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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">A Review of Zoonotic Pathogens of Dromedary Camels</title><author><name sortKey="Zhu, Sophie" sort="Zhu, Sophie" uniqKey="Zhu S" first="Sophie" last="Zhu">Sophie Zhu</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1936 9684</institution-id><institution-id institution-id-type="GRID">grid.27860.3b</institution-id><institution>Graduate Group in Epidemiology,</institution><institution>University of California,</institution></institution-wrap>Davis, CA 95616 USA</nlm:aff></affiliation></author><author><name sortKey="Zimmerman, Dawn" sort="Zimmerman, Dawn" uniqKey="Zimmerman D" first="Dawn" last="Zimmerman">Dawn Zimmerman</name><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="GRID">grid.419531.b</institution-id><institution>Global Health Program,</institution><institution>Smithsonian Conservation Biology Institute,</institution></institution-wrap>Washington, DC 20008 USA</nlm:aff></affiliation></author><author><name sortKey="Deem, Sharon L" sort="Deem, Sharon L" uniqKey="Deem S" first="Sharon L." last="Deem">Sharon L. Deem</name><affiliation><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 8504 5603</institution-id><institution-id institution-id-type="GRID">grid.502158.b</institution-id><institution>Institute for Conservation Medicine,</institution><institution>Saint Louis Zoo,</institution></institution-wrap>Saint Louis, MO 63110 USA</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31140075</idno><idno type="pmc">7087575</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7087575</idno><idno type="RBID">PMC:7087575</idno><idno type="doi">10.1007/s10393-019-01413-7</idno><date when="2019">2019</date><idno type="wicri:Area/Pmc/Corpus">000511</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000511</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">A Review of Zoonotic Pathogens of Dromedary Camels</title><author><name sortKey="Zhu, Sophie" sort="Zhu, Sophie" uniqKey="Zhu S" first="Sophie" last="Zhu">Sophie Zhu</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1936 9684</institution-id><institution-id institution-id-type="GRID">grid.27860.3b</institution-id><institution>Graduate Group in Epidemiology,</institution><institution>University of California,</institution></institution-wrap>Davis, CA 95616 USA</nlm:aff></affiliation></author><author><name sortKey="Zimmerman, Dawn" sort="Zimmerman, Dawn" uniqKey="Zimmerman D" first="Dawn" last="Zimmerman">Dawn Zimmerman</name><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="GRID">grid.419531.b</institution-id><institution>Global Health Program,</institution><institution>Smithsonian Conservation Biology Institute,</institution></institution-wrap>Washington, DC 20008 USA</nlm:aff></affiliation></author><author><name sortKey="Deem, Sharon L" sort="Deem, Sharon L" uniqKey="Deem S" first="Sharon L." last="Deem">Sharon L. Deem</name><affiliation><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 8504 5603</institution-id><institution-id institution-id-type="GRID">grid.502158.b</institution-id><institution>Institute for Conservation Medicine,</institution><institution>Saint Louis Zoo,</institution></institution-wrap>Saint Louis, MO 63110 USA</nlm:aff></affiliation></author></analytic><series><title level="j">Ecohealth</title><idno type="ISSN">1612-9202</idno><idno type="eISSN">1612-9210</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p id="Par1">Dromedary, or one-humped, camels <italic>Camelus dromedarius</italic> are an almost exclusively domesticated species that are common in arid areas as both beasts of burden and production animals for meat and milk. Currently, there are approximately 30 million dromedary camels, with highest numbers in Africa and the Middle East. The hardiness of camels in arid regions has made humans more dependent on them, especially as a stable protein source. Camels also carry and may transmit disease-causing agents to humans and other animals. The ability for camels to act as a point source or vector for disease is a concern due to increasing human demands for meat, lack of biosafety and biosecurity protocols in many regions, and a growth in the interface with wildlife as camel herds become sympatric with non-domestic species. We conducted a literature review of camel-borne zoonotic diseases and found that the majority of publications (65%) focused on Middle East respiratory syndrome (MERS), brucellosis, <italic>Echinococcus granulosus</italic>, and Rift Valley fever. The high fatality from MERS outbreaks during 2012–2016 elicited an immediate response from the research community as demonstrated by a surge of MERS-related publications. However, we contend that other camel-borne diseases such as <italic>Yersinia pestis</italic>, <italic>Coxiella burnetii</italic>, and Crimean–Congo hemorrhagic fever are just as important to include in surveillance efforts. Camel populations, particularly in sub-Saharan Africa, are increasing exponentially in response to prolonged droughts, and thus, the risk of zoonoses increases as well. In this review, we provide an overview of the major zoonotic diseases present in dromedary camels, their risk to humans, and recommendations to minimize spillover events.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Abbas, B" uniqKey="Abbas B">B Abbas</name></author><author><name sortKey="Agab, H" uniqKey="Agab H">H Agab</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Abdel Aaty, He" uniqKey="Abdel Aaty H">HE Abdel Aaty</name></author><author><name sortKey="Abdel Hameed, Dm" uniqKey="Abdel Hameed D">DM Abdel-Hameed</name></author><author><name sortKey="Alam Eldin, Yh" uniqKey="Alam Eldin Y">YH Alam-Eldin</name></author><author><name sortKey="El Shennawy, Sf" uniqKey="El Shennawy S">SF El-Shennawy</name></author><author><name sortKey="Aminou, Ha" uniqKey="Aminou H">HA Aminou</name></author><author><name sortKey="Makled, Ss" uniqKey="Makled S">SS Makled</name></author><author><name 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Ecohealth</journal-id><journal-id journal-id-type="iso-abbrev">Ecohealth</journal-id><journal-title-group><journal-title>Ecohealth</journal-title></journal-title-group><issn pub-type="ppub">1612-9202</issn><issn pub-type="epub">1612-9210</issn><publisher><publisher-name>Springer US</publisher-name><publisher-loc>New York</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31140075</article-id><article-id pub-id-type="pmc">7087575</article-id><article-id pub-id-type="publisher-id">1413</article-id><article-id pub-id-type="doi">10.1007/s10393-019-01413-7</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review</subject></subj-group></article-categories><title-group><article-title>A Review of Zoonotic Pathogens of Dromedary Camels</article-title></title-group><contrib-group><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0002-8694-4058</contrib-id><name><surname>Zhu</surname><given-names>Sophie</given-names></name><address><phone>406-600-5788</phone><email>sozhu@ucdavis.edu</email></address><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Zimmerman</surname><given-names>Dawn</given-names></name><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Deem</surname><given-names>Sharon L.</given-names></name><xref ref-type="aff" rid="Aff3">3</xref></contrib><aff id="Aff1"><label>1</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1936 9684</institution-id><institution-id institution-id-type="GRID">grid.27860.3b</institution-id><institution>Graduate Group in Epidemiology,</institution><institution>University of California,</institution></institution-wrap>Davis, CA 95616 USA</aff><aff id="Aff2"><label>2</label><institution-wrap><institution-id institution-id-type="GRID">grid.419531.b</institution-id><institution>Global Health Program,</institution><institution>Smithsonian Conservation Biology Institute,</institution></institution-wrap>Washington, DC 20008 USA</aff><aff id="Aff3"><label>3</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 8504 5603</institution-id><institution-id institution-id-type="GRID">grid.502158.b</institution-id><institution>Institute for Conservation Medicine,</institution><institution>Saint Louis Zoo,</institution></institution-wrap>Saint Louis, MO 63110 USA</aff></contrib-group><pub-date pub-type="epub"><day>28</day><month>5</month><year>2019</year></pub-date><pub-date pub-type="ppub"><year>2019</year></pub-date><volume>16</volume><issue>2</issue><fpage>356</fpage><lpage>377</lpage><history><date date-type="received"><day>14</day><month>8</month><year>2018</year></date><date date-type="rev-recd"><day>12</day><month>3</month><year>2019</year></date><date date-type="accepted"><day>12</day><month>3</month><year>2019</year></date></history><permissions><copyright-statement>© EcoHealth Alliance 2019</copyright-statement><license><license-p>This article is made available via the PMC Open Access Subset for unrestricted research re-use and secondary analysis in any form or by any means with acknowledgement of the original source. These permissions are granted for the duration of the World Health Organization (WHO) declaration of COVID-19 as a global pandemic.