocara seropositivity, atopy and wheezing in children living in poor neighbourhoods in urban Latin American. PLoS Negl Trop Dis 6: e1886.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Souza RF, Dattoli VCC, Mendonça LR, Jesus JR, Baqueiro T, Santana C de C, Santos NM, Barrouin-Melo SM, Alcantara-Neves NM, 2011. PrevalĂȘncia e fatores de risco da infecção humana por Toxocara canis em Salvador, Estado da Bahia. Rev Soc Bras Med Trop 44: 516–519.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Dattoli VCC, Freire SM, Mendonça LR, Santos PC, Meyer R, Alcantara-Neves NM, 2011. Toxocara canis infection is associated with eosinophilia and total IgE in blood donors from a large Brazilian centre. Trop Med Int Health 16: 514–517.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Oliart-GuzmĂĄn H, Delfino BM, Martins AC, Mantovani SAS, Braña AM, Pereira TM, Branco FLCC, Ramalho AA, Campos RG, Fontoura PS, de Araujo TS, de Oliveira CSM, Muniz PT, Rubinsky-Elefant G, Codeço CT, da Silva-Nunes M, 2014. Epidemiology and control of child toxocariasis in the western Brazilian Amazon—a population-based study. Am J Trop Med Hyg 90: 670–681.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44.

    Rubinsky-Elefant G, da Silva-Nunes M, Malafronte RS, Muniz PT, Ferreira MU, 2008. Human toxocariasis in rural Brazilian Amazonia: seroprevalence, risk factors, and spatial distribution. Am J Trop Med Hyg 79: 93–98.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45.

    NĂșñez CR, MartĂ­nez GDM, Arteaga SY, Macotela MP, Montes PB, DurĂĄn NR, 2013. Prevalence and risk factors associated with Toxocara canis infection in children. Scientific World J 2013: 572089.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46.

    Kim Y-H, Huh S, Chung Y-B, 2008. Seroprevalence of toxocariasis among healthy people with eosinophilia. Korean J Parasitol 46: 29–32.

  • 47.

    RoldĂĄn WH, Espinoza YA, AtĂșncar A, Ortega E, Martinez A, Saravia M, 2008. Frequency of eosinophilia and risk factors and their association with Toxocara infection in schoolchildren during a health survey in the north of Lima, Peru. Rev Inst Med Trop Sao Paulo 50: 273–278.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48.

    Paludo ML, Falavigna DLM, Elefant GR, Gomes ML, Baggio MLM, Amadei LB, Falavigna-Guilherme AL, 2007. Frequency of Toxocara infection in children attended by the health public service of Maringá, south Brazil. Rev Inst Med Trop Sao Paulo 49: 343–348.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 49.

    Figueiredo SDP, Taddei JAAC, Menezes JJC, Novo NF, Silva EOM, Cristóvão HLG, Cury MCFS, 2005. Estudo clínico-epidemiológico da toxocaríase em população infantil. J Pediatr (Rio J) 81: 126–132.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 50.

    Jacob CMA, Pastorino AC, Peres BA, Mello EO, Okay Y, Oselka GW, 1994. Clinical and laboratorial features of visceral toxocariasis in infancy. Rev Inst Med Trop Sao Paulo 36: 19–26.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 51.

    Woodhall DM, Eberhard ML, Parise ME, 2014. Neglected parasitic infections in the United States: toxocariasis. Am J Trop Med Hyg 90: 810–813.

  • 52.

    Won KY, Kruszon-Moran D, Schantz PM, Jones JL, 2008. National seroprevalence and risk factors for zoonotic Toxocara spp. infection. Am J Trop Med Hyg 79: 552–557.

Past two years Past Year Past 30 Days
Abstract Views 741 658 83
Full Text Views 581 87 0
PDF Downloads 225 16 0
 
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save