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Enterobiasis and its risk factors in urban, rural and indigenous children of subtropical Argentina

Published online by Cambridge University Press:  03 November 2021

Maria Romina Rivero*
Affiliation:
Instituto Nacional de Medicina Tropical, INMeT, Neuquén y Jujuy s/n., Puerto Iguazú, Misiones 3370, Argentina Instituto de Desarrollo Agroindustrial y de la Salud (IDAS-CONCIET), Universidad Nacional de Rio Cuarto, Ruta 36 Km 601, Rio Cuarto, Córdoba 5800, Argentina
Carlos De Angelo
Affiliation:
Assoc. Civil Centro de Investigaciones del Bosque Atlántico (CeIBA), Bertoni 85, Puerto Iguazú, Misiones 3370, Argentina Instituto de Ciencias de la Tierra, Biodiversidad y Ambiente (ICBIA-CONICET), Universidad Nacional de Rio Cuarto, Ruta 36 Km 601, Rio Cuarto, Córdoba 5800, Argentina
Constanza Feliziani
Affiliation:
Instituto de Investigación Médica Mercedes y Martín Ferreyra, INIMEC-CONCIET, Universidad Nacional de Córdoba, Friuli 2434, Córdoba 5000, Argentina
Song Liang
Affiliation:
Department of Environmental and Global Health, University of Florida, Gainesville, FL 32610, USA Emerging Pathogens Institute, University of Florida, Gainesville, FL 32610, USA
Karina Tiranti
Affiliation:
Departamento de Patología Animal, Facultad de Agronomía y Veterinaria, Universidad Nacional de Rio Cuarto, Ruta 36 Km 601, Rio Cuarto, Córdoba 5800, Argentina
Martin Miguel Salas
Affiliation:
Instituto Nacional de Medicina Tropical, INMeT, Neuquén y Jujuy s/n., Puerto Iguazú, Misiones 3370, Argentina
Oscar Daniel Salomon
Affiliation:
Instituto Nacional de Medicina Tropical, INMeT, Neuquén y Jujuy s/n., Puerto Iguazú, Misiones 3370, Argentina
*
Author for correspondence: Maria Romina Rivero, E-mail: rivero.maria@conicet.gov.ar

Abstract

A cross-sectional survey to assess the prevalence of Enterobius vermicularis infection and its associated factors among the child population of infant, preschool and school age in the urban, rural and indigenous population of Iguazú city, in subtropical Argentina was presented. Additionally, the status of enterobiasis at country level was reviewed and analysed. Enterobius vermicularis presence was assessed employing an oviscopic serial sampling technique. Statistical analysis of socio-demographic determinants was performed by generalized linear mixed models at individual, household and community levels. Preferred Reporting Items for Systematic Reviews and Meta-Analysis guidelines were used to gather national information about E. vermicularis prevalence spanning the decade 2010–2020. A total of 916 children from 470 families participated. Overall prevalence was 29.8%, with 25.3, 30.7 and 34.2% detected for children inhabiting urban, rural and indigenous villages, respectively. The multi-level analysis showed that the presence of E. vermicularis was mostly determined by individual (e.g. age, playing habits, previous pinworm infection) and household-level factors (e.g. family size, overcrowding conditions). Interestingly, WASH variables, such as waste disposal, analysed at community level were also important. Data were analysed to provide eco-epidemiological features of enterobiasis in a heterogeneous subtropical child population in the same territory but with different socio-sanitary realities. The importance of promoting multi-level actions against the determinants identified, to control this public health problem integratively was evidenced. The scoping review of national data updated the state of knowledge of this parasitosis, identifying risk determinants and gaps in knowledge at country level.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Barton, K (2020) MuMIn, Multi-model inference. R package version 1.43. 17. Available at https://CRAN.R-project.org/package=MuMIn (Accessed 8 December 2020).Google Scholar
