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What Diseases Are Transferred From Humans To Animals

  • Journal Listing
  • PLoS One
  • PMC3938448

PLoS 1. 2014; nine(2): e89055.

Reverse Zoonotic Disease Transmission (Zooanthroponosis): A Systematic Review of Seldom-Documented Human Biological Threats to Animals

Ali M. Messenger

i College of Public Health and Health Professions, University of Florida, Gainesville, Florida, Us

2 Emerging Pathogens Institute, University of Florida, Gainesville, Florida, United States of America

Amber N. Barnes

one Higher of Public Health and Health Professions, University of Florida, Gainesville, Florida, Us

Gregory C. Gray

one College of Public Health and Health Professions, University of Florida, Gainesville, Florida, U.s.a.

2 Emerging Pathogens Plant, University of Florida, Gainesville, Florida, Usa of America

Bradley S. Schneider, Editor

Received 2013 Sep 24; Accustomed 2013 Nov 4.

Abstract

Background

Research regarding zoonotic diseases oftentimes focuses on infectious diseases animals take given to humans. However, an increasing number of reports point that humans are transmitting pathogens to animals. Contempo examples include methicillin-resistant Staphylococcus aureus, flu A virus, Cryptosporidium parvum, and Ascaris lumbricoides. The aim of this review was to provide an overview of published literature regarding contrary zoonoses and highlight the need for future work in this area.

Methods

An initial wide literature review yielded 4763 titles, of which 4704 were excluded as non meeting inclusion criteria. After conscientious screening, 56 articles (from 56 countries over iii decades) with documented human-to-animal disease transmission were included in this report.

Findings

In these publications, 21 (38%) pathogens studied were bacterial, 16 (29%) were viral, 12 (21%) were parasitic, and 7 (13%) were fungal, other, or involved multiple pathogens. Effected animals included wild fauna (due north = 28, 50%), livestock (n = 24, 43%), companion animals (n = thirteen, 23%), and various other animals or animals not explicitly mentioned (n = 2, 4%). Published reports of reverse zoonoses transmission occurred in every continent except Antarctica therefore indicating a worldwide disease threat.

Interpretation

As we see a global increase in industrial animate being production, the rapid move of humans and animals, and the habitats of humans and wildlife intertwining with cracking complexity, the future promises more opportunities for humans to crusade reverse zoonoses. Scientific inquiry must be conducted in this area to provide a richer agreement of emerging and reemerging affliction threats. As a outcome, multidisciplinary approaches such as One Wellness will be needed to mitigate these problems.

Introduction

With today'due south rapid transport systems, mod public wellness issues are growing increasingly complex. A pathogen that emerges today in i country can easily be transported unnoticed in people, animals, plants, or food products to distant parts of the world in less than 24 hours [1]. This high level of mobility makes tracking and designing interventions against emerging pathogens exceedingly difficult, requiring close international and interdisciplinary collaborations. Cardinal to these efforts is an understanding of the ecology of emerging diseases. Published works ofttimes cite the large proportion of human emerging pathogens that originate in animals [ii], [3], [four], [5]. However, scientific reports seldom mention homo contributions to the multifariousness of emerging diseases that impact animals. The focus of this review is to examine and summarize the scientific literature regarding such zoonoses transmission. A comprehensive table of the results is included in this certificate.

Methods

For the purpose of this review several terms require definitions. Despite the fact that the term "zoonosis" unremarkably refers to a disease that is transmitted from animals to humans (also called "anthropozoonosis") [6], in this paper, "zoonosis" was divers equally whatsoever illness that is transmitted from animals to humans, or vice versa [6], At that place are 2 related terms ("zooanthroponosis" and "reverse zoonosis") that refer to any pathogen unremarkably reservoired in humans that can be transmitted to other vertebrates [half-dozen]. Acknowledging that the terms "contrary zoonosis" or "zooanthroponosis" are seldom used, and that the term "zoonosis" can have several meanings, search methods were designed to include all of these terms in an effort to capture the widest possible subset of publications with documented human-to-beast transmission.

