Socioeconomic Factors Associated with Fasciola hepatica Infection Among Children from 26 Communities of the Cusco Region of Peru

Miguel M. Cabada Infectious Diseases Division, Department of Internal Medicine, University of Texas Medical Branch, Galveston, Texas;
Alexander von Humboldt Tropical Medicine Institute, Department of Medicine, Universidad Peruana Cayetano Heredia, Cusco Branch, Peru;

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Maria Luisa Morales Alexander von Humboldt Tropical Medicine Institute, Department of Medicine, Universidad Peruana Cayetano Heredia, Cusco Branch, Peru;

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Camille M. Webb Infectious Diseases Division, Department of Internal Medicine, University of Texas Medical Branch, Galveston, Texas;

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Logan Yang School of Medicine, University of Texas Medical Branch, Galveston, Texas;

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Chelsey A. Bravenec School of Medicine, University of Texas Medical Branch, Galveston, Texas;

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Martha Lopez Alexander von Humboldt Tropical Medicine Institute, Department of Medicine, Universidad Peruana Cayetano Heredia, Cusco Branch, Peru;

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Ruben Bascope Zoonosis Unit, Direccion Regional de Salud del Cusco, Ministerio de Salud, Cusco, Peru

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A. Clinton White Jr. Infectious Diseases Division, Department of Internal Medicine, University of Texas Medical Branch, Galveston, Texas;

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Eduardo Gotuzzo Alexander von Humboldt Tropical Medicine Institute, Department of Medicine, Universidad Peruana Cayetano Heredia, Cusco Branch, Peru;

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Fasciola hepatica is the most widely distributed trematode-affecting humans. The Andes Mountains are highly endemic for fascioliasis. We report results of a cross-sectional study evaluating the epidemiology of Fasciola among children in 26 agricultural communities in the Cusco region of Peru. Children 3 to 16 years old were enrolled in preschools and schools. Blood from participants was tested for complete blood counts, transaminases, and Fasciola antibodies. Stool samples were tested for Fasciola and other parasites. A total of 2,515 children were included in the analysis and the mean age was 9.6 years (±3.6). Ten percent (253) of the children had at least one positive test for Fasciola, 6% had chronic infection, and 0.4% acute infection. The rest of the subjects had only antibodies against Fasciola. The prevalence of infection varied from 0% to 20% between communities. Children with evidence of Fasciola exposure were older, lived at higher altitudes, and had a lower socioeconomic status than children without infection. The logistic regression analysis showed that children from Ancahuasi district, older children, and children with higher measures of poverty were more likely to have Fasciola exposure. Fascioliasis is common in the Cusco region and associated with poverty. However, the distribution varies markedly between communities.

Author Notes

Address correspondence to Miguel M. Cabada, Infectious Diseases Division, Department of Internal Medicine, University of Texas Medical Branch, 301 University Bvd., Route 0435, Galveston, TX 77555. E-mail: micabada@utmb.edu

Financial support: This work was supported by the National Institute for Allergy and Infectious Diseases at the National Institutes of Health (grant number 1R01AI104820–01).

Authors’ addresses: Miguel M. Cabada, Infectious Diseases Division, Department of Internal Medicine, University of Texas Medical Branch, Galveston, TX, and Alexander von Humboldt Tropical Medicine Institute, Department of Medicine, Universidad Peruana Cayetano Heredia, Cusco Branch, Peru, E-mail: micabada@utmb.edu. Maria Luisa Morales, Martha Lopez, and Eduardo Gotuzzo, Department of Medicine, Alexander von Humboldt Tropical Medicine Institute, Universidad Peruana Cayetano Heredia, Cusco, Peru, E-mails: malu.morales.fernadez@gmail.com, martlop2000@gmail.com, and eduardo.gotuzzo@upch.pe. Camille M. Webb and A. Clinton White, Jr., Infectious Diseases Division, Department of Internal Medicine, University of Texas Medical Branch, Galveston, TX, E-mails: cmwebbca@utmb.edu and acwhite@utmb.edu. Logan Yang and Chelsey A. Bravenec, School of Medicine, University of Texas Medical Branch, Galveston, TX, E-mails: lryang@utmb.edu and cabraven@utmb.edu. Ruben Bascope, Programa de Control de Enfermedades Zoonoticas, Direccion Regional de Salud Cusco, Cusco, Peru, E-mail: bascopeq@gmail.com.