</license-p></license></permissions><abstract id="Abs1"><p id="Par1">Dromedary, or one-humped, camels <italic>Camelus dromedarius</italic> are an almost exclusively domesticated species that are common in arid areas as both beasts of burden and production animals for meat and milk. Currently, there are approximately 30 million dromedary camels, with highest numbers in Africa and the Middle East. The hardiness of camels in arid regions has made humans more dependent on them, especially as a stable protein source. Camels also carry and may transmit disease-causing agents to humans and other animals. The ability for camels to act as a point source or vector for disease is a concern due to increasing human demands for meat, lack of biosafety and biosecurity protocols in many regions, and a growth in the interface with wildlife as camel herds become sympatric with non-domestic species. We conducted a literature review of camel-borne zoonotic diseases and found that the majority of publications (65%) focused on Middle East respiratory syndrome (MERS), brucellosis, <italic>Echinococcus granulosus</italic>, and Rift Valley fever. The high fatality from MERS outbreaks during 2012–2016 elicited an immediate response from the research community as demonstrated by a surge of MERS-related publications. However, we contend that other camel-borne diseases such as <italic>Yersinia pestis</italic>, <italic>Coxiella burnetii</italic>, and Crimean–Congo hemorrhagic fever are just as important to include in surveillance efforts. Camel populations, particularly in sub-Saharan Africa, are increasing exponentially in response to prolonged droughts, and thus, the risk of zoonoses increases as well. In this review, we provide an overview of the major zoonotic diseases present in dromedary camels, their risk to humans, and recommendations to minimize spillover events.</p></abstract><kwd-group xml:lang="en"><title>Keywords</title><kwd>Camel</kwd><kwd>Nomadic</kwd><kwd>One health</kwd><kwd>Pathogen</kwd><kwd>Spillover</kwd><kwd>Zoonoses</kwd></kwd-group><funding-group><award-group><funding-source><institution-wrap><institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/100000200</institution-id><institution>United States Agency for International Development</institution></institution-wrap></funding-source><award-id>PREDICT (Cooperative Agreement No. AID-OAA-A-14-00</award-id></award-group></funding-group><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© EcoHealth Alliance 2019</meta-value></custom-meta></custom-meta-group></article-meta></front><body><sec id="Sec1"><title>Introduction</title><p id="Par2">Worldwide there are roughly 30 million dromedary camels, with highest numbers found in Africa and the Middle East (Figure <xref rid="Fig1" ref-type="fig">1</xref>). Due to increased consumption and contact with camel meat and milk, camels represent a significant point source for zoonotic disease transmission to humans. Pastoralist camel production, in particular, is associated with a risk of disease spillover from wildlife into camel populations, and from camels to wildlife, as well as less opportunities for disease surveillance and control. By 2050 the human population is projected to grow by 2.5 billion, with nearly half of all population growth occurring in the African continent (Roser <xref ref-type="bibr" rid="CR251">2018</xref>). Along with the increase in human population in Africa and the Middle East, the camel population has also experienced steady growth as the demand and production of camel meat and milk escalates (FAOSTAT <xref ref-type="bibr" rid="CR112">2016</xref>). More and more, nomadic herders are switching to an agricultural or urban setting to raise camels and this change in camel production brings potential risks of disease emergence and transmission. In addition, with the realities of climate change and the increase in drought conditions, camel hardiness has led to a shift in livestock choice in many regions of the world from cattle to camels, making camels even more abundant (Watson et al. <xref ref-type="bibr" rid="CR298">2016</xref>)<fig id="Fig1"><label>Figure 1</label><caption><p>Map of domesticated dromedary camel population by country in 2016; data from Food and Agricultural Organization (Food and Agricultural Organization, 2016)</p></caption><graphic xlink:href="10393_2019_1413_Fig1_HTML" id="MO1"></graphic></fig></p><p id="Par3">Limited resources, low levels of regulation, poor hygiene, high mobility of animals and herders, and lack of consistent veterinary care also act as drivers for disease spillover (Gossner et al. <xref ref-type="bibr" rid="CR125">2016</xref>; Megersa et al. <xref ref-type="bibr" rid="CR186">2011</xref>). Knowledge of camel-borne diseases, clinical signs, and pathways of transmission is thus important to mitigate human risks of camel-associated zoonoses. Many infectious diseases that have been an issue in Africa and the Middle East during the last decades, such as Middle East respiratory syndrome (MERS) and brucellosis, have an association with camel contact (Ahmed et al. <xref ref-type="bibr" rid="CR10">2010</xref>; Ferguson and Van Kerkhove <xref ref-type="bibr" rid="CR109">2014</xref>). Additionally, novel camel-borne diseases continue to be identified, as best exemplified by reports of a prion disease from Algerian abattoir camels published during the editing of this review paper (Babelhadj et al. <xref ref-type="bibr" rid="CR38">2018</xref>)</p><p id="Par4">Significant research on seropositivity and detection of specific diseases of camels, those that have implications for human health, has been conducted; however, to the authors’ knowledge no publication has summarized the current literature on these zoonotic diseases. Realizing the need for a thorough review of the literature to identify the risks that camels pose to human health was the impetus for this review. In this paper, we review publications of the most common confirmed and potential camel zoonoses of interest: bacterial, viral, and parasitic, and offer recommendations for surveillance and control of the diseases of highest priority.</p></sec><sec id="Sec2"><title>Methods</title><p id="Par5">We utilized two search engines, Google Scholar and PubMed, to search for publications related to camel-borne disease and zoonotic spillover. We chose Google Scholar for breadth and volume of content, while PubMed was chosen from medical and public health-specific search engines for its specificity. Publications on Bactrian camels <italic>Camelus bactrianus</italic> were excluded because they are primarily wild but are used as beasts of burden and food in select countries and only account for 2 million out of 30 million total camels (IUCN <xref ref-type="bibr" rid="CR150">2008</xref>). To cast a wide net for possible diseases we did not search for specific zoonotic diseases and instead classified publications by disease after the initial literature search. All search terms included the words camel and human as well as one of six other words keywords: camel + human + zoonotic, illness, spillover, outbreak, transmission, or disease. For each set of search terms, we reviewed the first 100 results for relevancy or all results if < 100. Included publications were restricted to those written in English, but there was no date limit, no other restrictions were set, and papers were sorted by relevance. From a total of 1054 papers, 619 were unique or non-duplicates and 304 of these were relevant (Figure <xref rid="Fig2" ref-type="fig">2</xref>). Five of these 304 papers reported on multiple diseases. Results that were excluded included papers that inconclusively related to transmission from camels <italic>n</italic> = 96, non-camelid animals <italic>n</italic> = 40, studies that focused on vaccines <italic>n</italic> = 25, camel-specific diseases <italic>n</italic> = 22, articles/seminars <italic>n</italic> = 15, and non-relevant topics <italic>n</italic> = 117. Examples of non-relevance were papers that did not mention camels at all, papers that did not discuss transmission of disease, papers on human-to-human transmission, or papers that discussed laboratory testing and techniques related to these diseases. Food-borne bacterial diseases from pathogens such as <italic>Escherichia coli</italic>, <italic>Salmonella,</italic> and <italic>Campylobacter</italic> were consolidated into one category termed “food-borne” because they share transmission pathways, have similar symptoms, and were pre-grouped by several publications in this review. We also elected to present these pathogens in this fashion because there was a precedence set by said publications. Papers with positive serologic testing in camels, probable disease through an explained epidemiologic link between human disease and camel-borne pathogens, and isolation of similar strains in humans and camels fit criteria for inclusion. Relevant papers were sorted into bacterial, viral, and parasitic categories along with recorded counts for each disease. Results were separated out in this manner to cover scope number of diseases as well as depth number of papers per disease. Figures were created in Quantum GIS 3.6 (QGIS Development Team <xref ref-type="bibr" rid="CR400">2019</xref>). We completed the literature search in February and March of 2018.