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Ascaris and hookworm transmission in preschool children in rural Panama: role of subsistence agricultural activities

Published online by Cambridge University Press:  22 March 2016

RACHEL J. KRAUSE ,
KRISTINE G. KOSKI ,
EMÉRITA PONS ,
ODALIS SINISTERRA  and
MARILYN E. SCOTT
RACHEL J. KRAUSE*
Affiliation:
Department of Biology, Canadian Mennonite University, Winnipeg, Manitoba, Canada
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
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, Ste-Anne de Bellevue, Quebec, Canada
*
*Corresponding author: Department of Biology, Canadian Mennonite University, 500 Shaftesbury Blvd., Winnipeg, Manitoba R3P 2N2, Canada. E-mail: rkrause@cmu.ca
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Summary

This longitudinal study explored whether aspects of subsistence agriculture were associated with presence and intensity of Ascaris and hookworm in preschool children in rural Panama. Questionnaires were used to collect data on household socio-demographics, child exposure to agriculture and household agricultural practices. Stool samples were collected from children (6 months–5 years) at 3 time points, with albendazole administered after each to clear infections, resulting in 1 baseline and 2 reinfection measures. A novel Agricultural Activity Index (AAI) was developed using principal components analysis to measure the intensity of household agricultural practices. Zero-inflated negative binomial regression models revealed baseline hookworm egg counts were higher if children went to the agricultural plot and if the plot was smaller. Baseline and reinfection Ascaris egg counts were higher if children went to the plot and households had higher AAI, and higher at baseline if the plot was smaller. Caregiver time in the plot was negatively associated with baseline Ascaris egg counts, but positively associated with baseline hookworm and Ascaris reinfection egg counts. Children who spent more time playing around the home were less likely to be infected with Ascaris at baseline. We conclude that preschool child exposure to subsistence agriculture increased Ascaris and hookworm intensity.

Keywords

soil-transmitted helminthsAscarishookwormsubsistence agricultureAgricultural Activity IndexVERASANagricultural plot sizecaregiver work
Type
Research Article
Information
Parasitology , Volume 143 , Issue 8 , July 2016 , pp. 1043 - 1054
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Adegnika, A. A., Zinsou, J. F., Issifou, S., Ateba-Ngoa, U., Kassa, R. F., Feugap, E. N., Honkpehedji, Y. J., Agobe, J.-C. D., Kenguele, H. M. and Massinga-Loembe, M. (2014). Randomized, controlled, assessor-blind clinical trial to assess the efficacy of single versus repeated-dose albendazole to treat Ascaris lumbricoides, Trichuris trichiura, and hookworm infection. Antimicrobial Agents and Chemotherapy 58, 2535–2540.CrossRefGoogle ScholarPubMed
Adenusi, A. A., Abimbola, W. A. and Adewoga, T. O. S. (2015). Human intestinal helminth contamination in pre-washed, fresh vegetables for sale in major markets in Ogun State, southwest Nigeria. Food Control 50, 843–849.CrossRefGoogle Scholar
Al-Mekhlafi, M. H., Surin, J., Atiya, A., Ariffin, W., Mahdy, A. M. and Abdullah, H. C. (2008). Pattern and predictors of soil-transmitted helminth reinfection among aboriginal schoolchildren in rural Peninsular Malaysia. Acta Tropica 107, 200–204.CrossRefGoogle Scholar
Amoah, P., Drechsel, P. and Abaidoo, R. (2005). Irrigated urban vegetable production in Ghana: sources of pathogen contamination and health risk elimination. Irrigation and Drainage 54, S49–S61.CrossRefGoogle Scholar
Asaolu, S., Ofoezie, I., Odumuyiwa, P., Sowemimo, O. and Ogunniyi, T. (2002). Effect of water supply and sanitation on the prevalence and intensity of Ascaris lumbricoides among pre-school-age children in Ajebandele and Ifewara, Osun State, Nigeria. Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 600–604.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.CrossRefGoogle Scholar
Bethony, J., Brooker, S., Albonico, M., Geiger, S. M., Loukas, A., Diemert, D. and Hotez, P. J. (2006). Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. The Lancet 367, 1521–1532.CrossRefGoogle ScholarPubMed
Byerlee, D. (2009). Agriculture for development: toward a new paradigm. Annual Review of Resource Economics 1, 15–31.CrossRefGoogle Scholar