Bates, D, Mächler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 148.CrossRefGoogle Scholar
Bertonatti, C and Corcuera, J (eds) (2000) Situación Ambiental Argentina 2000. Buenos Aires, Argentina: Fundación Vida Silvestre Argentina.Google Scholar
Bethony, J, Brooker, S, Albonico, M, Geiger, SM, Loukas, A, Diemert, D and Hotez, PJ (2006) Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet (London, England) 367, 15211532.CrossRefGoogle ScholarPubMed
Bolker, B and Robinson, D (2021) broom.mixed: Tidying Methods for Mixed Models. R package version 0.2.7. Available at https://CRAN.R-project.org/package=broom.mixed (Accessed 2 September 2021).Google Scholar
Bórquez, C, Lobato, I, Montalvo, MT, Marchant, P and Martínez, P (2004) Enteroparasitosis en niños escolares del valle de Lluta. Arica-Chile. Parasitología latinoamericana 59, 175178.CrossRefGoogle Scholar
Botero, D and Restrepo, M (2012) Oxiuriasis. Parasitosis Humanas, 5th Edn. Medellín, Colombia: Corporación para Investigaciones Biológicas, pp. 177186.Google Scholar
Bracciaforte, R, Fernanda Diaz, M, Vottero Pivetta, V, Burstein, V, Varengo, H and Angel Orsilles, M (2010) Enteroparasites in children and adolescents of a periurban community in the province of Cordoba. Acta Bioquimica Clinica Latinoamericana 44, 353358.Google Scholar
Brandelli, CLC, Carli, GAd, Macedo, AJ and Tasca, T (2012) Intestinal parasitism and socio-environmental factors among Mbyá-Guarani Indians, Porto Alegre, Rio Grande do Sul, Brazil. Revista do Instituto de Medicina Tropical de Sao Paulo 54, 119122.CrossRefGoogle Scholar
Burnham, KP and Anderson, DR (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. New York, USA: Springer-Verlag.Google Scholar
Cazorla, DJ, Acosta, ME, Zarraga, A and Morales, P (2006) Estudio clínico-epidemiológico de enterobiasis en preescolares y escolares de Taratara, Estado Falcón, Venezuela. Parasitología latinoamericana 61, 4353.CrossRefGoogle Scholar
Cociancic, P, Zonta, ML and Navone, GT (2018) A cross-sectional study of intestinal parasitoses in dogs and children of the periurban area of La Plata (Buenos Aires, Argentina): Zoonotic importance and implications in public health. Zoonoses and Public Health 65, e44e53.CrossRefGoogle Scholar
Cociancic, P, Torrusio, SE, Zonta, ML and Navone, GT (2019) Risk factors for intestinal parasitoses among children and youth of Buenos Aires, Argentina. One Health 9, 100116. Published 102019 Nov 100128. doi:100110.101016/j.onehlt.102019.100116.CrossRefGoogle ScholarPubMed
Cook, G (1994) Enterobius vermicularis infection. Gut 35, 1159.CrossRefGoogle ScholarPubMed
Craggs, B, De Waele, E, De Vogelaere, K, Wybo, I, Laubach, M, Hoorens, A and De Waele, B (2009) Enterobius vermicularis infection with tuboovarian abscess and peritonitis occurring during pregnancy. Surgical Infections 10, 545547.CrossRefGoogle ScholarPubMed
Cranston, I, Potgieter, N, Mathebula, S and Ensink, JH (2015) Transmission of Enterobius vermicularis eggs through hands of school children in rural South Africa. Acta Tropica 150, 9496.CrossRefGoogle ScholarPubMed
Curtis, VA, Danquah, LO and Aunger, RV (2009) Planned, motivated and habitual hygiene behaviour: an eleven country review. Health Education Research 24, 655673.CrossRefGoogle ScholarPubMed
Das, DK, Pathan, SK, Hira, PR, Madda, JP, Hasaniah, WF and Juma, TH (2001) Pelvic abscess from Enterobius vermicularis. Report of a case with cytologic detection of eggs and worms. Acta Cytologica 45, 425429.CrossRefGoogle ScholarPubMed
