Hostname: page-component-76fb5796d-9pm4c Total loading time: 0 Render date: 2024-04-26T22:24:32.925Z Has data issue: false hasContentIssue false
  • English
  • Français

Ascaris and hookworm transmission in preschool children from rural Panama: role of yard environment, soil eggs/larvae and hygiene and play behaviours

Published online by Cambridge University Press:  25 August 2015

RACHEL J. KRAUSE ,
KRISTINE G. KOSKI ,
EMÉRITA PONS ,
NIDIA SANDOVAL ,
ODALIS SINISTERRA  and
MARILYN E. SCOTT
RACHEL J. KRAUSE
Affiliation:
Institute of Parasitology and Centre for Host-Parasite Interactions, McGill University, Montreal, Canada. Phone: 514-398-7996; Fax: 514-398-7857
KRISTINE G. KOSKI
Affiliation:
School of Dietetics and Human Nutrition and Centre for Host-Parasite Interactions, McGill University, Montreal, Canada
EMÉRITA PONS
Affiliation:
Department of Nutritional Health, Ministry of Health, Panama City, Republic of Panama
NIDIA SANDOVAL
Affiliation:
Department of Microbiology and Parasitology, University of Panama, Panama City, Republic of Panama
ODALIS SINISTERRA
Affiliation:
Department of Nutritional Health, Ministry of Health, Panama City, Republic of Panama
MARILYN E. SCOTT*
Affiliation:
Institute of Parasitology and Centre for Host-Parasite Interactions, McGill University, Montreal, Canada. Phone: 514-398-7996; Fax: 514-398-7857
*
*Corresponding author. Institute of Parasitology and Centre for Host-Parasite Interactions, McGill University (Macdonald Campus), Ste-Anne de Bellevue, Quebec, CanadaH9X 3V9. E-mail: marilyn.scott@mcgill.ca
Get access Rights & Permissions [Opens in a new window]

Summary

This study explored whether the yard environment and child hygiene and play behaviours were associated with presence and intensity of Ascaris and hookworm in preschool children and with eggs and larvae in soil. Data were collected using questionnaires, a visual survey of the yard, soil samples and fecal samples collected at baseline and following re-infection. The presence of eggs/larvae in soil was associated negatively with water storage (eggs) but positively with dogs (eggs) and distance from home to latrine (larvae). Baseline and re-infection prevalences were: hookworm (28·0%, 3·4%); Ascaris (16·9%, 9·5%); Trichuris (0·9%, 0·7%). Zero-inflated negative binomial regression models revealed a higher baseline hookworm infection if yards had eggs or larvae, more vegetation or garbage, and if the child played with soil. Baseline Ascaris was associated with dirt floor, dogs, exposed soil in yard, open defecation and with less time playing outdoors, whereas Ascaris re-infection was associated with water storage, vegetation cover and garbage near the home and not playing with animals. Our results show complex interactions between infection, the yard environment and child behaviours, and indicate that transmission would be reduced if latrines were closer to the home, and if open defecation and water spillage were reduced.

Keywords

soil-transmitted helminthsAscarishookwormsoil eggs and larvaevegetation coverwater storagelatrinesopen defecationsoil contactlandscape of yard
Type
Research Article
Information
Parasitology , Volume 142 , Issue 12 , October 2015 , pp. 1543 - 1554
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