Literature search

In June 2012, nosotros searched PubMed in addition to several databases inside Web of Knowledge and ProQuest to discover articles documenting reverse zoonoses transmission. Search terms included: opposite zoonosis, bidirectional zoonosis, anthroponosis, zooanthroponosis, anthropozoonosis, and human-to-animal disease transmission. Manufactures were express to clinical and observational type studies and were restricted to English only. Review articles were non included equally they did not demonstrate a specific business relationship of transmission. Letters to editors or similar correspondence were also excluded. Merely publications with documented man-to-animal manual were included. No time period was stipulated.

Iv search strings were used for the PubMed database: ((bidirectional OR reverse) AND (zoono* or "disease transmission")) OR anthropono* OR "human-to-animal"), ((bidirectional OR reverse OR "human being-to-brute") AND (zoono* or "disease transmission")) OR anthropono*), ("reverse zoonoses" OR " bidirectional zoonoses" OR "contrary zoonosis" OR " bidirectional zoonosis" OR "reverse zoonotic" OR " bidirectional zoonotic" OR anthropono* OR ("man-to-beast" AND affliction* AND transmi*)), and (((bidirectional OR reverse OR "human-to-animal") AND (zoonoses[majr] OR "Disease Manual, Infectious"[majr] OR zoonosis[tiab] OR zoonoses[tiab] OR zoonotic[tiab])) OR Anthroponos*[tiab] OR Zooanthroponos*[tiab] OR Anthropozoonos*[tiab]). In the ProQuest and Web of Knowledge databases, we but used i string: ((bidirectional OR reverse) AND (zoonosis OR zoonoses OR zoonotic)) OR anthropono* OR Zooanthropono* OR anthropozoono* OR "human-to-animal" OR "man to animate being"). The lack of additional search strings for the latter databases was due to less comprehensive search capabilities. Duplicate articles were removed.

Literature analyses

Titles and abstracts were reviewed and manufactures were retained when there was prove of disease transmission from humans to animals. During full text review, some citations proved straightforward in distinguishing transmission from humans to animals (e.g. via directly contact), while others were selected based on strong writer suggestion or research implications toward reverse zoonotic transmission. In an effort to highlight trends in an otherwise diverse gear up of articles, citations were grouped by pathogen type and year of publication. To further analyze relationships, nosotros too pictorially displayed the report locations and animal types discussed in the various manufactures.

Results

This comprehensive literature review yielded 4763 titles, 2507 of which were excluded as duplicates (Figure ane). During the review of abstracts, 2091 studies were excluded due to a lack of evidence of man-to-animal disease transmission. Afterward consideration of the 165 eligible for total text review, 109 studies were excluded based on full texts being written in a linguistic communication other than English language, absence of human being-to-animal affliction transmission, or full texts being unavailable. After all exclusions, 56 manufactures were considered for this review (Table 1).

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Flowchart demonstrating the identification and selection process for publications included in this review.

Table 1

Descriptors of reports included in review with documented homo-to-fauna transmission.