Dean, AG, Sullivan, KM and Soe, MM (2013) OpenEpi: Open Source Epidemiologic Statistics for Public Health, Version 3.01. Available at www.OpenEpi.com (Accessed 21 December 2017).Google Scholar
Dib, J, Oquilla, J, Lazarte, SG and Gonzalez, SN (2012) Parasitic prevalence in a suburban school of famailla, tucuman, Argentina. ISRN Microbiol 26, 14.CrossRefGoogle Scholar
Dib, JR, Fernandez-Zenoff, MV, Oquilla, J, Lazarte, S and Gonzalez, SN (2015) Prevalence of intestinal parasitic infection among children from a shanty town in Tucuman, Argentina. Trop Biomed 32, 210215.Google ScholarPubMed
Duflo, E, Galiani, S and Mobarak, M (2012) Improving Access to Urban Services for the Poor: Open Issues and a Framework for a Future Research Agenda. Cambridge, MA: Abdul Latif Jameel Poverty Action Lab.Google Scholar
Dunphy, L, Clark, Z and Raja, MH (2017) Enterobius vermicularis (pinworm) infestation in a child presenting with symptoms of acute appendicitis: a wriggly tale!. Case Reports 6, 2017220473.Google Scholar
Efared, B, Atsame-Ebang, G, Soumana, BM, Tahiri, L, Hammas, N, El Fatemi, H and Chbani, L (2017) Acute suppurative appendicitis associated with Enterobius vermicularis: an incidental finding or a causative agent? A case report. BMC Research Notes 10, 017-2822.CrossRefGoogle ScholarPubMed
Eisenberg, JN, Desai, MA, Levy, K, Bates, SJ, Liang, S, Naumoff, K and Scott, JC (2007) Environmental determinants of infectious disease: a framework for tracking causal links and guiding public health research. Environmental Health Perspectives 115, 1216.CrossRefGoogle ScholarPubMed
Elsaid, N, Mahmood, H, Tekkis, P and Tan, E (2014) Enterobiasis-related inflammatory caecal polyp masquerading as a malignancy. Case Reports 15, 2013201599.Google Scholar
Ferioli, S, Perazzo, JM and Paulin, P (2020) Prevalencia de parásitos intestinales en muestras de pacientes atendidos en el Hospital de Pediatría" Prof. Dr. Juan P. Garrahan", Argentina, 2018-2019. Acta bioquím. clín. latinoam 455460.Google Scholar
Gamboa, MI, Zonta, L and Navone, GT (2010) Parásitos intestinales y pobreza: la vulnerabilidad de los más carenciados en la Argentina de un mundo globalizado. Journal of the Selva Andina Research Society 1, 2337.CrossRefGoogle Scholar
Gamboa, MI, Giambelluca, LA and Navone, GT (2014) Spatial distribution of intestinal parasites in the City of La Plata, Argentina. Medicina 74, 363370.Google ScholarPubMed
Garbossa, G, Pia Buyayisqui, M, Geffner, L, Lopez Arias, L, de la Fourniere, S, Haedo, AS, Marconi, AE, Frid, JC, Nesse, AB and Bordoni, N (2013) Social and environmental health determinants and their relationship with parasitic diseases in asymptomatic children from a shantytown in Buenos Aires, Argentina. Pathog Glob Health 107, 141152.CrossRefGoogle ScholarPubMed
Gelaw, A, Anagaw, B, Nigussie, B, Silesh, B, Yirga, A, Alem, M, Endris, M and Gelaw, B (2013) Prevalence of intestinal parasitic infections and risk factors among schoolchildren at the University of Gondar Community School, Northwest Ethiopia: a cross-sectional study. BMC Public Health 13, 304.CrossRefGoogle ScholarPubMed
Georgiev, VS (2001) Chemotherapy of enterobiasis (oxyuriasis). Expert Opinion on Pharmacotherapy 2, 267275.CrossRefGoogle Scholar
Halpenny, CM, Koski, KG, Valdés, VE and Scott, ME (2012) Prediction of child health by household density and asset-based indices in impoverished indigenous villages in rural Panamá. The American Journal of Tropical Medicine and Hygiene 86, 280291.CrossRefGoogle ScholarPubMed