<fig id="Fig2"><label>Figure 2</label><caption><p>Methodology for inclusion and exclusion of publications of camel-borne zoonoses. Out of an initial 1054 eligible publications, 619 were unique and non-duplicate and 304 of those were included in the final selection of journal articles for further analysis</p></caption><graphic xlink:href="10393_2019_1413_Fig2_HTML" id="MO2"></graphic></fig></p></sec><sec id="Sec3"><title>Results</title><p id="Par6">Through this literature review, we identified 304 papers published between 1970 and 2018 that described disease agents in camels with probable (see above definition) or confirmed transmission to humans. Thirty-seven camel-borne diseases were identified, comprised of 12 bacterial diseases, 13 viral diseases, and 12 parasitic diseases (Table <xref rid="Tab1" ref-type="table">1</xref>). The most frequently occurring diseases or disease-causing agents in this study were MERS <italic>n</italic> = 118, <italic>Echinococcus granulosus n</italic> = 46, brucellosis <italic>n</italic> = 35, and Rift Valley fever <italic>n</italic> = 19. In this study, 42 countries were represented in the literature, with most papers originating from Saudi Arabia <italic>n</italic> = 36, Iran <italic>n</italic> = 27, Kenya <italic>n</italic> = 15, and Egypt <italic>n</italic> = 14 (Figure <xref rid="Fig3" ref-type="fig">3</xref>). There has been a dramatic increase in publications over the last eight years with a peak during 2012–2016, when research on MERS was undertaken in a number of laboratories following the first diagnosis of a human fatality reported in 2012 (Fig. <xref rid="Fig4" ref-type="fig">4</xref>) (Kupferschmidt <xref ref-type="bibr" rid="CR168">2014</xref>).<table-wrap id="Tab1"><label>Table 1</label><caption><p>Camel-borne diseases found in review by paper count</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left">Disease/agent</th><th align="left">Type</th><th align="left">Paper count</th><th align="left">References</th></tr></thead><tbody><tr><td align="left">Middle East respiratory syndrome</td><td align="left">Virus</td><td align="left">118</td><td align="left">Adney et al. (<xref ref-type="bibr" rid="CR5">2014</xref>), Ahmed (<xref ref-type="bibr" rid="CR7">2017a</xref>, <xref ref-type="bibr" rid="CR8">b</xref>), Al Hammadi et al. (<xref ref-type="bibr" rid="CR15">2015</xref>), Al salihi and Alrodhan (<xref ref-type="bibr" rid="CR17">2017</xref>), Al-Tawfiq and Memish (<xref ref-type="bibr" rid="CR18">2014a</xref>, <xref ref-type="bibr" rid="CR19">b</xref>), Al-Tawfiq et al. (<xref ref-type="bibr" rid="CR20">2014</xref>), Alagaili et al. (<xref ref-type="bibr" rid="CR21">2014</xref>), Aleanizy et al. (<xref ref-type="bibr" rid="CR23">2017</xref>), Alexandersen et al. (<xref ref-type="bibr" rid="CR24">2014</xref>), Alhakeem et al. (<xref ref-type="bibr" rid="CR25">2016</xref>), Alhamlan et al. (<xref ref-type="bibr" rid="CR26">2017</xref>), Ali et al. (<xref ref-type="bibr" rid="CR27">2017</xref>), Alraddadi et al. (<xref ref-type="bibr" rid="CR28">2016</xref>), Alsolamy et al. (<xref ref-type="bibr" rid="CR29">2017</xref>), Assiri et al. (<xref ref-type="bibr" rid="CR34">2016</xref>), Azhar et al. (<xref ref-type="bibr" rid="CR36">2014a</xref>, <xref ref-type="bibr" rid="CR37">b</xref>), Balkhy et al. (<xref ref-type="bibr" rid="CR40">2016</xref>), Banik et al. (<xref ref-type="bibr" rid="CR42">2015</xref>), Buchholz et al. (<xref ref-type="bibr" rid="CR57">2013</xref>), Chan et al. (<xref ref-type="bibr" rid="CR62">2014</xref>, <xref ref-type="bibr" rid="CR63">2015</xref>), Chu et al. (<xref ref-type="bibr" rid="CR70">2014</xref>, <xref ref-type="bibr" rid="CR69">2015</xref>, <xref ref-type="bibr" rid="CR68">2018</xref>), Corman et al. (<xref ref-type="bibr" rid="CR73">2014a</xref>, <xref ref-type="bibr" rid="CR74">b</xref>, <xref ref-type="bibr" rid="CR72">2016</xref>), Cotten et al. (<xref ref-type="bibr" rid="CR77">2013</xref>, <xref ref-type="bibr" rid="CR78">2014</xref>), Crameri et al. (<xref ref-type="bibr" rid="CR79">2015</xref>), Deem et al. (<xref ref-type="bibr" rid="CR80">2015</xref>), Devi et al. (<xref ref-type="bibr" rid="CR82">2014</xref>), Drosten et al. (<xref ref-type="bibr" rid="CR85">2015</xref>), Du and Han (<xref ref-type="bibr" rid="CR86">2016</xref>), Dudas et al. (<xref ref-type="bibr" rid="CR88">2018</xref>), Durai et al. (<xref ref-type="bibr" rid="CR90">2015</xref>), Eckerle et al. (<xref ref-type="bibr" rid="CR91">2014</xref>), El Bushra et al. (<xref ref-type="bibr" rid="CR97">2016</xref>), Fanoy et al. (<xref ref-type="bibr" rid="CR104">2014</xref>), Farag et al. (<xref ref-type="bibr" rid="CR105">2015</xref>), Fehr et al. (<xref ref-type="bibr" rid="CR108">2017</xref>), Ferguson and Van Kerkhove (<xref ref-type="bibr" rid="CR109">2014</xref>), Food and Agriculture Organization of the United Nations (<xref ref-type="bibr" rid="CR111">2017</xref>), Funk et al. (<xref ref-type="bibr" rid="CR113">2016</xref>), Gardner and MacIntyre (<xref ref-type="bibr" rid="CR115">2014</xref>), Gossner et al. (<xref ref-type="bibr" rid="CR125">2016</xref>), Gutiérrez et al. (<xref ref-type="bibr" rid="CR128">2015</xref>), Haagmans et al. (<xref ref-type="bibr" rid="CR132">2014</xref>, <xref ref-type="bibr" rid="CR133">2016</xref>), Han et al. (<xref ref-type="bibr" rid="CR138">2016</xref>), Hemida et al. (<xref ref-type="bibr" rid="CR145">2013</xref>, <xref ref-type="bibr" rid="CR143">2014</xref>, <xref ref-type="bibr" rid="CR142">2015</xref>, <xref ref-type="bibr" rid="CR144">2017</xref>), Holmes (<xref ref-type="bibr" rid="CR146">2014</xref>), Hunter et al. (<xref ref-type="bibr" rid="CR148">2016</xref>), Kayali and Peiris (<xref ref-type="bibr" rid="CR158">2015</xref>), Khalafalla et al. (<xref ref-type="bibr" rid="CR159">2015</xref>), Kupferschmidt (<xref ref-type="bibr" rid="CR169">2015</xref>), Liljander et al. (<xref ref-type="bibr" rid="CR173">2016</xref>), Mackay and Arden (<xref ref-type="bibr" rid="CR176">2015</xref>, <xref ref-type="bibr" rid="CR177">2017</xref>), Majumder (<xref ref-type="bibr" rid="CR181">2015</xref>), Memish et al. (<xref ref-type="bibr" rid="CR193">2013</xref>, <xref ref-type="bibr" rid="CR190">2014a</xref>, <xref ref-type="bibr" rid="CR191">b</xref>, <xref ref-type="bibr" rid="CR188">2015</xref>), Meyer et al. (<xref ref-type="bibr" rid="CR196">2014</xref>, <xref ref-type="bibr" rid="CR195">2016</xref>), Miguel et al. (<xref ref-type="bibr" rid="CR198">2016</xref>, <xref ref-type="bibr" rid="CR197">2017</xref>), Mohd et al. (<xref ref-type="bibr" rid="CR204">2016</xref>), Muhairi et al. (<xref ref-type="bibr" rid="CR206">2016</xref>), Müller et al. (<xref ref-type="bibr" rid="CR208">2014</xref>, <xref ref-type="bibr" rid="CR209">2015</xref>), Ng et al. (<xref ref-type="bibr" rid="CR212">2016</xref>), Nowotny and Kolodziejek (<xref ref-type="bibr" rid="CR215">2014</xref>), Oladipo (<xref ref-type="bibr" rid="CR217">2015</xref>), Olival and Epstein (<xref ref-type="bibr" rid="CR218">2015</xref>), Omrani et al. (<xref ref-type="bibr" rid="CR221">2015</xref>), Omrani and Shalhoub (<xref ref-type="bibr" rid="CR222">2015</xref>), Park et al. (<xref ref-type="bibr" rid="CR226">2015</xref>), Rabaan (<xref ref-type="bibr" rid="CR231">2017</xref>), Raj et al. (<xref ref-type="bibr" rid="CR235">2014</xref>), Rasmussen et al. (<xref ref-type="bibr" rid="CR238">2015</xref>, <xref ref-type="bibr" rid="CR239">2016</xref>), Reeves et al. (<xref