• 1.

    Lai Y-S, Biedermann P, Shrestha A, Chammartin F, à Porta N, Montresor A, Mistry NF, Utzinger J, Vounatsou P, 2019. Risk profiling of soil-transmitted helminth infection and estimated number of infected people in South Asia: a systematic review and Bayesian geostatistical analysis. PLoS Negl Trop Dis 13: e0007580.

    • Search Google Scholar
    • Export Citation
  • 2.

    Jourdan PM, Lamberton PHL, Fenwick A, Addiss DG, 2018. Soil-transmitted helminth infections. Lancet 391: 252265.

  • 3.

    Strunz EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, Freeman MC, 2014. Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Med 11: e1001620.

    • Search Google Scholar
    • Export Citation
  • 4.

    World Health Organization, 2017. Guideline: Preventive Chemotherapy to Control Soil-transmitted Helminth Infections in At-risk Population Groups. Geneva, Switzerland: WHO.

  • 5.

    Press Information Bureau Government of India, 2019. Health Ministry Conducts 8th Round of National Deworming Day (NDD) Campaign. Available at: https://pib.gov.in/Pressreleaseshare.aspx?PRID=1563589. Accessed March 28, 2021.

    • Search Google Scholar
    • Export Citation
  • 6.

    Kaliappan SP 2013. Prevalence and clustering of soil‐transmitted helminth infections in a tribal area in southern India. Trop Med Int Health 18: 14521462.

    • Search Google Scholar
    • Export Citation
  • 7.

    Ganguly S 2017. High prevalence of soil-transmitted helminth infections among primary school children, Uttar Pradesh, India, 2015. Infect Dis Poverty 6: 139.

    • Search Google Scholar
    • Export Citation
  • 8.

    Traub RJ, Robertson ID, Irwin P, Mencke N, Thompson RCA, 2002. The role of dogs in transmission of gastrointestinal parasites in a remote tea-growing community in northeastern India. Am J Trop Med Hyg 67: 539545.

    • Search Google Scholar
    • Export Citation
  • 9.

    Traub RJ, Robertson ID, Irwin P, Mencke N, Monis P, Thompson RCA, 2003. Humans, dogs and parasitic zoonoses—unravelling the relationships in a remote endemic community in northeast India using molecular tools. Parasitol Res 90: S156S157.

    • Search Google Scholar
    • Export Citation
  • 10.

    Panigrahi PN, Gupta AR, Behera SK, Panda BSK, Patra RC, Mohanty BN, Sahoo GR, 2014. Evaluation of gastrointestinal helminths in canine population of Bhubaneswar, Odisha, India: a public health appraisal. Vet World 7: 295.

    • Search Google Scholar
    • Export Citation
  • 11.

    Traub RJ, Robertson ID, Irwin PJ, Mencke N, Thompson RCAA, 2005. Canine gastrointestinal parasitic zoonoses in India. Trends Parasitol 21: 4248.

  • 12.

    Biswal DK, Debnath M, Kharumnuid G, Thongnibah W, Tandon V, 2016. Northeast India Helminth Parasite Information Database (NEIHPID): knowledge base for helminth parasites. PLoS One 11: e0157459.

    • Search Google Scholar
    • Export Citation
  • 13.

    Borkataki S, Islam S, Borkakati MR, Goswami P, Deka DK, 2012. Prevalence of porcine cysticercosis in Nagaon, Morigaon and Karbianglong district of Assam, India. Vet World 5: 86.

    • Search Google Scholar
    • Export Citation
  • 14.

    Kaur M, Singh BB, Sharma R, Gill JPS, 2016. Pervasive environmental contamination with human feces results in high prevalence of zoonotic Sarcocystis infection in pigs in the Punjab, India. J Parasitol 102: 229232.

    • Search Google Scholar
    • Export Citation
  • 15.

    Sadaow L 2018. Molecular identification of Ascaris lumbricoides and Ascaris suum recovered from humans and pigs in Thailand, Lao PDR, and Myanmar. Parasitol Res 117: 24272436.

    • Search Google Scholar
    • Export Citation
  • 16.

    George S, Kaliappan SP, Kattula D, Roy S, Geldhof P, Kang G, Vercruysse J, Levecke B, 2015. Identification of Ancylostoma ceylanicum in children from a tribal community in Tamil Nadu, India using a semi-nested PCR-RFLP tool. Trans R Soc Trop Med Hyg 109: 283285.

    • Search Google Scholar
    • Export Citation
  • 17.