Publications Study Location Specimen Source Pathogen Name Creature(south) Infected
Bacteria
Cosivi et al (1995) [vii] Morocco Assorted Mycobacterium tuberculosis, Mycobacterium bovis 1 Wild fauna
Seguin et al (1999) [8] U.s. Veterinary hospital Methicillin-resistant Staphylococcus aureus (MRSA)i , 2 Livestock
Donnelly et al (2000) [ix] U.s. 4H project livestock Streptococcus pneumonia 1 Livestock
Nizeyi et al (2001) [10] Uganda National park Campylobacter spp., Salmonella spp., Shigella sonnei, Shigella boydii, Shigella flexneri 1 , 3 Wildlife
Michel et al (2003) [xi] South Africa Zoo 1000. tuberculosis ane , iii Wildlife
Hackendahl et al (2004) [12]; likewise meet Erwin et al (2004) [thirteen] United States Veterinary infirmary M. tuberculosis 1 , 4 Companion
Prasad et al (2005) [14] India Veterinary hospital One thousand. tuberculosis iii , 4 Livestock
Weese et al (2006) [15] Canada, United States Household; Veterinary hospital MRSAone Companion
Morris et al (2006) [xvi] U.s. Household; Veterinary hospital MRSA1 Companion
Kwon et al (2006) [17] Korea Slaughterhouse MRSA1 , 3 Companion; Livestock
Rwego et al (2008) [xviii] Uganda National park Escherichia coli ane , iii Livestock; Wildlife
Hsieh et al (2008) [19] Taiwan Livestock subcontract Oxacillin-resistant Staphylococcus aureus (ORSA) Livestock
Berg et al (2009) [20] Ethiopia Abattoir M. tuberculosis 3 Livestock
Heller et al (2010) [21] United Kingdom Household; Veterinary infirmary MRSAane , 2 Companion
Kottler et al (2010) [22] United states of america Household; Veterinary hospital MRSA1 Companion
Ewers et al (2010) [23] Germany, Italy, Netherlands, French republic, Spain, Denmark, Austria & Luxembourg Veterinary hospital Escherichia coli Companion; Livestock
Every et al (2011) [24] Australia University zoology section Helicobacter pylori ane Wildlife
Lin et al (2011) [25] United States Veterinary hospital MRSA1 Companion; Livestock
Rubin et al (2011) [26] Canada Veterinary hospital; Human hospital MRSAone Companion
Price et al (2012) [27] Republic of austria, Belgium, Canada, Switzerland, Cathay, Deutschland, Denmark, Spain, Republic of finland, France, French Guiana, Hungary, Italian republic, the netherlands, Peru, Poland, Portugal, Slovenia, and United States Animal meat for auction MRSA1 Livestock
Virus
Meng et al (1998) [28] Us Veterinarian laboratory; Human sample Hepatitis East5 Wild fauna
Willy et al (1999) [29] The states Veterinary laboratory Measles1 , 4 Wild fauna
Kaur et al (2008) [thirty] Tanzania National park Man metapneumovirus (hMPV)1 , 4 Wildlife
Feagins et al (2008) [31] United States Commercially sold laboratory animals Hepatitis E5 Livestock
Song et al (2010) [32] Republic of korea Livestock farm Influenza A (2009 pandemic H1N1)1 Livestock
Swenson et al (2010) [33] United States Household; Veterinarian hospital Influenza A (2009 pandemic H1N1)i , 4 Companion
Tischer et al (2010) [34] Various; Unspecified Unknown (previous reports cited) Human herpesvirus 1, human herpesvirus four1 , 3 , 4 Companion; Wild fauna
Abe et al (2010) [35] Japan Wildlife Rotavirusane , three Wildlife
Berhane et al (2010) [36] Canada, Republic of chile Livestock farm Influenza A (2009 pandemic H1N1)1 , 4 , five Livestock
Poon et al (2010) [37] Hong Kong Slaughterhouse Flu A (2009 pandemic H1N1) Livestock
Forgie et al (2011) [38] Canada Veterinary laboratory Influenza A (2009 pandemic H1N1) Livestock
Holyoake et al (2011) [39] Commonwealth of australia Livestock farm Influenza A (2009 pandemic H1N1)iv Livestock
Scotch et al (2011) [40] Mexico, United States, Canada, Australia, United Kingdom, France, Ireland, Argentina, Republic of chile, Singapore, Kingdom of norway, Cathay, Italy, Thailand, S Korea, Republic of indonesia, Deutschland, Japan, Russia, Republic of finland, and Iceland Unknown (previous reports cited) Flu A (2009 pandemic H1N1) Companion; Livestock; Wildlife
Trevennec et al (2011) [41] Vietnam Livestock farm; Shambles Flu A (2009 pandemic H1N1)one , two Livestock
Wevers et al (2011) [42] Cameroon, Democratic Congo-brazzaville, Gamiba, Côte d'Ivoire, Republic of Congo, Rwanda, Tanzania, Uganda, Frg (initial samples in Asia and South America) Wild fauna; Zoo Human adenovirus A-F1 , iii Wildlife
Crossley et al (2012) [43] Usa Private zoo Influenza A (2009 pandemic H1N1)2 , 3 Wild fauna
Parasite
Sleeman et al (2000) [44] Rwanda National park Chilomastix mesnili, Endolimax nana, Stronglyoides fuelleborni, Trichuris trichiura 1 , 3 Wildlife
Graczyk et al (2001) [45] Uganda National park Cryptosporidium parvum Wildlife
Graczyk et al (2002) [46] Uganda National park Encephalitozoon intestinalis 1 , 3 Wildlife
Graczyk et al (2002) [47] Uganda National park Giardia duodenalis one , 3 Wildlife
Guk et al (2004) [48] Korea Laboratory C. parvum 5 Livestock; Wild animals
Noël et al (2005) [49] Singapore, Pakistan, Japan, Thailand, United States, France, Czech Commonwealth N/A Blastocystis spp Livestock; Wildlife
Coklin et al (2007) [50] Canada Livestock subcontract G. duodenalis, C. parvum 1 , iii Livestock
Adejinmi et al (2008) [51] Nigeria Zoo Ascaris lumbricoides, T. trichiura 1 Wildlife
Teichroeb et al (2009) [52] Republic of ghana Wild animals Isospora spp., Giardia duodenalis i , 3 Wildlife
Ash et al (2010) [53] Zambia; Namibia; Australia Wildlife; Zoo 1000. duodenalis 1 Wild fauna
Johnston et al (2010) [54] Republic of uganda National park G. duodenalis 1 , 3 Livestock; Wildlife
Dixon et al (2011) [55] Canada Livestock farm Grand. duodenalis, C. parvum i , 3 Livestock
Fungus
Jacobs et al (1988) [56] Unspecified Assorted Microsporum spp., Trichophyton spp.1 Contrasted
Pal et al (1997) [57] India Household Trichophyton rubrum 1 Wildlife
Wrobel (2008) [58] Usa Veterinarian hospital Candida albicans 3 Companion; Livestock; Wild animals
Sharma et al (2009) [59] Bharat Household; Veterinary hospital Microsporum gypseum 1 Wildlife
Other
Epstein et al (2009) [lx] + Assorted Wildlife; Livestock subcontract; Zoo; Laboratory Canker simplex 1, influenza A, parasite spp, Measles, MRSA, 1000. tuberculosis 1 , two , 3 , iv , 6 Assorted
Guyader et al (2000) [61] & France Shellfish-growing waters Astrovirus, enterovirus, hepatitis A, Norwalk-like (norovirus), rotavirusane , 3 Wildlife
Muehlenbein et al (2010) [62] Malaysia Wildlife Contrasted illnessesone , half-dozen Wildlife