Hamdona, SM, Lubbad, AM and Al-Hindi, AI (2016) Histopathological study of Enterobius vermicularis among appendicitis patients in Gaza strip, Palestine. Journal of Parasitic Diseases 40, 176183.CrossRefGoogle ScholarPubMed
Hartig, F (2021) DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models. R package version 0.4.3. Available at http://florianhartig.github.io/DHARMa/ (Accessed 2 September 2021).Google Scholar
Horne, P (2002) First evidence of enterobiasis in ancient Egypt. The Journal of Parasitology 88, 10191021.CrossRefGoogle ScholarPubMed
INDEC (2010) Censo Nacional de Población y Vivienda. Buenos Aires, Argentina: Instituto Nacional de Estadística y Censo de Argentina.Google Scholar
INDEC (2016) Incidencia de la Pobreza y de la Indigencia en 31 aglomerados urbanos. Buenos Aires: Resultados segundo trimestre de 2016. Ministerio de Hacienda y Financias Públicas.Google Scholar
INDEC (2018) Anuario Estadístico de la República Argentina 2017, 1st Edn. Buenos Aires, Argentina: Ciudad Autónoma de Buenos Aires.Google Scholar
INDEC (2019) Instituto Nacional de Estadísticas y Censos, Republica Argentina. Available at https://www.indec.gob.ar/indec/web/Institucional-Indec-QuienesSomosEng (Accessed 31 August 2021).Google Scholar
Kang, I-S, Kim, D-H, An, H-G, Son, H-M, Cho, MK, Park, M-K, Kang, SA, Kim, BY and Yu, HS (2012) Impact of health education on the prevalence of enterobiasis in Korean preschool students. Acta Tropica 122, 5963.CrossRefGoogle ScholarPubMed
Kashyap, B, Samantray, JC, Kumar, S, Jhamb, R, Singh, AK and Kaur, IR (2014) Recurrent paediatric pinworm infection of the vagina as a potential reservoir for Enterobius vermicularis. Journal of Helminthology 88, 381383.CrossRefGoogle ScholarPubMed
Kim, DH and Yu, HS (2014) Effect of a one-off educational session about enterobiasis on knowledge, preventative practices, and infection rates among schoolchildren in South Korea. PLoS ONE 9, e112149. doi: 10.1371/journal.pone.0112149CrossRefGoogle ScholarPubMed
Knudson, A, Lemos, E, Ariza, Y, Salazar, M, del Pilar Chaves, M, López, MC, Quintana, C, Moncada, LI, López, G and Sánchez, R (2003) Frecuencia de E. vermicularis en una población escolar rural de Quipile, Colombia, 2001. Revista de Salud Publica 5, 8799.Google Scholar
Lala, S and Upadhyay, V (2016) Enterobius vermicularis and its role in paediatric appendicitis: protection or predisposition? ANZ Journal of Surgery 86, 717719.CrossRefGoogle ScholarPubMed
Laoraksawong, P, Pansuwan, P, Krongchon, S, Pongpanitanont, P and Janwan, P (2020) Prevalence of Enterobius vermicularis infections and associated risk factors among schoolchildren in Nakhon Si Thammarat, Thailand. Tropical Medicine and Health 48, 17.CrossRefGoogle ScholarPubMed
Lazarte, SG, Christian, A, Oquilla, J and Gonzalez, SN (2006) Alarming levels of infection by enteric parasites in children of Burruyacu, Province of Tucumán, Argentina. International Journal of Tropical Medicine 1, 4043.Google Scholar
Levens, A, Schurink, M, Koetse, HA and van Baren, R (2014) Infestation with Enterobius vermicularis mimicking appendicitis. Nederlands Tijdschrift voor Geneeskunde 158, A7371A7371.Google ScholarPubMed
Lukes, J, Horák, A and Scholz, T (2005) Helminth genome projects: all or nothing. Trends in Parasitology 21, 265266.CrossRefGoogle ScholarPubMed
Magalhães, RJS, Clements, AC, Patil, AP, Gething, PW and Brooker, S (2011) The applications of model-based geostatistics in helminth epidemiology and control. Advances in Parasitology 74, 267.CrossRefGoogle ScholarPubMed
Makoni, F, Ndamba, J, Mbati, P and Manase, G (2004) Impact of waste disposal on health of a poor urban community in Zimbambwe. East African Medical Journal 81, 422426.CrossRefGoogle ScholarPubMed
