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Bushmeat and Emerging Infectious Diseases: Lessons from Africa

Identifieur interne : 000124 ( Pmc/Corpus ); précédent : 000123; suivant : 000125

Bushmeat and Emerging Infectious Diseases: Lessons from Africa

Auteurs :

Source :

RBID : PMC:7123567

Abstract

Zoonotic diseases are the main contributor to emerging infectious diseases (EIDs) and present a major threat to global public health. Bushmeat is an important source of protein and income for many African people, but bushmeat-related activities have been linked to numerous EID outbreaks, such as Ebola, HIV, and SARS. Importantly, increasing demand and commercialization of bushmeat is exposing more people to pathogens and facilitating the geographic spread of diseases. To date, these linkages have not been systematically assessed. Here we review the literature on bushmeat and EIDs for sub-Saharan Africa, summarizing pathogens (viruses, fungi, bacteria, helminths, protozoan, and prions) by bushmeat taxonomic group to provide for the first time a comprehensive overview of the current state of knowledge concerning zoonotic disease transmission from bushmeat into humans. We conclude by drawing lessons that we believe are applicable to other developing and developed regions and highlight areas requiring further research to mitigate disease risk.


Url:
DOI: 10.1007/978-3-319-22246-2_24
PubMed: NONE
PubMed Central: 7123567

Links to Exploration step

PMC:7123567

Le document en format XML

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<p id="Par1">Zoonotic diseases are the main contributor to emerging infectious diseases (EIDs) and present a major threat to global public health. Bushmeat is an important source of protein and income for many African people, but bushmeat-related activities have been linked to numerous EID outbreaks, such as Ebola, HIV, and SARS. Importantly, increasing demand and commercialization of bushmeat is exposing more people to pathogens and facilitating the geographic spread of diseases. To date, these linkages have not been systematically assessed. Here we review the literature on bushmeat and EIDs for sub-Saharan Africa, summarizing pathogens (viruses, fungi, bacteria, helminths, protozoan, and prions) by bushmeat taxonomic group to provide for the first time a comprehensive overview of the current state of knowledge concerning zoonotic disease transmission from bushmeat into humans. We conclude by drawing lessons that we believe are applicable to other developing and developed regions and highlight areas requiring further research to mitigate disease risk.</p>
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<pmc article-type="chapter-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="publisher-id">978-3-319-22246-2</journal-id>
<journal-id journal-id-type="doi">10.1007/978-3-319-22246-2</journal-id>
<journal-id journal-id-type="nlm-ta">Problematic Wildlife</journal-id>
<journal-title-group>
<journal-title>Problematic Wildlife</journal-title>
<journal-subtitle>A Cross-Disciplinary Approach</journal-subtitle>
</journal-title-group>
<isbn publication-format="print">978-3-319-22245-5</isbn>
<isbn publication-format="electronic">978-3-319-22246-2</isbn>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmc">7123567</article-id>
<article-id pub-id-type="publisher-id">24</article-id>
<article-id pub-id-type="doi">10.1007/978-3-319-22246-2_24</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Bushmeat and Emerging Infectious Diseases: Lessons from Africa</article-title>
</title-group>
<contrib-group content-type="book editors">
<contrib contrib-type="editor">
<name>
<surname>Angelici</surname>
<given-names>Francesco M.</given-names>
</name>
<address>
<email>frangema@tiscali.it</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
</contrib>
<aff id="Aff1">FIZV, Rome, Italy</aff>
</contrib-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Kurpiers</surname>
<given-names>Laura A.</given-names>
</name>
<address>
<email>Laura.Kurpiers@bucknell.edu</email>
</address>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Schulte-Herbrüggen</surname>
<given-names>Björn</given-names>
</name>
<address>
<email>bjorn.schulte-herbruggen@su.se</email>
</address>
<xref ref-type="aff" rid="Aff3">3</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ejotre</surname>
<given-names>Imran</given-names>
</name>
<address>
<email>Imran.Ejotre@bucknell.edu</email>
</address>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Reeder</surname>