ref-type="bibr" rid="CR241">2015</xref>), Reusken et al. (<xref ref-type="bibr" rid="CR242">2013a</xref>, <xref ref-type="bibr" rid="CR245">b</xref>, <xref ref-type="bibr" rid="CR244">2014a</xref>, <xref ref-type="bibr" rid="CR246">b</xref>, <xref ref-type="bibr" rid="CR243">2015</xref>, <xref ref-type="bibr" rid="CR247">2016</xref>), Reuss et al. (<xref ref-type="bibr" rid="CR248">2014</xref>), Sabir et al. (<xref ref-type="bibr" rid="CR252">2016</xref>), Salkeld et al. (<xref ref-type="bibr" rid="CR258">2016</xref>), Saqib et al. (<xref ref-type="bibr" rid="CR259">2017</xref>), Shapiro et al. (<xref ref-type="bibr" rid="CR269">2016</xref>), Sharif-Yakan and Kanj (<xref ref-type="bibr" rid="CR271">2014</xref>), Shehata et al. (<xref ref-type="bibr" rid="CR275">2016</xref>), Su et al. (<xref ref-type="bibr" rid="CR284">2016</xref>), Tai et al. (<xref ref-type="bibr" rid="CR288">2017</xref>), Watson et al. (<xref ref-type="bibr" rid="CR297">2014</xref>), Wernery et al. (<xref ref-type="bibr" rid="CR301">2015</xref>, <xref ref-type="bibr" rid="CR302">2016</xref>), Widagdo et al. (<xref ref-type="bibr" rid="CR303">2016</xref>), de Wit et al. (<xref ref-type="bibr" rid="CR304">2016</xref>), de Wit and Munster (<xref ref-type="bibr" rid="CR305">2013</xref>), World Health Organization (<xref ref-type="bibr" rid="CR308">2015</xref>), Younan et al. (<xref ref-type="bibr" rid="CR312">2016</xref>), Yusof et al. (<xref ref-type="bibr" rid="CR314">2015</xref>), Zhang et al. (<xref ref-type="bibr" rid="CR318">2016</xref>), Zumla et al. (<xref ref-type="bibr" rid="CR320">2015</xref>, <xref ref-type="bibr" rid="CR319">2016</xref>), Zumla and Memish (<xref ref-type="bibr" rid="CR321">2014</xref>)</td></tr><tr><td align="left">Hydatidosis (<italic>Echinococcus granulosus</italic>)</td><td align="left">Parasite</td><td align="left">46</td><td align="left">Abdel Aaty et al. (<xref ref-type="bibr" rid="CR2">2012</xref>), Abushhewa et al. (<xref ref-type="bibr" rid="CR4">2010</xref>), Ahmadi (<xref ref-type="bibr" rid="CR6">2005</xref>), Alvarez Rojas et al. (<xref ref-type="bibr" rid="CR30">2014</xref>), Azab et al. (<xref ref-type="bibr" rid="CR35">2004</xref>), Bardonnet et al. (<xref ref-type="bibr" rid="CR44">2002</xref>, <xref ref-type="bibr" rid="CR43">2003</xref>), Casulli et al. (<xref ref-type="bibr" rid="CR60">2010</xref>), Dinkel et al. (<xref ref-type="bibr" rid="CR83">2004</xref>), Eckert and Deplazes (<xref ref-type="bibr" rid="CR92">2004</xref>), Eckert et al. (<xref ref-type="bibr" rid="CR93">1989</xref>), Elmahdi et al. (<xref ref-type="bibr" rid="CR100">2004</xref>), Hailemariam et al. (<xref ref-type="bibr" rid="CR136">2012</xref>), Hajialilo et al. (<xref ref-type="bibr" rid="CR137">2012</xref>), Fasihi Harandi et al. (<xref ref-type="bibr" rid="CR139">2002</xref>), Hassanain et al. (<xref ref-type="bibr" rid="CR141">2016</xref>), Kamenetzky et al. (<xref ref-type="bibr" rid="CR156">2002</xref>), Karimi et al. (<xref ref-type="bibr" rid="CR157">2017</xref>), Kia et al. (<xref ref-type="bibr" rid="CR163">2010</xref>), Kinkar et al. (<xref ref-type="bibr" rid="CR165">2017</xref>), Latif et al. (<xref ref-type="bibr" rid="CR170">2010</xref>), Macpherson and McManus (<xref ref-type="bibr" rid="CR178">1982</xref>), Macpherson and Smyth (<xref ref-type="bibr" rid="CR179">1985</xref>), Maillard et al. (<xref ref-type="bibr" rid="CR180">2006</xref>), Mandal and Deb Mandal (<xref ref-type="bibr" rid="CR182">2012</xref>), McManus (<xref ref-type="bibr" rid="CR184">1981</xref>), McManus and Rishi (<xref ref-type="bibr" rid="CR185">1989</xref>), Mirzaei et al. (<xref ref-type="bibr" rid="CR199">2016</xref>), Mobedi et al. (<xref ref-type="bibr" rid="CR202">1970</xref>), Mrad et al. (<xref ref-type="bibr" rid="CR205">2005</xref>), Oksanen and Lavikainen (<xref ref-type="bibr" rid="CR216">2015</xref>), Omer et al. <xref ref-type="bibr" rid="CR219">2010a</xref>, <xref ref-type="bibr" rid="CR220">b</xref>, Sadjjadi (<xref ref-type="bibr" rid="CR253">2006</xref>), Salem et al. (<xref ref-type="bibr" rid="CR257">2011</xref>), Shahnazi et al. (<xref ref-type="bibr" rid="CR267">2011</xref>), Shariatzadeh et al. (<xref ref-type="bibr" rid="CR270">2015</xref>), Sharma et al. (<xref ref-type="bibr" rid="CR273">2013b</xref>), Singh et al. (<xref ref-type="bibr" rid="CR277">2014</xref>), Spotin et al. (<xref ref-type="bibr" rid="CR280">2015</xref>, <xref ref-type="bibr" rid="CR281">2017</xref>), Tigre et al. (<xref ref-type="bibr" rid="CR291">2016</xref>), Thompson (<xref ref-type="bibr" rid="CR292">2008</xref>), Utuk et al. (<xref ref-type="bibr" rid="CR293">2008</xref>), Wachira et al. (<xref ref-type="bibr" rid="CR295">1993</xref>), Youssef and Uga (<xref ref-type="bibr" rid="CR313">2014</xref>), Zhang et al. (<xref ref-type="bibr" rid="CR316">1998</xref>)</td></tr><tr><td align="left">Brucellosis</td><td align="left">Bacteria</td><td align="left">35</td><td align="left">Abbas and Agab (<xref ref-type="bibr" rid="CR1">2002</xref>), Ahmed et al. (<xref ref-type="bibr" rid="CR10">2010</xref>), Al Dahouk et al. (<xref ref-type="bibr" rid="CR14">2013</xref>), Bekele et al. (<xref ref-type="bibr" rid="CR46">2013</xref>), Cooper (<xref ref-type="bibr" rid="CR71">1992</xref>), Ducrotoy et al. (<xref ref-type="bibr" rid="CR87">2015</xref>), El-Ansary et al. (<xref ref-type="bibr" rid="CR94">2001</xref>), Fiori et al. (<xref ref-type="bibr" rid="CR110">2000</xref>), Garcell et al. (<xref ref-type="bibr" rid="CR114">2016</xref>), Gautret et al. (<xref ref-type="bibr" rid="CR117">2013</xref>), Godfroid et al. (<xref ref-type="bibr" rid="CR123">2005</xref>, <xref ref-type="bibr" rid="CR124">2013</xref>), Gumaa et al. (<xref ref-type="bibr" rid="CR126">2014</xref>), Gwida et al. (<xref ref-type="bibr" rid="CR129">2010</xref>, <xref ref-type="bibr" rid="CR130">2012</xref>), Kiel and Yousuf (<xref ref-type="bibr" rid="CR164">1989</xref>), Megersa et al. (<xref ref-type="bibr" rid="CR186">2011</xref>), Megersa et al. (<xref ref-type="bibr" rid="CR187">2012</xref>), Memish and Balkhy (<xref ref-type="bibr" rid="CR189">2004</xref>), Nimri (<xref ref-type="bibr" rid="CR213">2003</xref>), Omer et al. <xref ref-type="bibr" rid="CR219">2010a</xref>, <xref ref-type="bibr" rid="CR220">b</xref>, Osoro et al. (<xref ref-type="bibr" rid="CR224">2015</xref>), Pappas (<xref ref-type="bibr" rid="CR225">2010</xref>), Rhodes et al. (<xref ref-type="bibr" rid="CR250">2016</xref>), Schelling et al. (<xref ref-type="bibr" rid="CR261">2003</xref>), Schelling et al. (<xref ref-type="bibr" rid="CR262">2004</xref>), Seleem et al. (<xref ref-type="bibr" rid="CR264">2010</xref>), Shaalan et al. (<xref ref-type="bibr" rid="CR265">2002</xref>), Shimol et al. (<xref ref-type="bibr" rid="CR276">2012</xref>), Smits and Kadri (<xref ref-type="bibr" rid="CR278">2005</xref>), Sprague et al. (<xref ref-type="bibr" rid="CR282">2012</xref>), Teshome et al. (<xref ref-type="bibr" rid="CR290">2003</xref>), Wernery (<xref ref-type="bibr" rid="CR300">2014</xref>), Yahya (<xref ref-type="bibr" rid="CR311">2015</xref>), Zewolda and Wereta (<xref ref-type="bibr" rid="CR315">2012</xref>)</td></tr><tr><td align="left">Rift Valley fever</td><td align="left">Virus</td><td align="left">19</td><td align="left">Abdo-Salem et al. (<xref ref-type="bibr" rid="CR3">2006</xref>), Ahmed Kamal (<xref ref-type="bibr" rid="CR9">2011</xref>), Bird et al. (<xref ref-type="bibr" rid="CR51">2008</xref>), Britch et al. (<xref ref-type="bibr" rid="CR55">2013</xref>), Chevalier et al. (<xref ref-type="bibr" rid="CR64">2010</xref>), Chinikar et al. (<xref ref-type="bibr" rid="CR66">2013</xref>), El Mamy et al. (<xref ref-type="bibr" rid="CR98">2011</xref>, <xref ref-type="bibr" rid="CR99">2014</xref>), Faye et al. (<xref ref-type="bibr" rid="CR107">2014</xref>), Gerdes (<xref ref-type="bibr" rid="CR118">2004</xref>), Horton et al. (<xref ref-type="bibr" rid="CR147">2014</xref>), Jäckel et al. (<xref ref-type="bibr" rid="CR151">2013</xref>), Linthicum et al. (<xref ref-type="bibr" rid="CR174">2016</xref>), Lutomiah et al. (<xref ref-type="bibr" rid="CR175">2014</xref>), Merrill et al. (<xref ref-type="bibr" rid="CR192">2015</xref>), Macharia et al. (<xref ref-type="bibr" rid="CR210">2010</xref>), Paweska (<xref ref-type="bibr" rid="CR228">2015</xref>), Swai and Sindato (<xref ref-type="bibr" rid="CR286">2015</xref>), Weaver and Reisen (<xref ref-type="bibr" rid="CR299">2010</xref>)</td></tr><tr><td align="left">Food-borne</td><td align="left">Bacteria</td><td align="left">15</td><td align="left">Dehkordi et al. (<xref ref-type="bibr" rid="CR81">2013</xref>), Fadlelmula et al. (<xref ref-type="bibr" rid="CR103">2016</xref>), Ghoneim