Moffa, M, Cronk, R, Fejfar, D, Dancausse, S, Padilla, LA and Bartram, J (2019) A systematic scoping review of hygiene behaviors and environmental health conditions in institutional care settings for orphaned and abandoned children. Science of the Total Environment 658, 11611174.CrossRefGoogle ScholarPubMed
Moher, D, Shamseer, L, Clarke, M, Ghersi, D, Liberati, A, Petticrew, M, Shekelle, P and Stewart, LA (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Systematic Reviews 4, 1.CrossRefGoogle ScholarPubMed
Molina, N, Pezzani, B, Ciarmela, M, Orden, A, Rosa, D, Apezteguía, M, Basualdo, J and Minvielle, M (2011) Intestinal parasites and genotypes of Giardia intestinalis in school children from Berisso, Argentina. The Journal of Infection in Developing Countries 5, 527534.CrossRefGoogle ScholarPubMed
Moosazadeh, M, Abedi, G, Afshari, M, Mahdavi, SA, Farshidi, F and Kheradmand, E (2017) Prevalence of Enterobius vermicularis among children in Iran: a systematic review and meta-analysis. Osong Public Health and Research Perspectives 8, 108115.CrossRefGoogle ScholarPubMed
Morrow, JJ and Reinhard, KJ (2018) The paleoepidemiology of Enterobius vermicularis (Nemata: Oxyuridae) Among the Loma San Gabriel at La Cueva de los Muertos Chiquitos (600–800 CE), Rio Zape Valley, Durango, Mexico. Comparative Parasitology 85, 2733.CrossRefGoogle Scholar
Mwangi, W, de Figueiredo, P and Criscitiello, MF (2016) One health: addressing global challenges at the nexus of human, animal, and environmental health. PLoS Pathogens 12, e1005731.CrossRefGoogle Scholar
Navone, GT, Gamboa, MI, Oyhenart, EE and Orden, AB (2006) Intestinal parasitosis in Mbya-Guarani populations from Misiones Province, Argentina: epidemiological and nutritional aspects. Cadernos de Saude Publica 22, 10891100.CrossRefGoogle ScholarPubMed
Navone, GT, Zonta, ML, Cociancic, P, Garraza, M, Gamboa, MI, Giambelluca, LA, Dahinten, S and Oyhenart, EE (2017) Estudio transversal de las parasitosis intestinales en poblaciones infantiles de Argentina. Revista Panamericana de Salud Pública 41, e24.Google Scholar
Ngui, R, Ravindran, S, Ong, DB, Chow, TK, Low, KP, Nureena, ZS, Rajoo, Y, Chin, YT, Amir, A, Ahmad, AF, Lim, YA and Mahmud, R (2014) Enterobius vermicularis salpingitis seen in the setting of ectopic pregnancy in a Malaysian patient. Journal of Clinical Microbiology 52, 34683470.CrossRefGoogle Scholar
Nithikathkul, C, Akarachantachote, N, Wannapinyosheep, S, Pumdonming, W, Brodsky, M and Sukthana, Y (2005) Impact of health educational programmes on the prevalence of enterobiasis in schoolchildren in Thailand. Journal of Helminthology 79, 6165.CrossRefGoogle ScholarPubMed
Odonkor, ST, Frimpong, K and Kurantin, N (2020) An assessment of house-hold solid waste management in a large Ghanaian district. Heliyon 6, e03040.CrossRefGoogle Scholar
Olson, DM and Dinerstein, E (1998) The Global 200: a representation approach to conserving the Earth's most biologically valuable ecoregions. Conservation Biology 12, 502515.CrossRefGoogle Scholar
Orellano, P, Vezzani, D, Quaranta, N, Cionco, R, Reynoso, J and Salomon, O (2018 a) Potential occurrence of Zika from subtropical to temperate Argentina considering the basic reproduction number (R0). Revista Panamericana de Salud Pública 41, e120.Google Scholar
Orellano, P, Vezzani, D, Quaranta, N, Reynoso, J and Salomón, OD (2018 b) Estimation of expected dengue seroprevalence from passive epidemiological surveillance systems in selected areas of Argentina: a proxy to evaluate the applicability of dengue vaccination. Vaccine 36, 979985.CrossRefGoogle ScholarPubMed