<given-names>DeeAnn M.</given-names>
</name>
<address>
<email>DeeAnn.Reeder@bucknell.edu</email>
</address>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<aff id="Aff2">
<label>2</label>
<institution-wrap>
<institution-id institution-id-type="GRID">grid.253363.2</institution-id>
<institution-id institution-id-type="ISNI">0000000122979828</institution-id>
<institution>Department of Biology,</institution>
<institution>Bucknell University,</institution>
</institution-wrap>
Lewisburg, PA 17837 USA</aff>
<aff id="Aff3">
<label>3</label>
<institution-wrap>
<institution-id institution-id-type="GRID">grid.10548.38</institution-id>
<institution-id institution-id-type="ISNI">0000000419369377</institution-id>
<institution>Stockholm Resilience Centre,</institution>
<institution>Stockholm University,</institution>
</institution-wrap>
10691 Stockholm, Sweden</aff>
</contrib-group>
<pub-date pub-type="epub">
<day>21</day>
<month>09</month>
<year>2015</year>
</pub-date>
<fpage>507</fpage>
<lpage>551</lpage>
<permissions>
<copyright-statement>© Springer International Publishing Switzerland 2016</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">Zoonotic diseases are the main contributor to emerging infectious diseases (EIDs) and present a major threat to global public health. Bushmeat is an important source of protein and income for many African people, but bushmeat-related activities have been linked to numerous EID outbreaks, such as Ebola, HIV, and SARS. Importantly, increasing demand and commercialization of bushmeat is exposing more people to pathogens and facilitating the geographic spread of diseases. To date, these linkages have not been systematically assessed. Here we review the literature on bushmeat and EIDs for sub-Saharan Africa, summarizing pathogens (viruses, fungi, bacteria, helminths, protozoan, and prions) by bushmeat taxonomic group to provide for the first time a comprehensive overview of the current state of knowledge concerning zoonotic disease transmission from bushmeat into humans. We conclude by drawing lessons that we believe are applicable to other developing and developed regions and highlight areas requiring further research to mitigate disease risk.</p>
</abstract>
<kwd-group xml:lang="en">
<title>Keywords</title>
<kwd>Bushmeat</kwd>
<kwd>Africa</kwd>
<kwd>Emerging infectious disease</kwd>
<kwd>Hunting</kwd>
<kwd>Cross-species transmission</kwd>
</kwd-group>
<custom-meta-group>
<custom-meta>
<meta-name>issue-copyright-statement</meta-name>
<meta-value>© Springer International Publishing Switzerland 2016</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
<body>
<sec id="Sec1" sec-type="introduction">
<title>Introduction</title>
<p id="Par2">Emerging infectious diseases (EIDs) are human diseases that are either newly discovered or are increasing in incidence or geographical range. Some diseases, such as measles, sleeping sickness, and bubonic plague, emerged in prehistoric or ancient times (Babbott and Gordon
<xref ref-type="bibr" rid="CR19">1954</xref>
; Hays
<xref ref-type="bibr" rid="CR92">2005</xref>
; Steverding
<xref ref-type="bibr" rid="CR225">2008</xref>
), whereas others, such as Ebola virus, Nipah virus, and SARS, emerged more recently (World Health Organization
<xref ref-type="bibr" rid="CR273">1978</xref>
; Chua et al.
<xref ref-type="bibr" rid="CR46">2000</xref>
; Guan et al.
<xref ref-type="bibr" rid="CR86">2003</xref>
). The trend of EID emergence is accelerating: over 300 distinct emerging disease events have been recorded in the last six decades and more than 35 new infectious diseases have emerged in humans since 1980 (Lederberg et al.
<xref ref-type="bibr" rid="CR126">2003</xref>
; Jones et al.
<xref ref-type="bibr" rid="CR103">2008</xref>
).</p>
<p id="Par3">Upwards of 75 % of EIDs in humans are of zoonotic origin, which means the pathogen originates in animals and is transmitted to humans (Taylor et al.
<xref ref-type="bibr" rid="CR235">2001</xref>
; Jones et al.
<xref ref-type="bibr" rid="CR103">2008</xref>
; Karesh and Noble
<xref ref-type="bibr" rid="CR108">2009</xref>
). Although many zoonotic pathogen spillovers arise in domestic animals, including livestock, the majority (71.8 %) of zoonotic EIDs arise from wildlife species (Jones et al.
<xref ref-type="bibr" rid="CR103">2008</xref>
). In many developing countries, domesticated animals live in close proximity to wildlife. This facilitates the movement of pathogens between them and to humans through interactions with sylvatic disease cycles or through two-step wildlife-to-domestic animal-to-human emergences. Examples include rabies infections, which move between wildlife and domestic dogs, with recurring spillovers to humans; and the Henipah viruses, in which