et al. (<xref ref-type="bibr" rid="CR120">2017</xref>), Hajialilo et al. (<xref ref-type="bibr" rid="CR137">2012</xref>), Horton et al. (<xref ref-type="bibr" rid="CR147">2014</xref>), Jaros et al. (<xref ref-type="bibr" rid="CR152">2008</xref>), Kaindi et al. (<xref ref-type="bibr" rid="CR155">2012</xref>), Rahimi et al. (<xref ref-type="bibr" rid="CR232">2010</xref>, <xref ref-type="bibr" rid="CR233">2012</xref>), Rahimi and Kheirabadi (<xref ref-type="bibr" rid="CR234">2012</xref>), Raufu et al. (<xref ref-type="bibr" rid="CR240">2015</xref>), Salehi et al. (<xref ref-type="bibr" rid="CR256">2012</xref>), Shabana et al. (<xref ref-type="bibr" rid="CR266">2013</xref>), Sung et al. (<xref ref-type="bibr" rid="CR285">2008</xref>), Tadesse (<xref ref-type="bibr" rid="CR287">2015</xref>), Tejedor-Junco et al. (<xref ref-type="bibr" rid="CR289">2015</xref>)</td></tr><tr><td align="left">Plague (<italic>Yersinia pestis</italic>)</td><td align="left">Bacteria</td><td align="left">10</td><td align="left">Aikimbajev et al. (<xref ref-type="bibr" rid="CR12">2003</xref>), Arbaji et al. (<xref ref-type="bibr" rid="CR32">2005</xref>), Bramanti et al. (<xref ref-type="bibr" rid="CR54">2016</xref>), Cabanel et al. (<xref ref-type="bibr" rid="CR58">2013</xref>), Christie et al. (<xref ref-type="bibr" rid="CR67">1980</xref>), Drancourt et al. (<xref ref-type="bibr" rid="CR84">2006</xref>), El-Bahnasawy et al. (<xref ref-type="bibr" rid="CR95">2012</xref>), Leslie et al. (<xref ref-type="bibr" rid="CR172">2011</xref>), Saeed et al. (<xref ref-type="bibr" rid="CR255">2005</xref>), Stenseth et al. (<xref ref-type="bibr" rid="CR283">2008</xref>)</td></tr><tr><td align="left">Camelpox</td><td align="left">Virus</td><td align="left">9</td><td align="left">Balamurugan et al. (<xref ref-type="bibr" rid="CR39">2013</xref>), Bera et al. (<xref ref-type="bibr" rid="CR49">2010</xref>, <xref ref-type="bibr" rid="CR50">2011</xref>, <xref ref-type="bibr" rid="CR48">2015</xref>), Duraffour et al. (<xref ref-type="bibr" rid="CR89">2011</xref>), Jezek et al. (<xref ref-type="bibr" rid="CR154">1983</xref>), Khalafalla and Abdelazim (<xref ref-type="bibr" rid="CR160">2017</xref>), Pearce-Duvet (<xref ref-type="bibr" rid="CR229">2006</xref>), Shchelkunov (<xref ref-type="bibr" rid="CR274">2013</xref>)</td></tr><tr><td align="left">Q fever (<italic>Coxiella burnetii</italic>)</td><td align="left">Bacteria</td><td align="left">7</td><td align="left">Klemmer et al. (<xref ref-type="bibr" rid="CR167">2018</xref>), Mohabbati Mobarez et al. (<xref ref-type="bibr" rid="CR201">2017</xref>), Njeru et al. (<xref ref-type="bibr" rid="CR214">2016</xref>), Pirouz et al. (<xref ref-type="bibr" rid="CR230">2015</xref>), Schelling et al. (<xref ref-type="bibr" rid="CR261">2003</xref>, <xref ref-type="bibr" rid="CR262">2004</xref>), Vanderburg et al. (<xref ref-type="bibr" rid="CR294">2014</xref>)</td></tr><tr><td align="left"><italic>Linguatula serrata</italic></td><td align="left">Parasite</td><td align="left">7</td><td align="left">Bamorovat et al. (<xref ref-type="bibr" rid="CR41">2014</xref>), Farjanikish and Shokrani (<xref ref-type="bibr" rid="CR106">2016</xref>), Haddadzadeh et al. (<xref ref-type="bibr" rid="CR134">2010</xref>), Oryan et al. (<xref ref-type="bibr" rid="CR223">2011</xref>), Rezaei et al. (<xref ref-type="bibr" rid="CR249">2012</xref>), Sadjjadi et al. (<xref ref-type="bibr" rid="CR254">1998</xref>), Shakerian et al. (<xref ref-type="bibr" rid="CR268">2008</xref>)</td></tr><tr><td align="left">Hepatitis E</td><td align="left">Virus</td><td align="left">5</td><td align="left">Khuroo and Khuroo (<xref ref-type="bibr" rid="CR162">2016</xref>), Lee et al. (<xref ref-type="bibr" rid="CR171">2016</xref>), Pavio et al. (<xref ref-type="bibr" rid="CR227">2015</xref>), Rasche et al. (<xref ref-type="bibr" rid="CR236">2016</xref>), Spahr et al. (<xref ref-type="bibr" rid="CR279">2018</xref>)</td></tr><tr><td align="left">Crimean–Congo hemorrhagic fever</td><td align="left">Virus</td><td align="left">4</td><td align="left">Champour et al. (<xref ref-type="bibr" rid="CR61">2016</xref>), Khan et al. (<xref ref-type="bibr" rid="CR161">1997</xref>), Mertens et al. (<xref ref-type="bibr" rid="CR194">2013</xref>), Walker et al. (<xref ref-type="bibr" rid="CR296">2016</xref>)</td></tr><tr><td align="left">Tuberculosis</td><td align="left">Bacteria</td><td align="left">4</td><td align="left">Cosivi et al. (<xref ref-type="bibr" rid="CR76">1995</xref>), Garine-Wichatitsky et al. (<xref ref-type="bibr" rid="CR116">2013</xref>), Gumi et al. (<xref ref-type="bibr" rid="CR127">2012</xref>), Moda et al. (<xref ref-type="bibr" rid="CR203">1996</xref>)</td></tr><tr><td align="left">Anthrax</td><td align="left">Bacteria</td><td align="left">3</td><td align="left">Aikembayev et al. (<xref ref-type="bibr" rid="CR11">2010</xref>), Musa et al. (<xref ref-type="bibr" rid="CR211">1993</xref>), Woods et al. (<xref ref-type="bibr" rid="CR307">2004</xref>)</td></tr><tr><td align="left"><italic>Trypanosoma evansi</italic></td><td align="left">Parasite</td><td align="left">2</td><td align="left">Bennoune et al. (<xref ref-type="bibr" rid="CR47">2013</xref>), Haridy et al. (<xref ref-type="bibr" rid="CR140">2011</xref>)</td></tr><tr><td align="left">Ecthyma</td><td align="left">Virus</td><td align="left">2</td><td align="left">Bazargani et al. (<xref ref-type="bibr" rid="CR45">2010</xref>), Moallin and Zessin (<xref ref-type="bibr" rid="CR200">1988</xref>)</td></tr><tr><td align="left">Rotavirus</td><td align="left">Virus</td><td align="left">2</td><td align="left">Ghosh et al. (<xref ref-type="bibr" rid="CR121">2011</xref>), Jere et al. (<xref ref-type="bibr" rid="CR153">2014</xref>)</td></tr><tr><td align="left">Helminth</td><td align="left">Parasite</td><td align="left">2</td><td align="left">Anvari-Tafti et al. (<xref ref-type="bibr" rid="CR31">2013</xref>), McCarthy and Moore (<xref ref-type="bibr" rid="CR183">2000</xref>)</td></tr><tr><td align="left">Toxoplasmosis</td><td align="left">Parasite</td><td align="left">2</td><td align="left">Alanazi (<xref ref-type="bibr" rid="CR22">2013</xref>), Dehkordi et al. (<xref ref-type="bibr" rid="CR81">2013</xref>)</td></tr><tr><td align="left">Alkhurma hemorrhagic fever</td><td align="left">Virus</td><td align="left">1</td><td align="left">Carletti (<xref ref-type="bibr" rid="CR59">2010</xref>)</td></tr><tr><td align="left">Betacoronavirus UAE-HKU23</td><td align="left">Virus</td><td align="left">1</td><td align="left">Woo et al. (<xref ref-type="bibr" rid="CR306">2014</xref>)</td></tr><tr><td align="left">Dera Ghazi Khan virus</td><td align="left">Virus</td><td align="left">1</td><td align="left">Walker et al. (<xref ref-type="bibr" rid="CR296">2016</xref>)</td></tr><tr><td align="left">HCoV-229E</td><td align="left">Virus</td><td align="left">1</td><td align="left">Corman et al. (<xref ref-type="bibr" rid="CR75">2018</xref>)</td></tr><tr><td align="left">Rabies</td><td align="left">Virus</td><td align="left">1</td><td align="left">Bloch and Diallo (<xref ref-type="bibr" rid="CR52">1995</xref>)</td></tr><tr><td align="left">Torque teno virus</td><td align="left">Virus</td><td align="left">1</td><td align="left">Al-Moslih et al. (<xref ref-type="bibr" rid="CR16">2007</xref>)</td></tr><tr><td align="left"><italic>Aeromonas spp.</italic></td><td align="left">Bacteria</td><td align="left">1</td><td align="left">Ghenghesh et al. (<xref ref-type="bibr" rid="CR119">2001</xref>)</td></tr><tr><td align="left"><italic>Bartonella</italic></td><td align="left">Bacteria</td><td align="left">1</td><td align="left">Rasis et al. (<xref ref-type="bibr" rid="CR237">2014</xref>)</td></tr><tr><td align="left">Glanders (<italic>Burkholderia mallei)</italic></td><td align="left">Bacteria</td><td align="left">1</td><td align="left">Scholz et al. (<xref ref-type="bibr" rid="CR263">2014</xref>)</td></tr><tr><td align="left">Johne’s disease (paratuberculosis)</td><td align="left">Bacteria</td><td align="left">1</td><td align="left">Ghosh et al. (<xref ref-type="bibr" rid="CR122">2012</xref>)</td></tr><tr><td align="left"><italic>Klebsiella pneumoniae</italic></td><td align="left">Bacteria</td><td align="left">1</td><td align="left">Sharma et al. (<xref ref-type="bibr" rid="CR272">2013a</xref>)</td></tr><tr><td align="left"><italic>Rickettsia aeschlimannii</italic></td><td align="left">Bacteria</td><td align="left">1</td><td align="left">Kleinerman et al. (<xref ref-type="bibr" rid="CR166">2013</xref>)</td></tr><tr><td align="left"><italic>Babesia bovis</italic></td><td align="left">Parasite</td><td align="left">1</td><td align="left">Ereqat et al. (<xref