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

Adenusi, A. A. and Adewoga, T. O. (2013). Studies on the potential and public health importance of non-biting synanthropic flies in the mechanical transmission of human enterohelminths. Transactions of the Royal Society of Tropical Medicine and Hygiene 107, 812–818.Google Scholar
Al-Delaimy, A. K., Al-Mekhlafi, H. M., Nasr, N. A., Sady, H., Atroosh, W. M., Nashiry, M., Anuar, T. S., Moktar, N., Lim, Y. A. and Mahmud, R. (2014). Epidemiology of intestinal polyparasitism among Orang Asli school children in rural Malaysia. PLoS Neglected Tropical Diseases 8, e3074.Google Scholar
Alemu, A., Atnafu, A., Addis, Z., Shiferaw, Y., Teklu, T., Mathewos, B., Birhan, W., Gebretsadik, S. and Gelaw, B. (2011). Soil transmitted helminths and Schistosoma mansoni infections among school children in Zarima town, northwest Ethiopia. BMC Infectious Diseases 11, 189.CrossRefGoogle ScholarPubMed
Balen, J., Raso, G., Li, Y.-S., Zhao, Z.-Y., Yuan, L.-P., Williams, G. M., Luo, X.-S., Shi, M.-Z., Yu, X.-L. and Utzinger, J. (2011). Risk factors for helminth infections in a rural and a peri-urban setting of the Dongting Lake area, People's Republic of China. International Journal for Parasitology 41, 1165–1173.Google Scholar
Bergstrøm, K. and Langeland, G. (1981). Survival of Ascaris eggs, Salmonella and fecal coli in soil and on vegetables grown in infected soil (author's transl). (article in Norwegian). Nordisk Veterinaermedicin 33, 23–32.Google ScholarPubMed
Betson, M., Nejsum, P., Bendall, R. P., Deb, R. M. and Stothard, J. R. (2014). Molecular epidemiology of ascariasis: a global perspective on the transmission dynamics of Ascaris in people and pigs. Journal of Infectious Diseases 210, 932–941.CrossRefGoogle ScholarPubMed
Blaszkowska, J., Kurnatowski, P. and Damiecka, P. (2011). Contamination of the soil by eggs of geohelminths in rural areas of Lodz district (Poland). Helminthologia 48, 67–76.Google Scholar
Chongsuvivatwong, V., Uga, S. and Nagnaen, W. (1999). Soil contamination and infections by soil-transmitted helminths in an endemic village in southern Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 30, 64–67.Google Scholar
Cundill, B., Alexander, N., Bethony, J. M., Diemert, D., Pullan, R. L. and Brooker, S. (2013). Rates and intensity of re-infection with human helminths after treatment and the influence of individual, household, and environmental factors in a Brazilian community. Parasitology 138, 1406–1416.CrossRefGoogle Scholar
Eaton, A. D. and Franson, M. A. H. (2005). American Public Health Association, American Water Works Association and Water Environment Federation. Standard Methods for the Examination of Water and Wastewate. American Public Health Association, Washington, DC.Google Scholar
Fan, C. K. and Su, K. E. (2004). Cross-reactions with Ascaris suum antigens of sera from mice infected with A. suum, Toxocara canis, and Angiostrongylus cantonensis . Parasitology International 53, 263–271.Google Scholar
Filmer, D. and Pritchett, L. H. (2001). Estimating wealth effects without expenditure data—or tears: an application to educational enrollments in states of India. Demography 38, 115–132.Google Scholar
Fonseca, E. O., Teixeira, M. G., Barreto, M. L., Carmo, E. H. and Costa Mda, C. (2010). Prevalence and factors associated with geohelminth infections in children living in municipalities with low HDI in North and Northeast Brazil. (article in Portuguese). Cadernos de Saúde Pública 26, 143–152.Google Scholar
Gaasenbeek, C. P. H. and Borgsteede, F. H. M. (1998). Studies on the survival of Ascaris suum eggs under laboratory and simulated field conditions. Veterinary Parasitology 75, 227–234.CrossRefGoogle ScholarPubMed
Gamboa, M. I., Kozubsky, L. E., Costas, M. E., Garraza, M., Cardozo, M. I., Susevich, M. L., Magistrello, P. N. and Navone, G. T. (2009). Associations between geohelminths and socioenvironmental conditions among different human populations in Argentina. (article in Spanish). Revista Panamericana de Salud Pública 26, 1–8.Google Scholar
Geissler, P. W., Mwaniki, D., Thiong'o, F. and Friis, H. (1998). Geophagy as a risk factor for geohelminth infections: a longitudinal study of Kenyan primary schoolchildren. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 7–1.Google Scholar
Gyorkos, T. W., Kokoskin-Nelson, E., MacLean, J. D. and Soto, J. C. (1994). Parasite contamination of sand and soil from daycare sandboxes and play areas. Canadian Journal of Infectious Diseases 5, 17–20.Google Scholar