Oyhenart, EE, Garraza, M, Bergel, ML, Torres, MF, Castro, LE, Luis, MA, Forte, ML, Gamboa, MI, Zonta, ML, Cesani, MF, Quintero, FA, Luna, ME and Navone, GT (2013) Caracterización del estado nutricional, enteroparasitosis y condiciones socio-ambientales de la población infanto-juvenil del partido de La Plata. Revista Argentina de Antropología Biológica 15, 4760.Google Scholar
Park, JH, Han, ET, Kim, WH, Shin, EH, Guk, SM, Kim, JL and Chai, JY (2005) A survey of Enterobius vermicularis infection among children on western and southern coastal islands of the Republic of Korea. Korean Journal of Parasitology 43, 129134.CrossRefGoogle ScholarPubMed
Pezzani, B, Ciarmela, ML, Apezteguía, MC, Molina, N, Orden, A, Rosa, D and Minvielle, M (2012) Intestinal parasitoses in suburban and rural schoolchildren in Argentina. Revista Patol Trop 41, 6373.Google Scholar
Pigac, B, Masic, S and Masic, V (2017) Enterobius vermicularis in the endometrium of the uterus: a case report. Iranian Journal of Parasitology 12, 638641.Google ScholarPubMed
Powell, G, Sarmah, P, Sethi, B and Ganesan, R (2013) Enterobius vermicularis infection of the ovary. Case Reports 31, 2013201146.Google Scholar
Pullan, R and Brooker, S (2008) The health impact of polyparasitism in humans: are we under-estimating the burden of parasitic diseases? Parasitology 135, 783794.CrossRefGoogle ScholarPubMed
R Development Core Team (2016) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Reinhard, KJ, Araujo, A and Morrow, JJ (2016) Temporal and spatial distribution of Enterobius vermicularis (Nematoda: Oxyuridae) in the Prehistoric Americas. Korean Journal of Parasitology 54, 591603.CrossRefGoogle ScholarPubMed
Remm, K and Remm, M (2010) Geographical aspects of enterobiasis in Estonia. Health and Place 16, 291300.CrossRefGoogle ScholarPubMed
Requena-Certad, I, Lizardi, V, Mejía, LM, Castillo, H and Devera, R (2002) Infección por Enterobius vermicularis en niños preescolares de ciudad Bolívar, Venezuela. Revista Biomédica 13, 231240.CrossRefGoogle Scholar
Rivero, MR, De Angelo, C, Nunez, P, Salas, M, Motta, CE, Chiaretta, A, Salomon, OD and Liang, S (2017 a) Environmental and socio-demographic individual, family and neighborhood factors associated with children intestinal parasitoses at Iguazu, in the subtropical northern border of Argentina. PLoS Neglected Tropical Diseases 11, 0006098.CrossRefGoogle ScholarPubMed
Rivero, MR, Salas, MM, Valente, R, Nores, MJ, De Angelo, C, Arrabal, J, Costa, S and Salomon, OD (2017 b) Prevention of intestinal parasites in a tri-border area of Latin America: children perceptions and an integral health education strategy. Zoonoses and Public Health 7, 12365.Google Scholar
Rivero, MR, De Angelo, C, Nunez, P, Salas, M and Liang, S (2018) Intestinal parasitism and nutritional status among indigenous children from the Argentinian Atlantic Forest: determinants of enteroparasites infections in minority populations. Acta Tropica 187, 248256.CrossRefGoogle ScholarPubMed
Rivero, MR, Feliziani, C, De Angelo, C, Tiranti, K, Salomon, OD and Touz, MC (2020) Giardia spp., the most ubiquitous protozoan parasite in Argentina: human, animal and environmental surveys reported in the last 40 years. Parasitology Research 119, 31813201. doi: 10.1007/s00436-020-06853-7.CrossRefGoogle ScholarPubMed
Romero-Sandoval, N, Ortiz-Rico, C, Sánchez-Pérez, HJ, Valdivieso, D, Sandoval, C, Pástor, J and Martín, M (2017) Soil transmitted helminthiasis in indigenous groups. A community cross sectional study in the Amazonian southern border region of Ecuador. BMJ Open 7, e013626.CrossRefGoogle ScholarPubMed