    Inpankaew T 2014. High prevalence of Ancylostoma ceylanicum hookworm infections in humans, Cambodia, 2012. Emerg Infect Dis 20: 976982.

  • 18.

    Ngui R, Lim YAL, Traub R, Mahmud R, Mistam MS, 2012. Epidemiological and genetic data supporting the transmission of Ancylostoma ceylanicum among human and domestic animals. PLoS Negl Trop Dis 6: e1522.

    • Search Google Scholar
    • Export Citation
  • 19.

    Prendergast AJ 2019. Putting the “A” into WaSH: a call for integrated management of water, animals, sanitation, and hygiene. Lancet Planet Health 3: e336e337.

    • Search Google Scholar
    • Export Citation
  • 20.

    Berendes DM, Yang PJ, Lai A, Hu D, Brown J, 2018. Estimation of global recoverable human and animal faecal biomass. Nat Sustain 1: 679685.

  • 21.

    Matilla F, Velleman Y, Harrison W, Nevel M, 2018. Animal influence on water, sanitation and hygiene measures for zoonosis control at the household level: a systematic literature review. PLoS Negl Trop Dis 12: e0006619.

    • Search Google Scholar
    • Export Citation
  • 22.

    Penakalapati G, Swarthout J, Delahoy MJ, McAliley L, Wodnik B, Levy K, Freeman MC, 2017. Exposure to animal feces and human health: a systematic review and proposed research priorities. Environ Sci Technol 51: 1153711552.

    • Search Google Scholar
    • Export Citation
  • 23.

    Asbjornsdottir KH 2018. Assessing the feasibility of interrupting the transmission of soil-transmitted helminths through mass drug administration: the DeWorm3 cluster randomized trial protocol. PLoS Negl Trop Dis 12: e0006166.

    • Search Google Scholar
    • Export Citation
  • 24.

    Clarke NE, Clements ACA, Doi SA, Wang D, Campbell SJ, Gray D, Nery SV, 2017. Differential effect of mass deworming and targeted deworming for soil-transmitted helminth control in children: a systematic review and meta-analysis. Lancet 389: 287297.

    • Search Google Scholar
    • Export Citation
  • 25.

    Clarke NE, Clements ACA, Bryan S, McGown J, Gray D, Nery SV, 2016. Investigating the differential impact of school and community-based integrated control programmes for soil-transmitted helminths in Timor-Leste: the (S)WASH-D for Worms pilot study protocol. Pilot Feasibility Stud 2: 69.

    • Search Google Scholar
    • Export Citation
  • 26.

    Coffeng LE 2019. Impact of different sampling schemes for decision making in soil-transmitted Helminthiasis control programs. J Infect Dis 221 (Supp 5): S531S538.

    • Search Google Scholar
    • Export Citation
  • 27.

    George S, Levecke B, Kattula D, Velusamy V, Roy S, Geldhof P, Sarkar R, Kang G, 2016. Molecular identification of hookworm isolates in humans, dogs and soil in a tribal area in Tamil Nadu, India. PLoS Negl Trop Dis 10: e0004891.

    • Search Google Scholar
    • Export Citation
  • 28.

    Office of the Registrar General & Census Commissioner, 2011. C.D. Block Wise Primary Census Abstract Data (PCA). Tamil Nadu, India: author.

  • 29.

    Sack A, Daramragchaa U, Chuluunbaatar M, Gonchigoo B, Gray GC, 2018. Potential risk factors for zoonotic disease transmission among Mongolian herder households caring for horses and camels. Pastoralism 8: 2.

    • Search Google Scholar
    • Export Citation
  • 30.

    Utzinger J, Becker SL, van Lieshout L, van Dam GJ, Knopp S, 2015. New diagnostic tools in schistosomiasis. Clin Microbiol Infect 21: 529542.

  • 31.

    Levecke B 2011. A comparison of the sensitivity and fecal egg counts of the McMaster egg counting and Kato-Katz thick smear methods for soil-transmitted helminths (diagnostic methods for soil-transmitted helminths). PLoS Negl Trop Dis 5: e1201.

    • Search Google Scholar
    • Export Citation
  • 32.

    Speich B, Knopp S, Mohammed KA, Khamis IS, Rinaldi L, Cringoli G, Rollinson D, Utzinger J, 2010. Comparative cost assessment of the Kato-Katz and FLOTAC techniques for soil-transmitted helminth diagnosis in epidemiological surveys. Parasit Vectors 3: 71.