Hall, A., Hewitt, G., Tuffrey, V. and de Silva, N. (2008). A review and meta-analysis of the impact of intestinal worms on child growth and nutrition. Maternal and Child Nutrition 4, 118–236.Google Scholar
Hominick, W. M., Dean, C. G. and Schad, G. A. (1987). Population biology of hookworms in west Bengal: analysis of numbers of infective larvae recovered from damp pads applied to the soil surface at defaecation sites. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 978–986.Google Scholar
INEC (2014). Meteorología: año 2012. Instituto Nacional de Estadísticas y Censo, Contraloría General de la República de Panamá. http://www.contraloria.gob.pa/INEC/Publicaciones/Publicaciones.aspx?ID_SUBCATEGORIA=4&ID_PUBLICACION=583&ID_IDIOMA=1&ID_CATEGORIA=2. Viewed on July 15 2015.Google Scholar
Kattula, D., Sarkar, R., Ajjampur, S. S. R., Minz, S., Levecke, B., Muliyil, J. and Kang, G. (2014). Prevalence and risk factors for soil transmitted helminth infection among school children in south India. Indian Journal of Medical Research 139, 76–82.Google ScholarPubMed
Kirwan, P., Asaolu, S. O., Abiona, T. C., Jackson, A. L., Smith, H. V. and Holland, C. V. (2009). Soil-transmitted helminth infections in Nigerian children aged 0–25 months. Journal of Helminthology 83, 261–266.Google Scholar
Maikai, B., Umoh, J., Ajanusi, O. and Ajogi, I. (2008). Public health implications of soil contaminated with helminth eggs in the metropolis of Kaduna, Nigeria. Journal of Helminthology 82, 113–118.Google Scholar
Mizgajska, H. (1993). The distribution and survival of eggs of Ascaris suum in six different natural soil profiles. Acta Parasitologica 38, 170–174.Google Scholar
Mohd Zain, S. N., Rahman, R. and Lewis, J. W. (2014). Stray animal and human defecation as sources of soil-transmitted helminths in playgrounds around Peninsular Malaysia. Journal of Helminthology 1–8 (Epub ahead of print) doi:10.1017/S0022149X14000716.Google Scholar
Muñoz-Antoli, C., Pavón, A., Marcilla, A., Toledo, R. and Esteban, J. G. (2014). Prevalence and risk factors related to intestinal parasites among children in Department of Rio San Juan, Nicaragua. Transactions of the Royal Society of Tropical Medicine and Hygiene 108, 774–782.CrossRefGoogle Scholar
Nicholas, W. L., Stewart, A. C. and Mitchell, G. F. (1984). Antibody responses to Toxocara canis using sera from parasite-infected mice and protection from toxocariasis by immunisation with ES antigens. Australian Journal of Experimental Biology and Medical Science 62, 619–626.Google Scholar
Nishiura, H., Imai, H., Nakao, H., Tsukino, H., Changazi, M. A., Hussain, G. A., Kuroda, Y. and Katoh, T. (2002). Ascaris lumbricoides among children in rural communities in the Northern Area, Pakistan: prevalence, intensity, and associated socio-cultural and behavioral risk factors. Acta Tropica 83, 223–231.Google Scholar
Olsen, A., Permin, A. and Roepstorff, A. (2001). Chickens and pigs as transport hosts for Ascaris, Trichuris and Oesophagostomum eggs. Parasitology 123, 325–330.Google Scholar
Oluwole, A. S., Ekpo, U. F., Karagiannis-Voules, D. A., Abe, E. M., Olamiju, F. O., Isiyaku, S., Okoronkwo, C., Saka, Y., Nebe, O. J., Braide, E. I., Mafiana, C. F., Utzinger, J. and Vounatsou, P. (2015). Bayesian geostatistical model-based estimates of soil-transmitted helminth infection in Nigeria, including annual deworming requirements. PLoS Neglected Tropical Diseases 9, e0003740.Google Scholar
Peng, W. D., Zhou, X. M., Cui, X. M., Crompton, D. W. T., Whitehead, R. R., Xiong, J. Q., Wu, H. G., Peng, J. Y., Yang, Y., Wu, W. X., Xu, K. W. and Yan, Y. X. B. (1996). Ascaris, people and pigs in a rural community of Jiangxi Province, China. Parasitology 113, 545–557.Google Scholar
Quihui, L., Valencia, M. E., Crompton, D. W. T., Phillips, S., Hagan, P., Morales, G. and Díaz-Camacho, S. P. (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.Google Scholar
Quintero, K., Durán, C., Duri, D., Medina, F., Garcia, J., Hidalgo, G., Nakal, S., Echeverria-Ortega, M., Albano, C. and Incani, R. N. (2012). Household social determinants of ascariasis and trichuriasis in North Central Venezuela. International Health 4, 103–110.Google Scholar
Saathoff, E., Olsen, A., Kvalsvig, J. D., Appleton, C. C., Sharp, B. and Kleinschmidt, I. (2005 a). Ecological covariates of Ascaris lumbricoides infection in schoolchildren from rural KwaZulu-Natal, South Africa. Tropical Medicine and International Health 10, 412–422.Google Scholar
