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Zoonotic Enteric Parasites in Mongolian People, Animals, and the Environment: Using One Health to Address Shared Pathogens

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Zoonotic Enteric Parasites in Mongolian People, Animals, and the Environment: Using One Health to Address Shared Pathogens RESEARCH ARTICLE Zoonotic enteric parasites in Mongolian people, animals, and the environment: Using One Health to address shared pathogens 1,2,3☯ 1,4☯ 1,5☯ Amber N. BarnesID *, Anu Davaasuren , Uyanga Baasandavga , Paul 2³ 1³ 2,6,7,8³ M. Lantos , Battsetseg Gonchigoo , Gregory C. GrayID 1 Institute of Veterinary Medicine, Ulaanbaatar, Mongolia, 2 School of Medicine, Duke University, Durham, North Carolina, United States of America, 3 Department of Public Health, University of North Florida, Jacksonville, Florida, United States of America, 4 National Center for Communicable Disease, Ulaanbaatar, a1111111111 Mongolia, 5 National Center for Zoonotic Disease, Ulaanbaatar, Mongolia, 6 Duke Global Health Institute, a1111111111 Duke University, Durham, North Carolina, United States of America, 7 Global Health Research Institute, a1111111111 Duke-Kunshan University, Kunshan, Jiangsu, China, 8 Emerging Infectious Diseases Program, Duke-NUS a1111111111 Medical School, Singapore a1111111111 ☯ These authors contributed equally to this work. ³ PML, BC and GCG also contributed equally to this work. * [email protected] OPEN ACCESS Abstract Citation: Barnes AN, Davaasuren A, Baasandavga U, Lantos PM, Gonchigoo B, Gray GC (2021) Zoonotic enteric parasites in Mongolian people, animals, and the environment: Using One Health to Background address shared pathogens. PLoS Negl Trop Dis Cryptosporidium spp. and Giardia duodenalis are important zoonotic enteric pathogens of 15(7): e0009543. https://doi.org/10.1371/journal. pntd.0009543 One Health concern for humans, animals, and the environment. For this study, we investi- gated parasite prevalence and risk factors among rural, peri-urban, and urban households Editor: Matthew C. Freeman, Emory University, UNITED STATES and environments of Mongolia. Received: October 20, 2020 Methods Accepted: June 7, 2021 This cross-sectional study implemented a household risk factor survey at 250 home sites Published: July 8, 2021 along with sample collection from humans, animals, flies, and drinking water. Multiplex real- Copyright: © 2021 Barnes et al. This is an open time PCR analysis was conducted to look for Cryptosporidium spp. and/or Giardia duodena- access article distributed under the terms of the lis within household samples. Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original Results author and source are credited. Lab analysis found one or both zoonotic parasites at 20% of the participating households Data Availability Statement: Data cannot be shared publicly to protect the personal information (51/250). Human samples had a parasite prevalence of 6.4% (27/419), domestic animals at of participants. Data are available from the Duke 3.3% (19/570), pooled filth flies at 14.8% (17/115), and drinking water samples at 2% (5/ University Institutional Review Board 250). Parasite presence at the household was significantly associated with a household's ([email protected]) for researchers use of an improved drinking water source (OR 0.27; CI 0.12±0.61; p = < 0.01), having an who meet the criteria for access to confidential data. indoor handwashing site (OR 0.41; CI 0.19±0.92; p = 0.03), domestic animal ownership (OR 2.40; CI 1.02±5.65; p = 0.05), and rural location (OR 0.50; CI 0.25±0.98; p = 0.04). House- Funding: Funding for this work was provided by the USA National Institutes of Health, Fogarty hold use of an improved drinking water source remained significant in the multivariate model International Center grant, D43TW009373, ªOne (OR 0.16; CI 0.04±0.68; p = 0.01). PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0009543 July 8, 2021 1 / 24 PLOS NEGLECTED TROPICAL DISEASES Zoonotic enteric parasites in Mongolia Health Innovation Fellowships for Zoonotic Disease Conclusion Research in Mongoliaº to GCG (https:// projectreporter.nih.gov/project_info_description. In Mongolia, public and veterinary health are intertwined, particularly for rural herding house- cfm?aid=8743364&icde=17876 817). The funders holds. Increased access to safe water, sanitation and hygiene infrastructure could help pre- had no role in study design, data collection and vent further transmission of zoonotic enteric parasites. Public health interventions, policy analysis, decision to publish, or preparation of the and messaging should utilize a One Health framework employing joint leadership from local manuscript. human and animal health sectors. Competing interests: The authors have declared that no competing interests exist. Author summary The zoonotic enteric parasites of Cryptosporidium spp. and Giardia