    • Search Google Scholar
    • Export Citation
  • 33.

    Tropical Council for Companion Animal Parasites, 2019. Guidelines for the diagnosis, treatment and control of canine endoparasites in the tropics. Available at: https://www.troccap.com/canine-guidelines/. Accessed June 1, 2019.

  • 34.

    Steinbaum L, Kwong LH, Ercumen A, Negash MS, Lovely AJ, Njenga SM, Boehm AB, Pickering AJ, Nelson KL, 2017. Detecting and enumerating soil-transmitted helminth eggs in soil: new method development and results from field testing in Kenya and Bangladesh. PLoS Negl Trop Dis 11: e0005522.

    • Search Google Scholar
    • Export Citation
  • 35.

    Imai K, Keele L, Tingley D, 2010. A general approach to causal mediation analysis. Psychol Methods 15: 309334.

  • 36.

    Tun S, Ithoi I, Mahmud R, Samsudin NI, Kek Heng C, Ling LY, 2015. Detection of helminth eggs and identification of hookworm species in stray cats, dogs and soil from Klang Valley, Malaysia. PLoS One 10: e0142231.

    • Search Google Scholar
    • Export Citation
  • 37.

    Jung B-K, Lee J-Y, Chang T, Song H, Chai J-Y, 2020. Rare case of nteric Ancylostoma caninum hookworm infection, South Korea. Emerg Infect Dis 26: 181.

    • Search Google Scholar
    • Export Citation
  • 38.

    Ngcamphalala PI, Lamb J, Mukaratirwa S, 2019. Molecular identification of hookworm isolates from stray dogs, humans and selected wildlife from South Africa. J Helminthol 94: e39.

    • Search Google Scholar
    • Export Citation
  • 39.

    Conlan JV, Khamlome B, Vongxay K, Elliot A, Pallant L, Sripa B, Blacksell SD, Fenwick S, Thompson RCA, 2012. Soil-transmitted helminthiasis in Laos: a community-wide cross-sectional study of humans and dogs in a mass drug administration environment. Am J Trop Med Hyg 86: 624.

    • Search Google Scholar
    • Export Citation
  • 40.

    Steinbaum L, Njenga SM, Kihara J, Boehm AB, Davis J, Null C, Pickering AJ, 2016. Soil-transmitted helminth eggs are present in soil at multiple locations within households in rural Kenya. PLoS One 11: e0157780.

    • Search Google Scholar
    • Export Citation
  • 41.

    Steinbaum L, Mboya J, Mahoney R, Njenga SM, Null C, Pickering AJ, 2019. Effect of a sanitation intervention on soil-transmitted helminth prevalence and concentration in household soil: a cluster-randomized controlled trial and risk factor analysis. PLoS Negl Trop Dis 13: e0007180.

    • Search Google Scholar
    • Export Citation
  • 42.

    Ekong PS, Juryit R, Dika NM, Nguku P, Musenero M, 2012. Prevalence and risk factors for zoonotic helminth infection among humans and animals—Jos, Nigeria, 2005–2009. Pan Afr Med J 12: 6.

    • Search Google Scholar
    • Export Citation
  • 43.

    Robinson MW, Dalton JP, 2009. Zoonotic helminth infections with particular emphasis on fasciolosis and other trematodiases. Philos Trans R Soc Lond B Biol Sci 364: 27632776.

    • Search Google Scholar
    • Export Citation
  • 44.

    Osbjer K, Boqvist S, Sokerya S, Kannarath C, San S, Davun H, Magnusson U, 2015. Household practices related to disease transmission between animals and humans in rural Cambodia. BMC Public Health 15: 476.

    • Search Google Scholar
    • Export Citation
  • 45.

    Brooker S, Clements ACA, Bundy DAP, 2006. Global epidemiology, ecology and control of soil-transmitted helminth infections. Adv Parasitol 62: 221261.

    • Search Google Scholar
    • Export Citation
  • 46.

    Zajac A, 2012. Veterinary Clinical Parasitology. Chichester, West Sussex, United Kingdom: Wiley-Blackwell.

  • 47.

    Velusamy R, Rani N, Ponnudurai G, Anbarasi P, 2015. Prevalence of intestinal and haemoprotozoan parasites of small ruminants in Tamil Nadu, India. Vet World 8: 1205.

    • Search Google Scholar
    • Export Citation
  • 48.

    Brahmbhatt NN, Patel PV, Hasnani JJ, Pandya SS, Joshi BP, 2015. Study on prevalence of ancylostomosis in dogs at Anand district, Gujarat, India. Vet World 8: 14051409.