Included reports were based in 56 dissimilar countries. Although the reports spanned three decades, there seems to be an increasing number of studies published in recent years (Effigy ii). Twenty eight percent of the studies were conducted in the United States (n = 16), 14% in Canada (n = 8), and 13% in Uganda (northward = vii) (Effigy 3). Within the study results, 21 publications discussed human-to-creature transmission of bacterial pathogens (38%); 16 studies discussed viral pathogens (29%); 12 studies discussed human being parasites (21%); and 7 studies discussed transmission of fungi, other pathogens, or diseases of multiple etiologies (thirteen%). Bacterial pathogen reports were centered in North America and Europe. Viral studies were well-distributed globally. Parasitic affliction reports were conducted chiefly in Africa. Fungal studies were conducted almost exclusively in India (Figure 4).

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Timeline and frequency of reverse zoonoses publications included in this review shown past pathogen type.

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Proportion of reverse zoonoses scientific reports included in review as illustrated by study location.

Note: Many reports identified several countries therefore each country in this effigy does not necessarily represent a single corresponding publication.

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Study locations for literature included in review.

A. Proportion of reverse zoonoses scientific reports equally illustrated by study location and pathogen type; B. Proportion of reverse zoonoses scientific reports on bacterial pathogens as illustrated by study location; C. Proportion of opposite zoonoses scientific reports on viral pathogens as illustrated by report location; D. Proportion of contrary zoonoses scientific reports on parasitic pathogens as illustrated past written report location; Due east. Proportion of reverse zoonoses scientific reports on fungal pathogens as illustrated by study location.

Animals with reported infection or inoculation with homo diseases included wildlife (northward = 28, l%), livestock (due north = 24, 43%), companion animals (n = 13, 23%), and other animals or animals not explicitly mentioned (n = 2, 4%). The majority of companion and livestock animals were studied in Northward America and Europe, while wildlife studies were near prevalent in Africa (Table 1, Effigy 5). Typically, diagnostic specimens were nerveless at veterinary hospitals (northward = 15, 27%), national parks (northward = 8, xiv%) and livestock farms (northward = 8, 14%). Straight contact was the suggested transmission road 71% of the time (n = 40). Other transmission routes included fomite, oral contact, aerosols, and inoculation.