<italic>Pteropus</italic>
flying foxes are the reservoir host and domestic pigs or horses are amplifier hosts from which spillovers to humans have been documented (Childs et al.
<xref ref-type="bibr" rid="CR45">2007</xref>
; Daszak et al.
<xref ref-type="bibr" rid="CR51">2007</xref>
). Not surprisingly, the most devastating pandemics in human history, the Black Death, Spanish influenza, and HIV/AIDS, were all caused by zoonoses from wildlife (Morens et al.
<xref ref-type="bibr" rid="CR162">2008</xref>
).</p>
<p id="Par4">Zoonotic diseases can spill between animal hosts and humans in a variety of ways, including through (a) shared vectors, such as mosquitoes for malaria, (b) indirect contact, such as exposure to rodent feces in a peridomestic setting, or (c) direct contact with an animal through consumption, animal bites, scratches, body fluids, tissues, and excrement (Wolfe et al.
<xref ref-type="bibr" rid="CR269">2005a</xref>
). Most pathogens infecting animals fail to make the jump into humans, but 33 % of zoonotic pathogens (~286 out of 868 zoonotic pathogen species studied) that have spilled over are known to be transmissible between humans (Taylor et al.
<xref ref-type="bibr" rid="CR235">2001</xref>
). Of all EIDs, zoonotic spillovers from wildlife have been identified as the most significant, growing threat to global health (Cleaveland et al.
<xref ref-type="bibr" rid="CR47">2007</xref>
; Jones et al.
<xref ref-type="bibr" rid="CR103">2008</xref>
).</p>
<p id="Par5">Recent evidence highlights the link between infectious diseases and biodiversity loss, land use changes, and habitat fragmentation (Cleaveland et al.
<xref ref-type="bibr" rid="CR47">2007</xref>
; Maganga et al.
<xref ref-type="bibr" rid="CR140">2014</xref>
; Gottdenker et al.
<xref ref-type="bibr" rid="CR82">2014</xref>
). Although additional research on the relationship between habitat degradation and EIDs is needed, Gottdenker et al. (
<xref ref-type="bibr" rid="CR82">2014</xref>
) reviewed 305 studies incorporating a broad variety of diseases and found that the most common land use change types related to zoonotic disease transmission were deforestation, habitat fragmentation, agricultural development, irrigation, and urbanization. Functionally, the mechanisms influencing disease spillover include disruption of food web structures, changes in host–pathogen interactions, and mixing of pathogen gene pools resulting in increased pathogen genetic diversity (Jones et al.
<xref ref-type="bibr" rid="CR104">2013</xref>
). Many studies have shown that habitat fragmentation and biodiversity loss correspond to an increase in disease and pathogen abundance and diversity within a host species (Allan et al.
<xref ref-type="bibr" rid="CR9">2003</xref>
; Gillespie et al.
<xref ref-type="bibr" rid="CR76">2005</xref>
; Keesing et al.
<xref ref-type="bibr" rid="CR112">2006</xref>
; Salzer et al.
<xref ref-type="bibr" rid="CR208">2007</xref>
; Cottontail et al.
<xref ref-type="bibr" rid="CR48">2009</xref>
; Young et al.
<xref ref-type="bibr" rid="CR276">2014</xref>
). Specifically, the emergence or re-emergence of many zoonotic diseases including yellow fever, Lyme disease, hantavirus pulmonary syndrome, Nipah virus encephalitis, influenza, rabies, malaria, and human African trypanosomiasis have been linked to anthropogenic habitat changes (Jones et al.
<xref ref-type="bibr" rid="CR104">2013</xref>
).</p>
<p id="Par6">Many of these human environmental changes are occurring in sub-Saharan Africa where human bushmeat activities have been linked to numerous virulent disease outbreaks, including Ebola (Leroy et al.
<xref ref-type="bibr" rid="CR132">2004a</xref>
), HIV (Van Heuverswyn and Peeters
<xref ref-type="bibr" rid="CR249">2007</xref>
), and monkeypox (Rimoin et al.
<xref ref-type="bibr" rid="CR200">2010</xref>
). Pathogen spillover from bushmeat can occur through consumption; however, the main risks are associated with exposure to body fluids and feces during handling and butchering (Kilonzo et al.
<xref ref-type="bibr" rid="CR115">2014</xref>
; Paige et al.
<xref ref-type="bibr" rid="CR180">2014</xref>
). Historically, when a spillover occurred, the likelihood of an epidemic was limited because hunter-gatherer tribes were generally small and widely dispersed, hampering disease transmission between groups of people. Once agricultural expansion occurred, human population densities increased, and people became better connected, diseases could spread more easily. As a result, transmissions of infectious diseases from animals to humans have led to devastating outcomes across the globe (LeBreton et al.