    • Search Google Scholar
    • Export Citation

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

A One Health Approach to Defining Animal and Human Helminth Exposure Risks in a Tribal Village in Southern India

View More View Less
  • 1 Clinical and Translational Science Graduate Program, Tufts University Graduate School of Biomedical Sciences, Boston, Massachusetts;
  • 2 The Wellcome Trust Research Laboratory, Division of Gastrointestinal Sciences, Christian Medical College, Vellore, Tamil Nadu, India;
  • 3 Department of Community Medicine, Christian Medical College, Vellore, Tamil Nadu, India;
  • 4 Division of Geographic Medicine and Infectious Diseases, Tufts Medical Center, Tufts University School of Medicine, Boston, Massachusetts;
  • 5 Departments of Global Health, Medicine (Infectious Disease), Pediatrics and Epidemiology, University of Washington, Seattle, Washington;
  • 6 The DeWorm3 Project, University of Washington, Seattle, Washington;
  • 7 Faculty of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine, London, United Kingdom

Abstract.

The high burden of soil-transmitted helminth infections has been studied in India; however, little data exist on zoonotic helminths, and on animal-associated exposure to soil-transmitted helminths. Our study took place in the Jawadhu Hills, which is a tribal region in Tamil Nadu, India. Using a One Health approach, we included animal and environmental samples and human risk factors to answer questions about the associations among infected household soil, domestic animals, and human risk factors. Helminth eggs were identified by microscopy in animal and soil samples, and a survey about risk factors was administered to the head of the household. Contact with animals was reported in 71% of households. High levels of helminth infections were found across domestic animal species, especially in goats, chickens, and dogs. Helminth eggs were recorded in 44% of household soil (n = 43/97) and separately in 88% of soil near a water source (n = 28/32). Animal contact was associated with 4.05 higher odds of having helminth eggs in the household soil (P = 0.01), and also having a water source at the household was associated with a 0.33 lower odds of having helminth eggs in the household soil (P = 0.04). Soil moisture was a mediator of this association with a significant indirect effect (P < 0.001). The proportion mediated was 0.50. While our work does not examine transmission, these results support consideration of animal-associated exposure to STH and potentially zoonotic helminths in future interventions to reduce helminth burden. Our study provides support for further investigation of the effects of animals and animal fecal matter on human health.

Author Notes

Address correspondence to Sitara Swarna Rao Ajjampur, Ida Scudder Road, Vellore, Tamil Nadu, India 632004. E-mail: sitararao@cmcvellore.ac.in

Financial support: The project was supported by a TL1 grant to A. S. from the National Center for Advancing Translational Sciences, National Institutes of Health, Award Number UL1TR002544. The content is solely our responsibility and does not necessarily represent the official views of the NIH. The project was also supported by a Fellowship Grant from the Tufts’ Institute of the Environment to A. S. The DeWorm3 study is funded through a grant to the Natural History Museum, London from the Bill and Melinda Gates Foundation (OPP1129535, PI JLW).

Authors’ addresses: Alexandra Sack, Tufts Clinical and Translational Science Institute, Tufts Graduate School of Biomedical Sciences, Boston, MA, E-mail: alexandra.sack@tufts.edu. Gokila Palanisamy, Malathi Manuel, Chinnaduraipandi Paulsamy, Saravanakumar Puthupalayam Kaliappan, and Sitara Swarna Rao Ajjampur, The Wellcome Trust Research Laboratory, Division of Gastrointestinal Sciences, Christian Medical College, Vellore, Tamil Nadu, India, E-mails: gokilap01896@gmail.com, malathimanuel25@gmail.com, chechinnadurai@gmail.com, epipks@gmail.com, and sitararao@cmcvellore.ac.in. Anuradha Rose, Department of Community Medicine, Christian Medical College, Vellore, Tamil Nadu, India, E-mail: anurose@cmcvellore.ac.in. Honorine Ward, Division of Geographic Medicine and Infectious Diseases, Tufts Medical Center, Tufts University School of Medicine, Boston, MA, E-mail: hward@tuftsmedicalcenter.org. Judd L. Walson, Departments of Global Health, Medicine (Infectious Disease), Pediatrics and Epidemiology, University of Washington, Seattle, WA, E-mail: walson@uw.edu. Katherine E. Halliday, Faculty of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine, London, United Kingdom, E-mail: katherine.halliday@lshtm.ac.uk.

Save