  • 1.

    WHO, 2017. Foodborne Trematode Infections: Fascioliasis. Geneva, Switzerland: World Health Organization.

    • PubMed
    • Export Citation
  • 2.

    Moazeni M, Ahmadi A, 2016. Controversial aspects of the life cycle of Fasciola hepatica. Exp Parasitol 169: 8189.

  • 3.

    Cabada MM, White AC Jr., 2012. New developments in epidemiology, diagnosis, and treatment of fascioliasis. Curr Opin Infect Dis 25: 518522.

  • 4.

    Lopez M, White AC Jr., Cabada MM, 2012. Burden of Fasciola hepatica infection among children from Paucartambo in Cusco, Peru. Am J Trop Med Hyg 86: 481485.

  • 5.

    Karahocagil MK, Akdeniz H, Sunnetcioglu M, Cicek M, Mete R, Akman N, Ceylan E, Karsen H, Yapici K, 2011. A familial outbreak of fascioliasis in eastern Anatolia: a report with review of literature. Acta Trop 118: 177183.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    McDaniel CJ, Cardwell DM, Moeller RB Jr., Gray GC, 2014. Humans and cattle: a review of bovine zoonoses. Vector Borne Zoonotic Dis 14: 119.

  • 7.

    Ashrafi K, Bargues MD, O’Neill S, Mas-Coma S, 2014. Fascioliasis: a worldwide parasitic disease of importance in travel medicine. Travel Med Infect Dis 12 (6 Pt A): 636649.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Furst T, Keiser J, Utzinger J, 2012. Global burden of human food-borne trematodiasis: a systematic review and meta-analysis. Lancet Infect Dis 12: 210221.

  • 9.

    Esteban JG, Flores A, Angles R, Mas-Coma S, 1999. High endemicity of human fascioliasis between Lake Titicaca and La Paz valley, Bolivia. Trans R Soc Trop Med Hyg 93: 151156.

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

    González LC, Esteban JG, Bargues MD, Valero MA, Ortiz P, Náquira C, Mas-Coma S, 2011. Hyperendemic human fascioliasis in Andean valleys: an altitudinal transect analysis in children of Cajamarca province, Peru. Acta Trop 120: 119129.

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

    Esteban JG, González C, Bargues MD, Angles R, Sánchez C, Náquira C, Mas-Coma S, 2002. High fascioliasis infection in children linked to a man-made irrigation zone in Peru. Trop Med Int Health 7: 339348.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    El-Sahn F, Farghaly A, El-Masry A, Mandil A, Gad A, El-Morshedy H, 1995. Human fascioliasis in an Egyptian village: prevalence and some epidemiological determinants. J Egypt Public Health Assoc 70: 541557.

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

    Cabada MM, Goodrich MR, Graham B, Villanueva-Meyer PG, Lopez M, Argue E, White AC Jr, 2014. Fascioliasis and eosinophilia in the highlands of Cuzco, Peru and their association with water and socioeconomic factors. Am J Trop Med Hyg 91: 989993.

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

    Parkinson M, O’Neill SM, Dalton JP, 2007. Endemic human fasciolosis in the Bolivian Altiplano. Epidemiol Infect 135: 669674.

  • 15.

    MEF, 2007. Tasa de Analfabetismo Segun Departamento, Provincial, y Distrito 2007. Available at: http://www.mef.gob.pe/contenidos/estadisticas/pol_econ/cuadro60.xls. Accessed July 10, 2018.

    • PubMed
    • Export Citation
  • 16.