ref-type="bibr" rid="CR102">2016</xref>)</td></tr><tr><td align="left"><italic>Cryptosporidium</italic></td><td align="left">Parasite</td><td align="left">1</td><td align="left">Sazmand et al. (<xref ref-type="bibr" rid="CR260">2012</xref>)</td></tr><tr><td align="left">Fascioliasis</td><td align="left">Parasite</td><td align="left">1</td><td align="left">Younan et al. (<xref ref-type="bibr" rid="CR312">2016</xref>)</td></tr><tr><td align="left">Leishmaniosis</td><td align="left">Parasite</td><td align="left">1</td><td align="left">Ashford (<xref ref-type="bibr" rid="CR33">2000</xref>)</td></tr><tr><td align="left">Onchocerciasis</td><td align="left">Parasite</td><td align="left">1</td><td align="left">El-Bahnasawy et al. (<xref ref-type="bibr" rid="CR96">2015</xref>)</td></tr><tr><td align="left">Sarcocystis</td><td align="left">Parasite</td><td align="left">1</td><td align="left">Chhabra and Samantaray (<xref ref-type="bibr" rid="CR65">2012</xref>)</td></tr><tr><td align="left">Trichinellosis</td><td align="left">Parasite</td><td align="left">1</td><td align="left">Bommer et al. (<xref ref-type="bibr" rid="CR53">1980</xref>)</td></tr></tbody></table></table-wrap><fig id="Fig3"><label>Figure 3</label><caption><p>Number of publications by country of study, range <italic>n</italic> = 1 Finland, Argentina to <italic>n</italic> = 36 Saudi Arabia</p></caption><graphic xlink:href="10393_2019_1413_Fig3_HTML" id="MO3"></graphic></fig><fig id="Fig4"><label>Fig. 4</label><caption><p>Frequency of camel-borne disease publications between 1970 and 2018 identified in this review</p></caption><graphic xlink:href="10393_2019_1413_Fig4_HTML" id="MO4"></graphic></fig></p><sec id="Sec4"><title>Viral</title><p id="Par7">The large majority of publications were related to MERS <italic>n</italic> = 118, a novel coronavirus. Genetic comparisons between camel and human isolated MERS are highly similar and camels continue to exhibit positive seropositivity for MERS in recent tests (Chu et al. <xref ref-type="bibr" rid="CR68">2018</xref>).</p><p id="Par8">The review identified 19 papers on Rift Valley fever (RVF) transmission, most of which detailed how common seropositivity to RVF virus was in camel herds. Four of these papers emphasized that livestock like camels, cattle, and sheep served as important amplifiers for the virus, especially prior to outbreaks in Kenya and Mauritania (Bird et al. <xref ref-type="bibr" rid="CR51">2008</xref>; Britch et al. <xref ref-type="bibr" rid="CR55">2013</xref>; El Mamy et al. <xref ref-type="bibr" rid="CR98">2011</xref>, <xref ref-type="bibr" rid="CR99">2014</xref>).</p><p id="Par9">Four of nine publications on Camelpox discussed human transmission, including a paper that reported the first laboratory-confirmed case of human Camelpox (Bera et al. <xref ref-type="bibr" rid="CR50">2011</xref>).</p><p id="Par10">There were five papers on hepatitis E, one of the five known human hepatitis virus strains, in which camel meat and milk were implicated as risk factors in humans through whole-genome sequencing, HEV IgM, or HEV RNA detection (Pavio et al. <xref ref-type="bibr" rid="CR227">2015</xref> Khuroo and Khuroo <xref ref-type="bibr" rid="CR162">2016</xref>; Lee et al. <xref ref-type="bibr" rid="CR171">2016</xref>; Rasche et al. <xref ref-type="bibr" rid="CR236">2016</xref>; Spahr et al. <xref ref-type="bibr" rid="CR279">2018</xref>). In one of these reports, a liver transplant patient in the United Arab Emirates consumed camel meat and milk regularly and was chronically infected with hepatitis E (Lee et al. <xref ref-type="bibr" rid="CR171">2016</xref>).</p><p id="Par11">While no publication documented clinical evidence of camel–human rabies transmission, one paper presented probable evidence of camel-to-human rabies transmission (Bloch and Diallo <xref ref-type="bibr" rid="CR52">1995</xref>).</p><p id="Par12">A 2018 publication noted that HCoV-229E, a primarily non-lethal coronavirus responsible for a proportion of upper and lower respiratory tract infections, can be transmitted from camels to humans similar to MERS transmission, thus implicating dromedary camels as a possible reservoir of coronaviruses (Corman et al. <xref ref-type="bibr" rid="CR75">2018</xref>). Woo et al. (<xref ref-type="bibr" rid="CR306">2014</xref>) identified a novel betacoronavirus UAE-HKU23 or dromedary camel coronavirus DcCOV in the United Arab Emirates that was detected in 52% of tested camel serum samples.</p><p id="Par13">Other viruses that were found in camels include Alkhurma hemorrhagic fever (AHF) virus <italic>n</italic> = 1, Crimean–Congo hemorrhagic fever (CCHF) virus <italic>n</italic> = 4, rotavirus <italic>n</italic> = 2, camel contagious ecthyma <italic>n</italic> = 2, torque teno virus <italic>n</italic> = 1, and Dera Ghazi Khan virus <italic>n</italic> = 1 (Moallin and Zessin <xref ref-type="bibr" rid="CR200">1988</xref>; Khan et al. <xref ref-type="bibr" rid="CR161">1997</xref>; Al-Moslih et al. <xref ref-type="bibr" rid="CR16">2007</xref>; Bazargani et al. <xref ref-type="bibr" rid="CR45">2010</xref>; Carletti <xref ref-type="bibr" rid="CR59">2010</xref>; Ghosh et al. <xref ref-type="bibr" rid="CR121">2011</xref>; Horton et al. <xref ref-type="bibr" rid="CR147">2014</xref>; Jere et al. <xref ref-type="bibr" rid="CR153">2014</xref>; Champour et al. <xref ref-type="bibr" rid="CR61">2016</xref>; Walker et al. <xref ref-type="bibr" rid="CR296">2016</xref>).</p></sec><sec id="Sec5"><title>Bacterial</title><p id="Par14">A total of 35 papers discussed the risk of brucellosis as a public health threat from camels. Most of these 35 papers (18; 51%) were seroprevalence studies of brucellosis in camels, which reported a prevalence range of between 1.4 and 37.5% (Schelling et al. <xref ref-type="bibr" rid="CR262">2004</xref>; Omer et al. <xref ref-type="bibr" rid="CR219">2010a</xref>, <xref ref-type="bibr" rid="CR220">b</xref>).</p><p id="Par15">Bacterial diseases that are transmitted through food, water, or other types of fecal–oral transmission were grouped together as “food-borne.” This group included <italic>Salmonella</italic>, <italic>E. coli</italic>, <italic>Helicobacter</italic>, <italic>Staphylococcus</italic>, <italic>Enterococci</italic>, <italic>Campylobacter</italic>, and <italic>Leptospirosis</italic>. These diarrheal bacteria were reported in 15 papers, four of which discussed testing for antimicrobial resistance in camels and camel products (Rahimi et al. <xref ref-type="bibr" rid="CR232">2010</xref>; Tadesse <xref ref-type="bibr" rid="CR287">2015</xref>; Tejedor-Junco et al. <xref ref-type="bibr" rid="CR289">2015</xref>; Fadlelmula et al. <xref ref-type="bibr" rid="CR103">2016</xref>).</p><p id="Par16">Ten papers described camel transmission of plague, <italic>Yersinia pestis</italic>. In fact, three papers documented plague infection in patients who directly consumed raw camel meat (Christie et al. <xref ref-type="bibr" rid="CR67">1980</xref>; Arbaji et al. <xref ref-type="bibr" rid="CR32">2005</xref>; Cabanel et al. <xref ref-type="bibr" rid="CR58">2013</xref>).</p><p id="Par17">Seven papers detailed high Q fever <italic>Coxiella burnetii</italic> seropositivity in camels (Schelling et al. <xref ref-type="bibr" rid="CR261">2003</xref>; Schelling et al. <xref ref-type="bibr" rid="CR262">2004</xref>; Vanderburg et al. <xref ref-type="bibr" rid="CR294">2014</xref>; Pirouz et al. <xref ref-type="bibr" rid="CR230">2015</xref>; Njeru et al. <xref ref-type="bibr" rid="CR214">2016</xref>; Mohabbati Mobarez et al. <xref ref-type="bibr" rid="CR201">2017</xref>; Klemmer et al. <xref ref-type="bibr" rid="CR167">2018</xref>). Seroprevalence levels of up to 73% were present in camels in Chad (Schelling et al. <xref ref-type="bibr" rid="CR262">2004</xref>). Humans that work in close contact with camels such as herders, farmers, and breeders are especially at risk of Q fever transmission, with one study finding a high odds ratio (OR = 9) for the association of being a camel breeder and Q fever seropositivity (Schelling et al. <xref ref-type="bibr" rid="CR261">2003</xref>).</p><p id="Par18">The four papers on camel tuberculosis all discussed positive detection of <italic>M. bovis</italic>, indicating that camels are likely also a reservoir for human transmission (Cosivi et al. <xref ref-type="bibr" rid="CR76">1995</xref>; Moda et al. <xref ref-type="bibr" rid="CR203">1996</xref>; Gumi et al. <xref ref-type="bibr" rid="CR127">2012</xref>; Garine-Wichatitsky et al. <xref ref-type="bibr" rid="CR116">2013</xref>). Gumi et al. (<xref ref-type="bibr" rid="CR127">2012</xref>) found isolated <italic>M. tuberculosis</italic> from camels and <italic>M. bovis</italic> from humans, which suggests cross-species transmission of both strains of bacteria.