Cairncross, S., Blumenthal, U., Kolsky, P., Moraes, L. and Tayeh, A. (1996). The public and domestic domains in the transmission of disease. Tropical Medicine and International Health 1, 27–34.CrossRefGoogle ScholarPubMed
Chan, M.-S. (1997). The global burden of intestinal nematode infections – fifty years on. Parasitology Today 13, 438–443.CrossRefGoogle Scholar
Chipeta, M. G., Ngwira, B. M., Simoonga, C. and Kazembe, L. N. (2014). Zero adjusted models with applications to analysing helminths count data. BMC Research Notes 7, 856.CrossRefGoogle ScholarPubMed
Cobayashi, F., Augusto, R. A., Lourenco, B. H., Muniz, P. T. and Cardoso, M. A. (2014). Factors associated with stunting and overweight in Amazonian children: a population-based, cross-sectional study. Public Health Nutrition 17, 551–560.CrossRefGoogle ScholarPubMed
Corsini, E., Liesivuori, J., Vergieva, T., Van Loveren, H. and Colosio, C. (2008). Effects of pesticide exposure on the human immune system. Human & Experimental Toxicology 27, 671–680.CrossRefGoogle ScholarPubMed
Crompton, D. and Nesheim, M. (2002). Nutritional impact of intestinal helminthiasis during the human life cycle. Annual Review of Nutrition 22, 35–59.CrossRefGoogle ScholarPubMed
Cundill, B., Alexander, N., Bethony, J. M., Diemert, D., Pullan, R. L. and Brooker, S. (2011). 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
Drake, L., Jukes, M., Sternberg, R. and Bundy, D. (2000). Geohelminth infections (ascariasis, trichuriasis, and hookworm): cognitive and developmental impacts. Seminars in Pediatric Infectious Diseases 11, 245–251.CrossRefGoogle Scholar
Duramad, P., Harley, K., Lipsett, M., Bradman, A., Eskenazi, B., Holland, N. T. and Tager, I. B. (2006). Early environmental exposures and intracellular Th1/Th2 cytokine profiles in 24-month-old children living in an agricultural area. Environmental Health Perspectives 114, 1916–1922.CrossRefGoogle Scholar
Ensink, J. H. J., van der Hoek, W., Mukhtar, M., Tahir, Z. and Amerasinghe, F. P. (2005). High risk of hookworm infection among wastewater farmers in Pakistan. Transactions of the Royal Society of Tropical Medicine and Hygiene 99, 809–818.CrossRefGoogle ScholarPubMed
Faber, M., Phungula, M. A., Venter, S. L., Dhansay, M. A. and Benadé, A. S. (2002). Home gardens focusing on the production of yellow and dark-green leafy vegetables increase the serum retinol concentrations of 2–5-y-old children in South Africa. The American Journal of Clinical Nutrition 76, 1048–1054.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Freeman, M. C., Clasen, T., Brooker, S. J., Akoko, D. O. and Rheingans, R. (2013). The impact of a school-based hygiene, water quality and sanitation intervention on soil-transmitted helminth reinfection: a cluster-randomized trial. The American Journal of Tropical Medicine and Hygiene 89, 875–883.CrossRefGoogle ScholarPubMed
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
Gazzinelli, A., Correa-Oliveira, R., Yang, G.-J., Boatin, B. A. and Kloos, H. (2012). A research agenda for helminth diseases of humans: social ecology, environmental determinants, and health systems. PLoS Neglected Tropical Diseases 6, e1603.CrossRefGoogle ScholarPubMed
Gunawardena, G., Karunaweera, N. and Ismail, M. (2004). Wet-days: are they better indicators of Ascaris infection levels? Journal of Helminthology 78, 305–310.CrossRefGoogle ScholarPubMed
Gyorkos, T. W., Maheu-Giroux, M., Casapia, M., Joseph, S. A. and Creed-Kanashiro, H. (2011). Stunting and helminth infection in early preschool-age children in a resource-poor community in the Amazon lowlands of Peru. Transactions of the Royal Society of Tropical Medicine and Hygiene 105, 204–208.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Halpenny, C. M., Paller, C., Koski, K. G., Valdes, V. E. and Scott, M. E. (2013). Regional, household and individual factors that influence soil transmitted helminth reinfection dynamics in preschool children from rural indigenous Panama. PLoS Neglected Tropical Diseases 7, 11.CrossRefGoogle ScholarPubMed
Haswell-Elkins, M., Elkins, D. and Anderson, R. M. (1989). The influence of individual, social group and household factors on the distribution of Ascaris lumbricoides within a community and implications for control strategies. Parasitology 98, 125–134.CrossRefGoogle ScholarPubMed