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Animal type and study location included in review literature.

A. Proportion of reverse zoonoses scientific reports as illustrated by study location and brute(southward) infected; B. Proportion of opposite zoonoses scientific reports on companion animals as illustrated past study location; C. Proportion of reverse zoonoses scientific reports on livestock as illustrated past study location; D. Proportion of reverse zoonoses scientific reports on wild animals every bit illustrated by report location.

As early on as 1988, zoonoses research focusing on fungal pathogens was beingness conducted. Initial studies implied homo transmission of Microsporum (n = 2) and Trichophyton (northward = two) to various animal species, with a later on article centered on Candida albicans (n = ane) (Figure ii). These publications were set in India (n = 2) and the United states (n = 1).

Since 1988, research with implications of reverse zoonoses has been largely focused on infections of bacterial origin, beginning in 1995. The majority of manufactures in this review focused on methicillin-resistant Staphylococcus aureus (MRSA) (n = 9) and Mycobacterium tuberculosis (n = five). Reports regarding these bacteria were primarily conducted in the U.s. (n = 8) among livestock (n = 10) or companion animals (due north = 9).

Viruses were the 2d well-nigh common pathogen associated with human-to-animal manual. Reverse zoonoses reports regarding viral pathogens began in 1998 and have since been focused primarily on flu with neat involvement surrounding the 2009 H1N1 pandemic (northward = 9). These studies were conducted largely in the United states of america (n = half dozen) in livestock (n = 8) and wildlife (n = viii).

Studies suggestive of transmission of man parasites to animals were first published in 2000. The most commonly reported parasitic agents to be transmitted from humans to animals were Giardia duodenalis (n = 6) and Cryptosporidium parvum (n = 4). Parasitic research has been carried out about frequently in Uganda (n = 4) and Canada (northward = 2). The authors investigated human parasitic infections importantly in wildlife (northward = 10) and livestock (n = five).

Man-to-creature transmission is plausible for a large number of diseases because the pathogens concerned are known to infect multiple species [3]. For instance, 77.3% of the pathogens infecting livestock are considered "multiple species pathogens [three]." However, this review only found 24 reports which considered contrary zoonoses affliction transmission as a potential threat to livestock, underscoring a need for farther research in this area [three]. Similarly, in companion animals this review establish even fewer studies (n = thirteen) that implied reverse zoonoses as a possible cause of infection, despite the fact that 90% of known pathogens for domestic carnivores are recognized as "multiple species pathogens [iii]." The bulk of publications in this reverse zoonoses review involved studies documenting homo-to-wildlife transmission (north = 28). Unfortunately, they as well were severely lacking in comparison to the research need. Each type of animate being- livestock, companion, or wildlife, represents a unique gear up of risk factors for reverse zoonoses through their specific routes of human contact.

Discussion

Human and beast relationships are probable to continue to intensify worldwide over the next several decades due in function to animal husbandry practices, the growth of the companion animal market place, climate change and ecosystem disruption, anthropogenic development of habitats, and global travel and commerce [2]. Equally the man-brute connectedness escalates, and so does the threat for pathogen spread [1], [63]. This review notes a number of factors that influence the risk of illness manual from humans to animals.

For instance, human being population growth and expansion encourages unlike species to interact in ways and at rates previously non encountered, and to do so in novel geographical areas [4]. The term "pathogen pollution" refers to the procedure of bringing a foreign affliction into a new locality due to human involvement [64]. In the case of the endangered African painted dog, wild dogs have been infected with human strains of Giardia duodenalis, leading researchers to believe that pathogen pollution occurred through open up defecation in and effectually national parks by tourists and local residents [53]. Anthropogenic changes in the ecosystem increment the amount of shared habitats betwixt humans and animals thus exposing both to new pathogens. Researchers discovered the man strain of pandemic Escherichia coli strain 025:H4-ST131 CTX-M-15 in many dissimilar species of animals indicating inter-species manual from humans to pets and livestock [23]. This item man strain found to be infecting animals was documented beyond Europe.