</p><p id="Par19">One of three papers on anthrax conclusively extracted anthrax spores from infected camel meat, which led to illness in ten people (Musa et al. <xref ref-type="bibr" rid="CR211">1993</xref>).</p><p id="Par20">Other bacterial diseases in the literature but occurring less frequently included <italic>Rickettsia aeschlimannii</italic> 1, <italic>Klebsiella pneumoniae</italic> 1, <italic>Aeromonas spp.</italic> 1, <italic>Bartonella spp.</italic> 1, <italic>Burkholderia mallei</italic> 1, and <italic>M. avium subsp. paratuberculosis</italic> 1 (Ghenghesh et al. <xref ref-type="bibr" rid="CR119">2001</xref>; Ghosh et al. <xref ref-type="bibr" rid="CR122">2012</xref>; Kleinerman et al. <xref ref-type="bibr" rid="CR166">2013</xref>; Sharma et al. <xref ref-type="bibr" rid="CR272">2013a</xref>, <xref ref-type="bibr" rid="CR273">b</xref>; Rasis et al. <xref ref-type="bibr" rid="CR237">2014</xref>; Scholz et al. <xref ref-type="bibr" rid="CR263">2014</xref>).</p></sec><sec id="Sec6"><title>Parasitic</title><p id="Par21">The most common zoonotic parasite transmitted from camels to humans was <italic>Echinococcus granulosus n</italic> = 46. This parasite has a variety of hosts but is often found in livestock as intermediate hosts, including camels. A review by Alvarez Rojas et al. (<xref ref-type="bibr" rid="CR30">2014</xref>) estimated that the camel strain of <italic>E. granulosus</italic> causes between 7 and 11% of all hydatid infections in humans. This attributable risk estimate likely varies by geographic location; a molecular survey by Omar et al. (<xref ref-type="bibr" rid="CR219">2010a</xref>, <xref ref-type="bibr" rid="CR220">b</xref>) found that 59% of camels in Sudan were infected with <italic>E. granulosus</italic>, and a subsequent Sudanese paper found that camels and cattle were the principal intermediate host, not sheep as previously believed (Elmahdi et al. <xref ref-type="bibr" rid="CR100">2004</xref>).</p><p id="Par22">There were two papers on the parasite <italic>Trypanosoma evansi</italic>. Prevalence rates of up to 14% were found in camels in Algeria which is comparatively high to other countries and increases risk for human transmission (Bennoune et al. <xref ref-type="bibr" rid="CR47">2013</xref>). Human cases, confirmed with ELISA and stained blood films, of <italic>T. evansi</italic> have been reported in India and Egypt (Haridy et al. <xref ref-type="bibr" rid="CR140">2011</xref>).</p><p id="Par23">Parasitic diseases are commonly passed from camels to humans through meat and milk consumption. One paper on a trichinellosis outbreak in Germany detailed how camel meat brought from Egypt was responsible for zoonotic transmission (Bommer et al. <xref ref-type="bibr" rid="CR53">1980</xref>), and in 2013, researchers detected <italic>Toxoplasma gondii</italic> in camel milk (Dehkordi et al. <xref ref-type="bibr" rid="CR81">2013</xref>). Other fecal- and meat-/milk-transmitted parasites included <italic>Leishmania</italic> spp. <italic>n</italic> = 1, <italic>Babesia bovis n</italic> = 1, <italic>Cryptosporidium</italic> spp. <italic>n</italic> = 1, and <italic>Sarcocystis</italic> spp. <italic>n</italic> = 1 (Ashford <xref ref-type="bibr" rid="CR33">2000</xref>; Sazmand et al. <xref ref-type="bibr" rid="CR260">2012</xref>; Chhabra and Samantaray <xref ref-type="bibr" rid="CR65">2012</xref>; Ereqat et al. <xref ref-type="bibr" rid="CR102">2016</xref>). Four other parasite species found in this cohort were helminths <italic>Haemonchus tataricus</italic>, <italic>Trichostrongylus hamatus</italic>, and <italic>Trichuris infundibulus n</italic> = 2; <italic>Linguatula serrata n</italic> = 7; <italic>Onchocerca volvulus n</italic> = 1; and <italic>Fasciola hepatica</italic> or <italic>Fasciola gigantica n</italic> = 1 (Sadjjadi et al. <xref ref-type="bibr" rid="CR254">1998</xref>; McCarthy and Moore <xref ref-type="bibr" rid="CR183">2000</xref>; Shakerian et al. <xref ref-type="bibr" rid="CR268">2008</xref>; Haddadzadeh et al. <xref ref-type="bibr" rid="CR134">2010</xref>; Oryan et al. <xref ref-type="bibr" rid="CR223">2011</xref>; Rezaei et al. <xref ref-type="bibr" rid="CR249">2012</xref>; Anvari-Tafti et al. <xref ref-type="bibr" rid="CR31">2013</xref>; Bamorovat et al. <xref ref-type="bibr" rid="CR41">2014</xref>; Youssef and Uga <xref ref-type="bibr" rid="CR313">2014</xref>; El-Bahnasawy et al. <xref ref-type="bibr" rid="CR96">2015</xref>; Farjanikish and Shokrani <xref ref-type="bibr" rid="CR106">2016</xref>).</p></sec></sec><sec id="Sec7"><title>Discussion</title><p id="Par24">As determined by publication count as well as known mortality rates, viruses in this review are of highest interest, followed by bacteria and parasites (Table <xref rid="Tab1" ref-type="table">1</xref>). Camels are as ubiquitous as cattle or sheep in many parts of the world; yet, knowledge on potential health risks lags behind that of other livestock species. The combination of human-related climate change, population growth, decline in biodiversity, and land-use change are major drivers for the evolution and spread of zoonotic disease (Engering et al. <xref ref-type="bibr" rid="CR101">2013</xref>).</p><p id="Par25">The emergence of MERS, with outbreaks between 2012 and 2016, was an outcome of these realities, and it is no surprise that MERS continues to receive high amounts of publicity and funding due to its high human fatality rates ~35% and pandemic potential (World Health Organization <xref ref-type="bibr" rid="CR310">2017</xref>). There are currently no widely used vaccines against MERS, but knowledge of its transmission is critical to better implement food safety and sanitation practices within the camel value chain. Rift Valley fever (RVF) was the second most common camel-borne zoonosis in this review and is not a significant source of mortality as less than 3% of patients develop lethal symptoms. However, it is a significant cause of morbidity especially in high-risk populations such as veterinarians, butchers, scientists, animal health workers, farmers, and herders (Ikegami and Makino <xref ref-type="bibr" rid="CR149">2011</xref>). The same goes for Camelpox, which is a minor health problem for camel farmers but incurs significant economic damages from the death of young camels, reduced milk yield, and lasting morbidity (Balamurugan et al. <xref ref-type="bibr" rid="CR39">2013</xref>). MERS, RVF, and Camelpox were some of the most commonly reported camel-borne zoonotic viruses in this literature review, but for preventive purposes awareness of the following viruses is important to promote. Crimean–Congo hemorrhagic fever is listed as a disease with epidemic potential due to its high mortality rate, growing prevalence in Asia and Europe, and lack of vaccines (Mertens et al. <xref ref-type="bibr" rid="CR194">2013</xref>). Alkhurma hemorrhagic fever (AHF) is also a disease of interest because of its hemorrhagic symptoms, recent emergence, and lack of detailed knowledge of its symptoms and transmission. Mortality rates for these viruses along with other hemorrhagic fevers are high because of difficulties in disease diagnosis (World Health Organization <xref ref-type="bibr" rid="CR309">2016</xref>). Alkhurma hemorrhagic fever, CCHF, and Dera Ghazi Khan are mosquito- and tick-borne diseases where camels act as reservoirs and amplifiers (Carletti <xref ref-type="bibr" rid="CR59">2010</xref>; Walker et al. <xref ref-type="bibr" rid="CR296">2016</xref>). Thus, vector surveillance and management around camels in addition to the aforementioned sanitation practices could be highly beneficial to control the spread of these diseases.</p><p id="Par26">The bacterial disease of greatest concern is brucellosis, which is not only zoonotic but also causes severe economic losses for farmers and ranchers across the world in lost milk, reduced fertility, stillbirths, and abortions (Akakpo et al. <xref ref-type="bibr" rid="CR13">2010</xref>). Camel farmers should be cautious and aware when handling camels, and this exemplifies another area where increased attention to sanitation practices would be beneficial. Food-borne diseases are of high importance as evidenced by the rapid establishment of complex camel milk value chains in urban Kenya as well as the breadth of food-borne pathogens found in our review (Muloi et al. <xref ref-type="bibr" rid="CR207">2018</xref>). These locations exemplify the high-risk transmission interfaces that are formed due to a lack of proper protocol and oversight by government agencies in regard to food safety training and hygienic practices (Muloi et al. <xref ref-type="bibr" rid="CR207">2018</xref>). Camels contract plague from infected fleas and may infect humans through contact with infected bodily fluids or consumption of infected meat (Leslie et al. <xref ref-type="bibr" rid="CR172">2011</xref>). However, vaccination in humans can be used to control the spread and occurrence of outbreaks. For example, vaccination rates have steadily increased in Kazakhstan since 2001 and the usage of vaccines in combination with antibiotics has greatly reduced case fatality across the country (Aikimbajev et al. <xref ref-type="bibr" rid="CR12">2003</xref>). The abundance of publications on brucellosis, plague, and food-borne bacterial illnesses reaffirms their presence in camels.