Holland, C. V., Taren, D. L., Crompton, D. W. T., Nesheim, M. C., Sanjur, D., Barbeau, I., Tucker, K., Tiffanfy, J. and Rivera, G. (1988). Intestinal helminthiases in relation to the socioeconomic environment of Panamanian children. Social Science & Medicine 26, 209–213.CrossRefGoogle Scholar
Hotez, P. J., Fenwick, A., Savioli, L. and Molyneux, D. H. (2009). Rescuing the bottom billion through control of neglected tropical diseases. The Lancet 373, 1570–1575.CrossRefGoogle ScholarPubMed
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
Jones, A. D., Cruz Agudo, Y., Galway, L., Bentley, J. and Pinstrup-Andersen, P. (2012). Heavy agricultural workloads and low crop diversity are strong barriers to improving child feeding practices in the Bolivian Andes. Social Science & Medicine 75, 1673–1684.CrossRefGoogle ScholarPubMed
Keiser, J., Ingram, K. and Utzinger, J. (2011). Antiparasitic drugs for paediatrics: systematic review, formulations, pharmacokinetics, safety, efficacy and implications for control. Parasitology 138, 1620–1632.CrossRefGoogle ScholarPubMed
Kightlinger, L. K., Seed, J. R. and Kightlinger, M. B. (1998). Ascaris lumbricoides intensity in relation to environmental, socioeconomic, and behavioral determinants of exposure to infection in children from southeast Madagascar. The Journal of Parasitology 84, 480–484.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Kounnavong, S., Vonglokham, M., Houamboun, K., Odermatt, P. and Boupha, B. (2011). Soil-transmitted helminth infections and risk factors in preschool children in southern rural Lao People's Democratic Republic. Transactions of the Royal Society of Tropical Medicine and Hygiene 105, 160–166.CrossRefGoogle ScholarPubMed
Krause, R. J., Koski, K. G., Pons, E., Sandoval, N., Sinisterra, O. and Scott, M. E. (2015). Ascaris and hookworm transmission in preschool children from rural Panama: role of yard environment, soil eggs/larvae, and hygiene and play behaviours. Parasitology 142, 1543–1554.CrossRefGoogle ScholarPubMed
Levecke, B., Anderson, R. M., Berkvens, D., Charlier, J., Devleesschauwer, B., Speybroeck, N., Vercruysse, J. and Van Aelst, S. (2015). Mathematical inference on helminth egg counts in stool and its applications in mass drug administration programmes to control soil-transmitted helminthiasis in public health. Advances in Parasitology 87, 193–247.CrossRefGoogle ScholarPubMed
Low, J. W., Arimond, M., Osman, N., Cunguara, B., Zano, F. and Tschirley, D. (2007). A food-based approach introducing orange-fleshed sweet potatoes increased vitamin A intake and serum retinol concentrations in young children in rural Mozambique. The Journal of Nutrition 137, 1320–1327.CrossRefGoogle ScholarPubMed
Magalhaes, R. J. S., Biritwum, N. K., Gyapong, J. O., Brooker, S., Zhang, Y. B., Blair, L., Fenwick, A. and Clements, A. C. A. (2011). Mapping helminth co-infection and co-intensity: geostatistical prediction in Ghana. PLoS Neglected Tropical Diseases 5, 13.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.CrossRefGoogle ScholarPubMed
Matthys, B., Tschannen, A. B., Tian-Bi, N. T., Comoé, H., Diabaté, S., Traoré, M., Vounatsou, P., Raso, G., Gosoniu, L. and Tanner, M. (2007). Risk factors for Schistosoma mansoni and hookworm in urban farming communities in western Côte d'Ivoire. Tropical Medicine & International Health 12, 709–723.CrossRefGoogle ScholarPubMed
Menzies, S. K., Rodriguez, A., Chico, M., Sandoval, C., Broncano, N., Guadalupe, I. and Cooper, P. J. (2014). Risk factors for soil-transmitted helminth infections during the first 3 years of life in the tropics; findings from a birth cohort. PLoS Neglected Tropical Diseases 8, e2718.CrossRefGoogle ScholarPubMed
Mihrshahi, S., Casey, G. J., Montresor, A., Phuc, T. Q., Thach, D. T. C., Tien, N. T. and Biggs, B. A. (2009). The effectiveness of 4 monthly albendazole treatment in the reduction of soil-transmitted helminth infections in women of reproductive age in Viet Nam. International Journal for Parasitology 39, 1037–1043.CrossRefGoogle ScholarPubMed
Mueller, I., Vounatsou, P., Smith, T. and Allen, B. (2001). Subsistence agriculture and child growth in Papua New Guinea. Ecology of Food and Nutrition 40, 367–395.CrossRefGoogle Scholar
Mun, S., Cho, S.-H., Kim, T.-S., Oh, B.-T. and Yoon, J. (2009). Inactivation of Ascaris eggs in soil by microwave treatment compared to UV and ozone treatment. Chemosphere 77, 285–290.CrossRefGoogle ScholarPubMed
