Thompson RC, 2015. Neglected zoonotic helminths: Hymenolepis nana, Echinococcus canadensis and Ancylostoma ceylanicum. Clin Microbiol Infect 21: 426–432.
Al-Mekhlafi HM, 2020. The neglected cestode infection: Epidemiology of Hymenolepis nana infection among children in rural Yemen. Helminthologia 57: 293–305.
Cabada MM, Morales ML, Lopez M, Reynolds ST, Vilchez EC, Lescano AG, Gotuzzo E, Garcia HH, White AC Jr., 2016. Hymenolepis nana impact among children in the highlands of Cusco, Peru: An emerging neglected parasite infection. Am J Trop Med Hyg 95: 1031–1036. Erratum in: Am J Trop Med Hyg 2017;96(4):1004.
Martínez-Barbabosa I, Gutiérrez-Cárdenas EM, Gaona E, Shea M, 2010. The prevalence of Hymenolepis nana in schoolchildren in a bicultural community. Rev Biomed 21: 21–27.
Vilchez Barreto PM, Gamboa R, Santivañez S, O’Neal SE, Muro C, Lescano AG, Moyano LM, Gonzálvez G, García HH; The Cysticercosis Working Group in Perú, 2017. Prevalence, age profile, and associated risk factors for Hymenolepis nana infection in a large population-based study in northern Peru. Am J Trop Med Hyg 97: 583–586.
Spinicci M et al., 2018. Hymenolepis nana—An emerging intestinal parasite associated with anemia in school children from the Bolivian Chaco. Am J Trop Med Hyg 99: 1598–1601.
Pala E, Erguven M, Guven S, Erdogan M, Balta T, 2010. Psychomotor development in children with iron deficiency and iron-deficiency anemia. Food Nutr Bull 31: 431–435.
Lozoff B, Brittenham GM, Wolf AW, McClish DK, Kuhnert PM, Jimenez E, Jimenez R, Mora LA, Gomez I, Krauskoph D, 1987. Iron deficiency anemia and iron therapy effects on infant developmental test performance. Pediatrics 79: 981–995. Erratum in: Pediatrics 1988;81(5):683.
Shaw JG, Friedman JF, 2011. Iron deficiency anemia: Focus on infectious diseases in lesser developed countries. Anemia 2011: 260380.
Mohammad MA, Hegazi MA, 2007. Intestinal permeability in Hymenolepis nana as reflected by non invasive lactulose/mannitol dual permeability test and its impaction on nutritional parameters of patients. J Egypt Soc Parasitol 37: 877–891.
Bechir M, Schelling E, Hamit MA, Tanner M, Zinsstag J, 2012. Parasitic infections, anemia and malnutrition among rural settled and mobile pastoralist mothers and their children in Chad. Ecohealth 9: 122–131.
CDC, 2024. DPDx—Laboratory Identification of Parasites of Public Health Concern. Available at: https://www.cdc.gov/dpdx/hymenolepiasis/index.html. Accessed July 1, 2024.
Mason PR, Patterson BA, 1994. Epidemiology of Hymenolepis nana infections in primary school children in urban and rural communities in Zimbabwe. J Parasitol 80: 245–250.
Cabada MM, Morales ML, Webb CM, Yang L, Bravenec CA, Lopez M, Bascope R, White AC, Gotuzzo E, 2018. Socioeconomic factors associated with Fasciola hepatica infection among children from 26 communities of the Cusco region of Peru. Am J Trop Med Hyg 99: 1180–1185.
Webb CM, Morales ML, Lopez M, Baca-Turpo B, Arque E, White AC Jr., Cabada MM, 2021. Stunting in pre-school and school-age children in the Peruvian highlands and its association with Fasciola infection and demographic factors. PLoS Negl Trop Dis 15: e0009519.
Schreiner M, 2012. A Simple Poverty Scorecard for Peru. Available at: https://www.simplepovertyscorecard.com/PER_2010_ENG.pdf. Accessed July 1, 2024.
Anselin L, 1995. Local indicators of spatial association—LISA. Geogr Anal 27: 93–115.
Ord JK, Getis A, 2001. Testing for local spatial autocorrelation in the presence of global autocorrelation. J Reg Sci 41: 411–432.
Forson AO, Arthur I, Ayeh-Kumi PF, 2018. The role of family size, employment and education of parents in the prevalence of intestinal parasitic infections in school children in Accra. PLoS One 13: e0192303.
Delgado A, 2023. Altitude and distance relationships with the multidimensional poverty index: The case of Peru. Economia 46: 1–21.
Apaza C, Cuna W, Brañez F, Passera R, Rodriguez C, 2023. Frequency of gastrointestinal parasites, anemia, and nutritional status among children from different geographical regions of Bolivia. J Trop Med 8: 5020490.