duodenalis are a One Health concern for human, animal and environmental health. In this study, human, ani- mal, fly, and water samples were collected from 250 households in rural, peri-urban and urban areas of Mongolia in conjunction with a household risk factor survey. Twenty per- cent of the households (n = 51) had at least one sample positive for Cryptosporidium spp. and/or Giardia duodenalis with several households demonstrating parasite presence in multiple sample types (9.8%, 5/51). Households that used unimproved drinking water, did not have access to an indoor handwashing site, were located in rural areas, and owned animals were associated with higher rates of parasite presence. Our findings show that zoonotic enteric parasite exposure is occurring at the household level and from different hosts, vectors, and vehicles. Public health efforts to prevent the further spread of disease should concentrate on increased water, sanitation and hygiene measures and One Health collaboration between human and animal health care disciplines. Introduction The gastrointestinal zoonotic parasites of Cryptosporidium spp. and Giardia duodenalis cause a significant portion of the diarrheal disease burden worldwide [1±2]. Between the years 2011 and 2016, Cryptosporidium spp. are estimated to have caused 63% of the reported global out- breaks of waterborne protozoal parasites while Giardia spp. were responsible for approxi- mately 37% [3]. These pathogens have proven to be important etiological agents for childhood enteric disease, particularly among those living in households and communities that lack safe water, sanitation and hygiene [1,3±7]. Moderate to severe diarrheal disease from parasites such as Cryptosporidium spp. can increase a child's risk of death by 8.5 to 12 times that of a child without diarrhea and limit their nutritional intake leading to stunted physical growth [1,5]. These protozoan parasites can be transmitted through contact with contaminated water, sur- faces and fomites, filth flies and unwashed hands [2,8±12]. These pathogens also serve as a source of global foodborne disease [13±15]. Cryptosporidium spp. and Giardia duodenalis are resilient zoonotic enteric parasites (ZEPS) that can survive outside of a host from hours to months on surfaces, in soil, and in raw and potable water, regardless of chlorination [8,14,16±18]. The ownership and presence of domes- tic animals in close proximity to households presents an exposure risk for accidental fecal-oral ingestion from contact with unmanaged animal waste, whether directly through the collection of animal dung for cooking fuel or indirectly from drinking water from a contaminated source [6,19±20]. Wildlife, livestock, companion animals like dogs and cats, and synanthropic rodents PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0009543 July 8, 2021 2 / 24 PLOS NEGLECTED TROPICAL DISEASES Zoonotic enteric parasites in Mongolia can all serve as disease hosts and can spread these pathogens to one another, to people, and into their environment making these zoonotic agents a true One Health challenge [21±24]. In Mongolia, the health of humans, animals, and the environment have been intertwined for millennia through the tradition of nomadic herding [25]. Although the nation has the sec- ond lowest population density in the world with slightly more three million people, it is home to more than 66 million livestock [26±27]. Pastoralism and herding remain a popular liveli- hood and cultural practice within Mongolia, yet also present a unique threat for enteric zoono- ses [28±32]. Close contact with free-grazing livestock occurs frequently at the household level as the animals are used for meat and milk, racing and herding, sale and trade, and the manu- facture of animal goods such as leather and fiber [29,33±35]. The nomadic herding lifestyle often lead to interactions between domestic animals and wildlife across their many shared environments, particularly pasture and water sources, thus creating a risk for intraspecies transmission [36,37]. Endemic zoonotic diseases such as brucellosis, echinococcosis, plague, anthrax, and rabies are common and recent years have seen a growth in emerging and reemerging diseases of public health importance (e.g. Seoul hantavirus) [37±38]. However, diarrheal diseases are often unreported and undiagnosed in Mongolia, despite accounting for over 13% of all reported infectious disease [39]. Among hospitalized diarrheal patients in the capital city of Ulaanbaatar, the prevalence of Cryptosporidium spp. and Giardia duodenalis have been reported to be 3.6% and 5.1%, respectively [40]. In neighboring China, research has demonstrated an average prevalence of 2.97% for Cryptosporidium spp. and a range of 0.85% to 9.46% for Giardia spp. among patients [41±43] Access to safe water, sanitation and hygiene services varies
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