Needham, C., Kim, H. T., Hoa, N. V., Cong, L. D., Michael, E., Drake, L., Hall, A. and Bundy, D. A. (1998). Epidemiology of soil-transmitted nematode infections in Ha Nam Province, Vietnam. Tropical Medicine and International Health 3, 904–912.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Orozco, F., Cole, D., Muñoz, V., Altamirano, A., Wanigaratne, S., Espinosa, P. and Muñoz, F. (2007). Relationships among production systems, preschool nutritional status, and pesticide-related toxicity in seven Ecuadorian communities: a multi-case study approach. Food and Nutrition Bulletin 28, 247S–257S.CrossRefGoogle ScholarPubMed
Östan, İ., Kilimcioğlu, A. A., Girginkardeşler, N., Özyurt, B. C., Limoncu, M. E. and Ok, Ü. Z. (2007). Health inequities: lower socio-economic conditions and higher incidences of intestinal parasites. BMC Public Health 7, 342.CrossRefGoogle ScholarPubMed
Payne, L., Koski, K., Ortega-Barria, E. and Scott, M. (2007). Benefit of vitamin A supplementation on Ascaris reinfection is less evident in stunted children. Journal of Nutrition 137, 1455–1459.CrossRefGoogle ScholarPubMed
Peng, W. and Criscione, C. D. (2012). Ascariasis in people and pigs: new inferences from DNA analysis of worm populations. Infection, Genetics and Evolution 12, 227–235.CrossRefGoogle ScholarPubMed
Pichon, F. and Uquillas, J. (1997). Agricultural intensification and poverty reduction in Latin America's risk-prone areas: opportunities and challenges. The Journal of Developing Areas 31, 479–514.Google Scholar
Pullan, R. L., Kabatereine, N. B., Quinnell, R. J. and Brooker, S. (2010). Spatial and genetic epidemiology of hookworm in a rural community in Uganda. PLoS Neglected Tropical Diseases 4, e713.CrossRefGoogle Scholar
Pullan, R. L., Smith, J. L., Jasrasaria, R. and Brooker, S. J. (2014). Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasites & Vectors 7, 37.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Rose, D. D. (2008). Interventions to reduce household food insecurity: a synthesis of current concepts and approaches for Latin America. Revista De Nutricao-Brazilian Journal of Nutrition 21, 159–173.CrossRefGoogle Scholar
Siwila, J., Phiri, I. G., Enemark, H. L., Nchito, M. and Olsen, A. (2010). Intestinal helminths and protozoa in children in pre-schools in Kafue district, Zambia. Transactions of the Royal Society of Tropical Medicine and Hygiene 104, 122–128.CrossRefGoogle 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
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.CrossRefGoogle ScholarPubMed
Udonsi, J. K. and Atata, G. (1987). Necator americanus: temperature, pH, light, and larval development, longevity, and desiccation tolerance. Experimental Parasitology 63, 136–142.CrossRefGoogle ScholarPubMed
Ugbomoiko, U., Dalumo, V., Ofoezie, I. and Obiezue, R. (2009). Socio-environmental factors and ascariasis infection among school-aged children in Ilobu, Osun State, Nigeria. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 223–228.CrossRefGoogle ScholarPubMed
Ulukanligil, M. and Seyrek, A. (2004). Demographic and socio-economic factors affecting the physical development, haemoglobin and parasitic infection status of schoolchildren in Sanliurfa province, Turkey. Public Health 118, 151–158.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Walker, M., Hall, A., Anderson, R. M. and Basanez, M. G. (2009). Density-dependent effects on the weight of female Ascaris lumbricoides infections of humans and its impact on patterns of egg production. Parasites & Vectors 2, 18.CrossRefGoogle ScholarPubMed
Walker, M., Hall, A., and Basanez, M. G. (2011). Individual predisposition, household clustering and risk factors for human infection with Ascaris lumbricoides: new epidmiological insights. PLoS Neglected Tropical Diseases 5, e1047.CrossRefGoogle 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 ScholarPubMed
WHO (2002). Prevention and Control of Schistosomiasis and Soil-transmitted Helminthiasis. World Health Organization, Geneva, Switzerland.Google Scholar
WHO (2007). Action Against Worms. World Health Organization, Geneva, Switzerland.Google Scholar
Wong, H. J., Moy, F. M. and Nair, S. (2014). Risk factors of malnutrition among preschool children in Terengganu, Malaysia: a case control study. BMC Public Health 14, 785.CrossRefGoogle ScholarPubMed
Yu, S.-H. and Shen, W.-X. (1990). Hookworm infection and disease in China. In Hookworm Disease: Current Status and New Directions (ed. Schad, G. A. and Warren, K. S.), pp. 44–54. Taylor & Francis, London, UK.Google Scholar