Saathoff, E., Olsen, A., Sharp, B., Kvalsvig, J. D., Appleton, C. C. and Kleinschmidt, I. (2005 b). Ecologic covariates of hookworm infection and reinfection in rural Kwazulu-natal/South Africa: a geographic information system-based study. American Journal of Tropical Medicine and Hygiene 72, 384–391.Google Scholar
Schmidlin, T., Hürlimann, E., Silué, K. D., Yapi, R. B., Houngbedji, C., Kouadio, B. A., Acka-Douabélé, C. A., Kouassi, D., Ouattara, M., Zouzou, F., Bonfoh, B., N'Goran, E. K., Utzinger, J. and Raso, G. (2013). Effects of hygiene and defecation behavior on helminths and intestinal protozoa infections in Taabo, Côte d'Ivoire. PLoS ONE 8, e65722.CrossRefGoogle ScholarPubMed
Schüle, S. A., Clowes, P., Kroidl, I., Kowuor, D. O., Nsojo, A., Mangu, C., Riess, H., Geldmacher, C., Laubender, R. P., Mhina, S., Maboko, L., Löscher, T., Hoelscher, M. and Saathoff, E. (2014). Ascaris lumbricoides infection and its relation to environmental factors in the Mbeya region of Tanzania, a cross-sectional, population-based study. PLoS ONE 9, e92032.Google Scholar
Shalaby, H. A., Abdel-Shafy, S. and Derbala, A. A. (2010). The role of dogs in transmission of Ascaris lumbricoides for humans. Parasitology Research 106, 1021–1026.Google Scholar
Simpson, E. J., Mull, D., Longley, E. and East, J. (2000). Pica during pregnancy in low-income women born in Mexico. Western Journal of Medicine 173, 20–24.Google Scholar
Smith, G. (1990). The ecology of the free-living stages: a reappraisal. In Hookworm Disease: Current Status and New Directions (ed. Schad, G. A. and Warren, K. S.), pp. 89–104. Taylor & Francis, London, UK.Google Scholar
Steinmann, P., Usubalieva, J., Imanalieva, C., Minbaeva, G., Stefiuk, K., Jeandron, A. and Utzinger, J. (2010). Rapid appraisal of human intestinal helminth infections among schoolchildren in Osh oblast, Kyrgyzstan. Acta Tropica 116, 178–184.CrossRefGoogle ScholarPubMed
Strunz, E. C., Addiss, D. G., Stocks, M. E., Ogden, S., Utzinger, J. and Freeman, M. C. (2014). Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Medicine 11, e1001620.Google Scholar
Tomczyk, S., Deribe, K., Brooker, S. J., Clark, H., Rafique, K., Knopp, S., Utzinger, J. and Davey, G. (2014). Association between footwear use and neglected tropical diseases: a systematic review and meta-analysis. PLoS Neglected Tropical Diseases 8, e3285.Google Scholar
Traub, R. J., Robertson, I. D., Irwin, P., Mencke, N. and Thompson, R. C. A. (2002). The role of dogs in transmission of gastrointestinal parasites in a remote tea-growing community in northeastern India. American Journal of Tropical Medicine and Hygiene 67, 539–545.Google Scholar
Udonsi, J. K. and Atata, G. (1987). Necator americanus: temperature, pH, light, and larval development, longevity, and desiccation tolerance. Experimental Parasitology 63, 136–142.Google Scholar
Utzinger, J., Rinaldi, L., Lohourignon, L. K., Rohner, F., Zimmermann, M. B., Tschannen, A. B., N'Goran, E. K. and Cringoli, G. (2008). FLOTAC: a new sensitive technique for the diagnosis of hookworm infections in humans. Transactions of the Royal Society of Tropical Medicine and Hygiene 102, 84–90.CrossRefGoogle ScholarPubMed
Vyas, S. and Kumaranayake, L. (2006). Constructing socio-economic status indices: how to use principal components analysis. Health Policy and Planning 21, 459–468.Google Scholar
Wang, X., Zhang, L., Luo, R., Wang, G., Chen, Y., Medina, A., Eggleston, K., Rozelle, S. and Smith, D. S. (2012). Soil-transmitted helminth infections and correlated risk factors in preschool and school-aged children in rural Southwest China. PLoS ONE 7, e45939.Google Scholar
World Health Organization (1996). Fact sheet 3·4. Simple pit latrines. In Fact Sheets on Environmental Sanitation. 328 pp. http://helid.digicollection.org/en/d/Js13461e/3.4.html. Viewed on May 28 2015.Google Scholar
World Health Organization (2006). Preventive Chemotherapy in Human Helminthiasis. Coordinated Use of Anthelminthic Drugs in Control Interventions: a Manual for Health Professionals and Programme Managers. World Health Organization, Geneva, Switzerland.Google Scholar
Zhou, C., Li, M., Yuan, K., Deng, S. and Peng, W. (2012). Pig Ascaris: an important source of human ascariasis in China. Infection, Genetics and Evolution 12, 1172–1177.Google Scholar
Ziegelbauer, K., Speich, B., Mausezahl, D., Bos, R., Keiser, J. and Utzinger, J. (2012). Effect of sanitation on soil-transmitted helminth infection: systematic review and meta-analysis. PLoS Medicine 9, e1001162.Google Scholar