Schmidlin T et al., 2013. Effects of hygiene and defecation behavior on helminths and intestinal protozoa infections in Taabo, Côte d’Ivoire. PLoS One 8: e65722.
Caravedo MA, Ramirez W, Morales ML, Lopez M, Janes CE, Bunag BA, Mixon KL, White AC, Tanabe MB, Cabada MM, 2021. Fasciola hepatica infection risk for adult household members living with children with fascioliasis in Cusco, Peru. Am J Trop Med Hyg 104: 2069–2073.
Panti-May JA, Servían A, Ferrari W, Zonta ML, Hernández-Mena DI, Hernández-Betancourt SF, Robles MR, Machain-Williams C, 2020. Morphological and molecular identification of hymenolepidid cestodes in children and synanthropic rodents from rural Mexico.Parasitol Int 75: 102042.
Ben-Ismail R, 1984. Evaluation of the activity of mebendazole in taeniasis caused by Hymenolepis nana in Tunisia. Bull Soc Pathol Exot Filiales 77: 363–368.
Khan W, Khan J, Rahman A, Ullah H, Salim M, Iqbal M, Khan I, Salman M, Munir B, 2018. Albendazole in the treatment of hymenolepiasis in school children. Pak J Pharm Sci 31 (1 Suppl): 305–309.
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Hymenolepis nana is an emergent parasitosis, and the role of schools in infection transmission is unclear. Data from a cross-sectional study evaluating children for H. nana infection in schools in three districts of Anta province in Peru were analyzed. Geospatial information from the children’s residence and school was obtained. A total of 2,961 children were included from 51 different schools. The median age was 9.6 years old (interquartile range [IQR]: 6.8–12.4), 1,479 (50%) were female, and the median H. nana prevalence per school was 15% (IQR: 3.61–24.20). Regression analysis demonstrated that those living in Ancahuasi and Zurite and those with higher poverty score and higher residence altitude were more likely to reside on a hot spot than a cold spot based on residence distribution, whereas being of school age was protective. Children living in low-risk areas (nonhot spots) who were attending schools with higher prevalence of H. nana (≥15%) were less likely to reside in Ancahuasi or Zurite than in Anta, had lower paternal education, and were older than 6 years of age. Our study shows that schools have a role in infection transmission among children in the highlands of Peru.
Financial support: This work was supported by the
Disclosures: The authors do not have any relevant disclosures. Part of the work was presented at the Conference of the American Society of Tropical Medicine and Hygiene meeting in 2023 in Chicago, IL.
Current contact information: Melinda B. Tanabe and Maria Caravedo Martinez, Division of Infectious Diseases, Department of Medicine, University of Texas Medical Branch, Galveston, TX, E-mails: mbtanabe@utmb.edu and alejandra.caravedo@gmail.com. Maria L. Morales and Martha Lopez, UPCH–UTMB Collaborative Research Center—Cusco, Universidad Peruana Cayetano Heredia, Cusco, Peru, E-mails: maria.morales.f@upch.pe and martlop2000@gmail.com. Miguel M. Cabada, Division of Infectious Diseases, Department of Medicine, University of Texas Medical Branch, Galveston, TX, UPCH–UTMB Collaborative Research Center—Cusco, Universidad Peruana Cayetano Heredia, Cusco, Peru, and Sede Cusco—Alexander von Humboldt Tropical Medicine Institute, Department of Medicine, Universidad Peruana Cayetano Heredia, Cusco, Peru, E-mail: micabada@utmb.edu.
Thompson RC, 2015. Neglected zoonotic helminths: Hymenolepis nana, Echinococcus canadensis and Ancylostoma ceylanicum. Clin Microbiol Infect 21: 426–432.
Al-Mekhlafi HM, 2020. The neglected cestode infection: Epidemiology of Hymenolepis nana infection among children in rural Yemen. Helminthologia 57: 293–305.
Cabada MM, Morales ML, Lopez M, Reynolds ST, Vilchez EC, Lescano AG, Gotuzzo E, Garcia HH, White AC Jr., 2016. Hymenolepis nana impact among children in the highlands of Cusco, Peru: An emerging neglected parasite infection. Am J Trop Med Hyg 95: 1031–1036. Erratum in: Am J Trop Med Hyg 2017;96(4):1004.
Martínez-Barbabosa I, Gutiérrez-Cárdenas EM, Gaona E, Shea M, 2010. The prevalence of Hymenolepis nana in schoolchildren in a bicultural community. Rev Biomed 21: 21–27.
Vilchez Barreto PM, Gamboa R, Santivañez S, O’Neal SE, Muro C, Lescano AG, Moyano LM, Gonzálvez G, García HH; The Cysticercosis Working Group in Perú, 2017. Prevalence, age profile, and associated risk factors for Hymenolepis nana infection in a large population-based study in northern Peru. Am J Trop Med Hyg 97: 583–586.