In addition to habitat alter, growth, and/or devastation, there is the e'er-increasing global move of products and travelers that extends to both humans and animals. During the pandemic of 2009 H1N1 influenza, the novel virus was able to travel across the globe and from humans to swine in less than two months [32]. I driving force behind the move of animals and fauna products is the worldwide shipment of meat. This phenomenon is a relatively new event as developing countries adjust their diets to include more than meat- and dairy-based products [4]. While food and animal rubber guidelines attempt to go on up with the speed of global merchandise, international efforts announced to be outpaced by product demand. For example, it has been estimated that five tons of illegal bushmeat laissez passer through Paris' master Roissy-Charles de Gaulle airport each week in personal luggage [65]. Still, overt retail systems of creature and animal products can too contribute to the danger of zoonoses and reverse zoonoses manual. Many animals are sold in markets which allow humans and a myriad of animal species to interact in weather condition that are known to trigger emerging diseases [66]. Specifically, this is true for alive brute markets and warehouses for exotic pets [4].

The pet manufacture is an enormous global business that now expands from domestic to exotic animals. A 2011–2012 national pet owners survey found that in the United states alone, 72.9 million homes or 62% of the population have a pet [67]. Of these pets, the majority of animals are dogs (78.2 one thousand thousand) or cats (86.four million), but a large number of pets are birds (16.2 million), reptiles (13 million), or small animals (xvi million) [67]. As pet ownership seems to be increasing worldwide and more exotic pets are being introduced to private homes, the potential for affliction transmission between humans and animals will continue to increase. Veterinarians must more fervently protect animals under their care from human disease threats [68]. Adopting a I Wellness strategy for emerging disease surveillance and reporting will benefit both humans and animals and produce a more collaborative response plan.

Veterinarians, animal wellness workers, and public wellness professionals are not the only ones who should recognize the threat of opposite zoonoses. Increased sensation must besides be communicated to the general public. Worldwide, there are 1,300 zoos and aquariums that sustain more than 700 million visitors each twelvemonth [69]. The potential for pathogen spread to animals tin can come from a visitor with an illness, contamination of a shared surround or food, and the spread of disease through relocation of animals for captivity or educational purposes. In Tanzania, a fatal outbreak of human metapneumovirus in wild chimpanzees is believed to be the result of researchers and visitors viewing the animals in a national park that was one time the great apes' territory [thirty]. Public education and sensation should be augmented to include the potential wellness threats inflicted on a susceptible animal past an unhealthy human.

This report has limitations. Every bit demonstrated in this review paper, the trend for reporting pathogen spread of human being-to-animal is increasing. Still the route of homo transmission to creature disease manifestation is frequently unknown in these reports and non well documented in this review. Also the written report did not examine articles that did not certificate homo-to-animal manual. We acknowledge that many additional works that have recorded the existence of human pathogens in animals were non evaluated. Withal, this review was designed to summarize only the publications that document opposite zoonotic transmission.

Many mutual and dangerous pathogens have non, to the authors' knowledge, been researched as reverse zoonoses threats to animals representing a significant gap in the scientific literature. Time to come investigations of reverse zoonoses should take into account both transmission routes and affliction prevalence. Prospective research should as well include a wider variety of etiological agents and beast species. Scientific literature must document the presence and manual of man diseases in animals such that the wealth of literature on this subject will become defined and accessible across multiple disciplines. A wider knowledge and understanding of reverse zoonoses should exist sought for a successful One Health response. We recommend that future research be conducted on how human disease can, and does, impact the animals around us.

Supporting Information

File S1

PLOS PRISMA 2009 checklist.

(DOC)

Acknowledgments

The authors especially thank Nancy Schaffer and Jennifer Lyon from the University of Florida Library Sciences for their enquiry aid.

Funding Argument

This work was supported by the US Military machine Health Surveillance Middle - Global Emerging Infections Surveillance Operations (multiple grants to GCG) and a supplement from the National Institute of Allergy and Infectious Diseases (R01 AI068803 to GCG). The funders had no role in report design, data collection and analysis, decision to publish, or grooming of the manuscript.

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Articles from PLoS 1 are provided here courtesy of Public Library of Science


Source: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3938448/#:~:text=However%2C%20an%20increasing%20number%20of,Cryptosporidium%20parvum%2C%20and%20Ascaris%20lumbricoides.

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