    INEI, 2013. Mapa de Pobreza Provincial y Distrital 2013 Instituto Nacional de Estadistica e Informatica, Lima, Peru. Available at: https://www.inei.gob.pe/media/MenuRecursivo/publicaciones_digitales/Est/Lib1261/Libro.pdf. Accessed July 10, 2018.

    • PubMed
    • Export Citation
  • 17.

    DIRESA-Cusco, 2016. Boletin Estadistico Año 1 Número 1, 2016 Dirección Regional de Salud del Cusco, Cusco, Peru. Available at: http://www.diresacusco.gob.pe/estaditica/monitoreo/Boletin%20estadistico2015.pdf. Accessed July 10, 2018.

    • PubMed
    • Export Citation
  • 18.

    Schreiner M, 2012. A Simple Poverty Scorecard for Peru. Available at: http://microfinance.com/English/Papers/Scoring_Poverty_Peru_2010_EN.pdf. Accessed July 10, 2018.

    • PubMed
    • Export Citation
  • 19.

    Mas-Coma MS, Esteban JG, Bargues MD, 1999. Epidemiology of human fascioliasis: a review and proposed new classification. Bull World Health Organ 77: 340346.

  • 20.

    Mas-Coma S, Anglés R, Esteban JG, Bargues MD, Buchon P, Franken M, Strauss W, 1999. The northern Bolivian Altiplano: a region highly endemic for human fascioliasis. Trop Med Int Health 4: 454467.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Heydarian P, Ashrafi K, Mohebali M, Kia EB, Aryaeipour M, Chegeni Sharafi A, Mokhayeri H, Bozorgomid A, Rokni MB, 2017. Seroprevalence of human fasciolosis in Lorestan Province, western Iran, in 2015–16. Iran J Parasitol 12: 389397.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Mas-Coma S, Funatsu IR, Bargues MD, 2001. Fasciola hepatica and lymnaeid snails occurring at very high altitude in South America. Parasitology 123 (Suppl): S115S127.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Vignoles P, Favennec L, Dreyfuss G, Rondelaud D, 2002. Highland populations of Lymnaea truncatula infected with Fasciola hepatica survive longer under experimental conditions than lowland ones. Parasitol Res 88: 386388.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Nematian J, Nematian E, Gholamrezanezhad A, Asgari AA, 2004. Prevalence of intestinal parasitic infections and their relation with socio-economic factors and hygienic habits in Tehran primary school students. Acta Trop 92: 179186.

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

    Quihui L, Valencia ME, Crompton DWT, Phillips S, Hagan P, Morales G, Díaz-Camacho SP, 2006. Role of the employment status and education of mothers in the prevalence of intestinal parasitic infections in Mexican rural schoolchildren. BMC Public Health 6: 225.

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

    Yentur Doni N, Gurses G, Simsek Z, Yildiz Zeyrek F, 2015. Prevalence and associated risk factors of intestinal parasites among children of farm workers in the southeastern Anatolian region of Turkey. Ann Agric Environ Med 22: 438442.

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

    Ngui R, Ishak S, Chuen CS, Mahmud R, Lim YA, 2011. Prevalence and risk factors of intestinal parasitism in rural and remote west Malaysia. PLoS Negl Trop Dis 5: e974.

  • 28.

    El-Shazly AM, El-Nahas HA, Abdel-Mageed AA, El Beshbishi SN, Azab MS, Abou El Hasan M, Arafa WA, Morsy TA, 2005. Human fascioliasis and anaemia in Dakahlia Governorate, Egypt. J Egypt Soc Parasitol 35: 421432.

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

    Shang Y, Tang LH, Zhou SS, Chen YD, Yang YC, Lin SX, 2010. Stunting and soil-transmitted-helminth infections among school-age pupils in rural areas of southern China. Parasit Vectors 3: 97.

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

    Human Development Reports United Nations Development Programme, 2018. Available at: http://hdr.undp.org/en/countries/profiles/PER. Accessed July 10, 2018.

    • PubMed
    • Export Citation
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