<xref ref-type="bibr" rid="CR124">2006</xref>
). EIDs cause hundreds of thousands of deaths annually (Bogich et al.
<xref ref-type="bibr" rid="CR29">2012</xref>
). Some outbreaks have spread across large regions and became pandemics, costing the global economy tens of billions of dollars (e.g., SARS, H5N1, the 2014–2015 West African Ebola outbreak) and bringing entire nations to the brink of economic collapse.</p>
<p id="Par7">In this review, we explore the links between bushmeat-related activities and EIDs in sub-Saharan Africa, where the vast majority of African emerging infectious zoonotic diseases occur (Jones et al.
<xref ref-type="bibr" rid="CR103">2008</xref>
). The recent Ebola outbreaks have highlighted the potential role of bushmeat as a source of pathogens, but a comprehensive review of the different pathogens that may emerge from wildlife through bushmeat-related activities is lacking. Although we are in no way suggesting that this issue is more important than other pressing health crises in sub-Saharan Africa (such as malaria prevention/treatment and improving healthcare infrastructure), we argue that a better assessment of the public health threats associated with this human-wildlife interaction is warranted and necessary to improve management of future disease outbreaks.</p>
</sec>
<sec id="Sec2">
<title>Bushmeat</title>
<p id="Par8">The term “bushmeat” refers to the meat derived from wild animals for human consumption (Milner-Gulland and Bennett
<xref ref-type="bibr" rid="CR158">2003</xref>
) (Fig.
<xref rid="Fig1" ref-type="fig">24.1</xref>
). It includes a wide range of animals, such as invertebrates, amphibians, insects, fish, reptiles, birds, and mammals, including as many as 500 species in sub-Saharan Africa (Ape Alliance
<xref ref-type="bibr" rid="CR12">2006</xref>
). Although research has focused largely on mammals and, to a lesser extent, birds, theoretically any wildlife species harvested for bushmeat could be a potential source of zoonotic disease that can spillover during the hunting, butchering, and preparation process (Wolfe et al.
<xref ref-type="bibr" rid="CR266">2000</xref>
; Karesh and Noble
<xref ref-type="bibr" rid="CR108">2009</xref>
). Hunters face risk of injury from live animals, which might allow animal blood to enter the hunter’s bloodstream through open wounds. While small animals can be carried in bags, large animals are commonly carried on the shoulder or back, bringing the hunter in close contact with the animal and facilitating transfer of body fluids (LeBreton et al.
<xref ref-type="bibr" rid="CR124">2006</xref>
). The highest risk of disease transmission occurs during the butchering of animals, e.g. skinning, opening of the body cavity, removal of organs, and cutting of meat. More people butcher than hunt animals (83 % and 42 %, respectively, LeBreton et al.
<xref ref-type="bibr" rid="CR124">2006</xref>
) and butchering involves the use of sharp tools, which may lead to cuts during the process. Subramanian (
<xref ref-type="bibr" rid="CR227">2012</xref>
) found that 38 % of respondents cut themselves on a regular basis during butchering. Women are especially at risk of disease transmission as they engage more often in butchering and in food preparation than men. In discussing the links between bushmeat and disease, we refer to this all-encompassing suite of risky behaviors as “bushmeat-related activities.”
<fig id="Fig1">
<label>Fig. 24.1</label>
<caption>
<p>Bushmeat being smoked in rural South Sudan; photo credit Adrian Garside</p>
</caption>
<graphic xlink:href="332204_1_En_24_Fig1_HTML" id="MO1"></graphic>
</fig>
</p>
<p id="Par9">Nonhuman primates, rodents, and bats have all been linked to the spillover of zoonotic diseases into humans (Cleaveland et al.
<xref ref-type="bibr" rid="CR47">2007</xref>
; Jones et al.
<xref ref-type="bibr" rid="CR103">2008</xref>
; Kilonzo et al.
<xref ref-type="bibr" rid="CR115">2014</xref>
). A review of the West and Central African bushmeat literature including market, offtake, and consumption surveys documented a total of 177 species from 25 orders that were harvested for bushmeat, including 134 (76 %) mammal species, 24 (14 %) bird species, 18 (10 %) reptile species, and 1 (<1 %) amphibian species (Taylor et al.
<xref ref-type="bibr" rid="CR236">2015</xref>