Ross, H (2012) One health from a social–ecological systems perspective: enriching social and cultural dimensions. In Mackenzie, John S, Jeggo, Martyn, Daszak, Peter and Richt, Juergen A (eds), One Health: The Human-Animal-Environment Interfaces in Emerging Infectious Diseases. Springer Heidelberg: Springer, pp. 217229.CrossRefGoogle Scholar
Rustan, ME, Altamira, SM, Gili, M, Peralta, NB, Zitta, ME and Varengo, HT (2011) Epidemiología de las enteroparasitosis y micosis superficiales en comunidades y Hospital Infantil de Córdoba. Revista de Salud Publica 15, 1826.Google Scholar
Salomón, OD, Acardi, SA, Liotta, DJ, Fernández, MS, Lestani, E, López, D, Mastrángelo, AV, Figueroa, M and Fattore, G (2009) Epidemiological aspects of cutaneous leishmaniasis in the Iguazú falls area of Argentina. Acta Tropica 109, 511.CrossRefGoogle ScholarPubMed
Song, H-J, Cho, C-H, Kim, J-S, Choi, M-H and Hong, S-T (2003) Prevalence and risk factors for enterobiasis among preschool children in a metropolitan city in Korea. Parasitology Research 91, 4650.CrossRefGoogle Scholar
Soriano, SV, Barbieri, LM, Pierangeli, NB, Giayetto, AL, Manacorda, AM, Castronovo, E, Pezzani, BC, Minvielle, M and Basualdo, JA (2001) Intestinal parasites and the environment: frequency of intestinal parasites in children of Neuquen, Patagonia, Argentina. Revista Latinoamericana de Microbiologia 43, 96101.Google ScholarPubMed
Soto, JCR and Quiñones, MC (2015) Factores sociales e incidencia de Enterobius vermicularis en instituciones educativas de nivel inicial del distrito de Cascas. In Crescendo 6, 2132.Google Scholar
Sung, J, Lin, RS, Huang, KC, Wang, SY and Lu, Y-J (2001) Pinworm control and risk factors of pinworm infection among primary-school children in Taiwan. The American Journal of Tropical Medicine and Hygiene 65, 558562.CrossRefGoogle ScholarPubMed
Tapia, Ó and Muñoz, C (2011) Oxiuriasis apendicular: estudio de prevalencia y descripción clínico-morfológica. Revista chilena de cirugía 63, 599603.CrossRefGoogle Scholar
United Nations Environment Programme (2009) Developing integrated solid waste management plan training manual. Vol. 4 pp. 176. UNEP, Osaka/Shiga, Japan.Google Scholar
Vaumourin, E, Vourc'h, G, Gasqui, P and Vayssier-Taussat, M (2015) The importance of multiparasitism: examining the consequences of co-infections for human and animal health. Parasites & Vectors 8, 10151167.CrossRefGoogle ScholarPubMed
Wendt, S, Trawinski, H, Schubert, S, Rodloff, AC, Mössner, J and Lübbert, C (2019) The diagnosis and treatment of pinworm infection. Deutsches Ärzteblatt International 116, 213.Google ScholarPubMed
Worrell, CM, Wiegand, RE, Davis, SM, Odero, KO, Blackstock, A, Cuellar, VM, Njenga, SM, Montgomery, JM, Roy, SL and Fox, LM (2016) A cross-sectional study of water, sanitation, and hygiene-related risk factors for soil-transmitted helminth infection in urban school- and preschool-aged children in Kibera, Nairobi. PLoS ONE 11, e0150744.CrossRefGoogle ScholarPubMed
Zafar, S, Tariq, MU and Ahmed, Z (2018) Ectopic Enterobius vermicularis infestation; an extremely rare cause of mesenteric lymphadenopathy mimicking tuberculous lymphadenitis. Journal of Ayub Medical College, Abbottabad 30, 124126.Google ScholarPubMed
Zonta, ML, Cociancic, P, Oyhenart, EE and Navone, GT (2019) Intestinal parasitosis, undernutrition and socio-environmental factors in schoolchildren from Clorinda Formosa, Argentina. Revista de Salud Publica 21, 224231.CrossRefGoogle ScholarPubMed
Zuur, A, Ieno, E, Walker, N, Savilev, A and Smith, G (2009) Mixed Effects Models and Extensions in Ecology with R. New York, USA: Spring Science & Business Media.CrossRefGoogle Scholar
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