Spinicci M et al., 2018. Hymenolepis nana—An emerging intestinal parasite associated with anemia in school children from the Bolivian Chaco. Am J Trop Med Hyg 99: 1598–1601.
Pala E, Erguven M, Guven S, Erdogan M, Balta T, 2010. Psychomotor development in children with iron deficiency and iron-deficiency anemia. Food Nutr Bull 31: 431–435.
Lozoff B, Brittenham GM, Wolf AW, McClish DK, Kuhnert PM, Jimenez E, Jimenez R, Mora LA, Gomez I, Krauskoph D, 1987. Iron deficiency anemia and iron therapy effects on infant developmental test performance. Pediatrics 79: 981–995. Erratum in: Pediatrics 1988;81(5):683.
Shaw JG, Friedman JF, 2011. Iron deficiency anemia: Focus on infectious diseases in lesser developed countries. Anemia 2011: 260380.
Mohammad MA, Hegazi MA, 2007. Intestinal permeability in Hymenolepis nana as reflected by non invasive lactulose/mannitol dual permeability test and its impaction on nutritional parameters of patients. J Egypt Soc Parasitol 37: 877–891.
Bechir M, Schelling E, Hamit MA, Tanner M, Zinsstag J, 2012. Parasitic infections, anemia and malnutrition among rural settled and mobile pastoralist mothers and their children in Chad. Ecohealth 9: 122–131.
CDC, 2024. DPDx—Laboratory Identification of Parasites of Public Health Concern. Available at: https://www.cdc.gov/dpdx/hymenolepiasis/index.html. Accessed July 1, 2024.
Mason PR, Patterson BA, 1994. Epidemiology of Hymenolepis nana infections in primary school children in urban and rural communities in Zimbabwe. J Parasitol 80: 245–250.
Cabada MM, Morales ML, Webb CM, Yang L, Bravenec CA, Lopez M, Bascope R, White AC, Gotuzzo E, 2018. Socioeconomic factors associated with Fasciola hepatica infection among children from 26 communities of the Cusco region of Peru. Am J Trop Med Hyg 99: 1180–1185.
Webb CM, Morales ML, Lopez M, Baca-Turpo B, Arque E, White AC Jr., Cabada MM, 2021. Stunting in pre-school and school-age children in the Peruvian highlands and its association with Fasciola infection and demographic factors. PLoS Negl Trop Dis 15: e0009519.
Schreiner M, 2012. A Simple Poverty Scorecard for Peru. Available at: https://www.simplepovertyscorecard.com/PER_2010_ENG.pdf. Accessed July 1, 2024.
Anselin L, 1995. Local indicators of spatial association—LISA. Geogr Anal 27: 93–115.
Ord JK, Getis A, 2001. Testing for local spatial autocorrelation in the presence of global autocorrelation. J Reg Sci 41: 411–432.
Forson AO, Arthur I, Ayeh-Kumi PF, 2018. The role of family size, employment and education of parents in the prevalence of intestinal parasitic infections in school children in Accra. PLoS One 13: e0192303.
Delgado A, 2023. Altitude and distance relationships with the multidimensional poverty index: The case of Peru. Economia 46: 1–21.
Apaza C, Cuna W, Brañez F, Passera R, Rodriguez C, 2023. Frequency of gastrointestinal parasites, anemia, and nutritional status among children from different geographical regions of Bolivia. J Trop Med 8: 5020490.
Schmidlin T et al., 2013. Effects of hygiene and defecation behavior on helminths and intestinal protozoa infections in Taabo, Côte d’Ivoire. PLoS One 8: e65722.
Caravedo MA, Ramirez W, Morales ML, Lopez M, Janes CE, Bunag BA, Mixon KL, White AC, Tanabe MB, Cabada MM, 2021. Fasciola hepatica infection risk for adult household members living with children with fascioliasis in Cusco, Peru. Am J Trop Med Hyg 104: 2069–2073.
Panti-May JA, Servían A, Ferrari W, Zonta ML, Hernández-Mena DI, Hernández-Betancourt SF, Robles MR, Machain-Williams C, 2020. Morphological and molecular identification of hymenolepidid cestodes in children and synanthropic rodents from rural Mexico.Parasitol Int 75: 102042.
Ben-Ismail R, 1984. Evaluation of the activity of mebendazole in taeniasis caused by Hymenolepis nana in Tunisia. Bull Soc Pathol Exot Filiales 77: 363–368.
Khan W, Khan J, Rahman A, Ullah H, Salim M, Iqbal M, Khan I, Salman M, Munir B, 2018. Albendazole in the treatment of hymenolepiasis in school children. Pak J Pharm Sci 31 (1 Suppl): 305–309.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 1056 | 1056 | 721 |
Full Text Views | 25 | 25 | 8 |
PDF Downloads | 28 | 28 | 14 |