</p><p id="Par27">The earliest papers in this review came from the 1970s and almost exclusively discussed parasites like <italic>E. granulosus</italic> with occasional papers on viral and bacterial disease. This finding is consistent with a historical lack of widespread high-quality technology for viral and bacterial detection, as well as increased focus on viruses today as compared to 30–40 years ago. Parasitic diseases in this review were not significant sources of mortality. Cysts from <italic>E. granulosus</italic> occur on lung and liver tissue along with other internal organs and contribute to morbidity in humans through pressure effects and problematic locations of cysts <bold>(</bold>Mandal and Deb Mandal <xref ref-type="bibr" rid="CR182">2012</xref>). Vaccination of camels against <italic>E. granulosus</italic> is not widely practiced because sheep and dogs are considered to be more important hosts: This, in combination with unsanitary practices and high camel and sheep densities, creates higher risk for humans in these areas (Zhang and McManus <xref ref-type="bibr" rid="CR317">2006</xref>). No other publications on parasites showed that they were significant sources of human mortality, and there were low paper counts for most parasites, which could indicate their rarity in camels and largely non-lethal status.</p><p id="Par28">Many studies demonstrated a high seroprevalence to a variety of zoonotic pathogens in camel populations along with current or past examples of camel–human transmission. However, few validated standardized tests exist for camels, making disease detection and confirmation difficult (Gwida et al. <xref ref-type="bibr" rid="CR131">2011</xref>). Seropositivity is an indication of antibodies and not antigens, so while this shows that a camel was exposed, it does not provide information on the infection status of the individual or the ability of the camel to transmit a pathogen. These papers may not have exact confirmation for each strain in each country or population, but high prevalence coupled with known instances of transmission provides a guideline for prospective risks. Additionally, because we did not analyze our results with statistical methods we were unable to assess the strength of association between pathogens and human risk. Another limitation of our review was the absence of certain pivotal papers; this may have been due to the use of Google Scholar as one of the two major search engines. A serosurvey of Q fever in Laikipia County, Kenya, that revealed high seroprevalence 18.6% in dromedaries was one such paper that fit our inclusion and search criteria keywords: camel, zoonotic, human, but did not appear in any searches (Browne et al. <xref ref-type="bibr" rid="CR56">2017</xref>). A common critique of Google Scholar is the limited ability to sort results, which thus provides evidence that it misses important literature in many case studies (Haddaway et al. <xref ref-type="bibr" rid="CR135">2015</xref>). Although we did use PubMed we still may have missed eligible publications because of relevance sorting and/or using only the first 100 results. Our study was limited to peer-reviewed material in English and excludes a thorough review of French, Turkish, Farsi, and Arabic literature which could have provided more information in target regions. The use of additional search engines or search terms may improve the scope of literature reviews, which we will make note of for the future.</p><p id="Par29">Lastly, a limitation not necessary related to methodology but rather the epidemiology of diseases relates to missing diseases at the camel–other livestock/wildlife–human interface that we would not have captured in our review. Although we did not include them as part of this review there were papers found in our initial searches that described camel–livestock and camel–wildlife transmission. These shared pathogens may be zoonotic and include camels as part of the transmission cycle but are not necessarily identified as a camel-borne zoonosis. For example, other animals may be the original or primary source of many pathogens, such as the case of MERS in bats, with the camel being an intermediate host in the transmission from animal to human (Corman et al. <xref ref-type="bibr" rid="CR73">2014a</xref>, <xref ref-type="bibr" rid="CR74">b</xref>).</p><p id="Par30">Dromedary camels are a staple in the diets and lives of humans like their cattle and pig counterparts, but research on their zoonotic disease potential is lacking in comparison. When the map of camel population density is compared to the geographic site of published papers found in this review, we see that the two have high levels of intersection in Africa, Asia, and the Middle East (Figures <xref rid="Fig1" ref-type="fig">1</xref> and <xref rid="Fig3" ref-type="fig">3</xref>). However, these maps also show that in many instances camel-borne zoonoses are not restricted to areas of high camel numbers and human infections can and do occur in countries with very low camel populations, and even in countries with no camels as a person may be exposed in one region and travel to another. Therefore, veterinarians, farmers, and others working in close contact with camels and camel products should be cognizant of these potential pathogens, not just in areas where camels are raised but also where camel products may be processed and transported. Additionally, physicians must be aware of where their patients have traveled. Knowledge of potential camel-borne diseases is thus important for researchers and health workers to consider globally.</p></sec><sec id="Sec8"><title>Conclusion</title><p id="Par31">Camels are not common outside of hot and arid areas such as sub-Saharan Africa or the Middle East, but knowledge of their potential carrier status is important to researchers, zoo personnel, and travelers. The MERS and Ebola outbreaks in recent years have shown how rapidly pathogens can travel and erupt in novel human populations; population expansion and a lack of extensive healthcare systems make camel-endemic areas a potential hot spot for zoonotic spillover. Many of the zoonotic pathogens of camels are a current or possible future risk to human health and must be considered by medical professionals, especially in light of the increased use of camels as a growing protein source globally. As we collect epidemiologic data on the routes of transmission and sources of these infectious agents, we become better prepared to manage and mitigate their impact on humans. Camel milk and meat act as a point source for infection and should be managed with proper slaughter protocols, pasteurization, and improved overall sanitation practices. Dromedary camels also act as a significant source and amplifier for vector-borne disease; therefore, vaccination of camels, control of mosquitoes and ticks, insecticide application, and consistent screening will help control infection rates in camels and humans. In this literature review, we highlight a number of camel-borne zoonotic diseases. The number of pathogens and spillover events will most likely continue to grow as human and camel populations increase and increasingly intersect.</p></sec></body><back><ack><title>Acknowledgements</title><p>This work was made possible by the generous support of the American people through the United States Agency for International Development (USAID) Emerging Pandemic Threats PREDICT Cooperative Agreement No. AID-OAA-A-14-00102. The contents are the responsibility of the authors and do not necessarily reflect the views or the policy of USAID or the US Government, and no official endorsement should be inferred. Thank you to Smithsonian Conservation Biology Institute and Saint Louis Zoo Institute for Conservation Medicine for additional funding to complete this research. 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