). Among mammals, the largest group was primates (48 species) including western gorillas (
<italic>Gorilla gorilla</italic>
), bonobos (
<italic>Pan paniscus</italic>
), and common chimpanzees (
<italic>Pan troglodytes</italic>
), followed by ungulates (34 species), carnivores (22 species), and rodents (16 species). In terms of biomass offtake, however, ungulates are generally the most prominent group. Although the Taylor et al. (
<xref ref-type="bibr" rid="CR236">2015</xref>
) study is very comprehensive, it only included studies that: (1) provided a quantitative measure of bushmeat offtake, consumption, and/or market availability/sales; (2) used non-biased data collection methods and systematically sampled settlements/hunters to prevent selection bias; (3) identified carcasses to the species level; and (4) recorded either the number of carcasses or the total biomass (kg). For a more inclusive and general review of existing Central African bushmeat studies, see Wilkie and Carpenter (
<xref ref-type="bibr" rid="CR262">1999</xref>
), and for West African studies, see Schulte-Herbrüggen (
<xref ref-type="bibr" rid="CR210">2011</xref>
). Fa et al. (
<xref ref-type="bibr" rid="CR66">2006</xref>
) found that of the approximately one million carcasses traded in the Cross-Sanaga region of Nigeria and Cameroon, 99 % were mammals; of which around 40 % were ungulates, 30 % rodents, and nearly 15 % primates. However, as wildlife populations become depleted, such as near urban areas and intensively used agricultural landscapes, smaller bodied mammals comprise a larger share of hunters’ offtake (Bowen-Jones et al.
<xref ref-type="bibr" rid="CR33">2003</xref>
; Schulte-Herbrüggen et al.
<xref ref-type="bibr" rid="CR211">2013a</xref>
).</p>
<sec id="Sec3">
<title>Livelihood Importance</title>
<p id="Par10">Humans have hunted wild animals for consumption and to protect their crops for millennia (Shipman et al.
<xref ref-type="bibr" rid="CR215">1981</xref>
; Grubb et al.
<xref ref-type="bibr" rid="CR85">1998</xref>
; Davies et al.
<xref ref-type="bibr" rid="CR53">2007</xref>
), and it remains an important source of food and income security among rural communities today (de Merode et al.
<xref ref-type="bibr" rid="CR56">2004</xref>
; Brashares et al.
<xref ref-type="bibr" rid="CR35">2011</xref>
). Bushmeat is an important source of animal protein in many West and Central African countries, with up to 90 % of total animal protein consumption coming from wild animals (Fa et al.
<xref ref-type="bibr" rid="CR65">2003</xref>
). Overall, the contribution of bushmeat to protein and food security is generally lower in urban than rural areas and is highest among remote rural communities (Brashares et al.
<xref ref-type="bibr" rid="CR35">2011</xref>
). For example, the relative importance of bushmeat in the diet of rural Gabonese households ranged from 13 % of total household consumption value in a village near a town to 25 % in a remote community (Starkey
<xref ref-type="bibr" rid="CR223">2004</xref>
). Similarly, for rural Equatorial Guinea, Allebone-Webb (
<xref ref-type="bibr" rid="CR10">2008</xref>
) showed that bushmeat consumption contributed 43 % to total protein consumption in a village with poor transport links, but only 18 % in a village with good connections. In remote Cameroonian communities with very few opportunities for purchasing alternative protein sources, bushmeat comprised 80–98 % of animal protein consumption (Muchaal and Ngandjui
<xref ref-type="bibr" rid="CR165">1999</xref>
). In rural communities with relatively good market access and low levels of bushmeat consumption, the importance of bushmeat for food has been shown to increase seasonally during the agricultural lean season (e.g. the planting season between harvests) when farming households receive little income (Dei
<xref ref-type="bibr" rid="CR57">1989</xref>
, de Merode et al.
<xref ref-type="bibr" rid="CR56">2004</xref>
, Schulte-Herbrüggen et al.
<xref ref-type="bibr" rid="CR212">2013b</xref>
) and during the dry season when fish is not available (Poulsen et al.
<xref ref-type="bibr" rid="CR193">2009</xref>
). Bushmeat is also an important source of nutrients, especially among children. Evidence from rural Madagascar shows that removing bushmeat consumption would result in a 29 % increase in the number of children suffering from anemia and triple the cases of anemia among children in the poorest households (Golden et al.
<xref ref-type="bibr" rid="CR80">2011</xref>
).</p>
<p id="Par11">Most hunters sell at least part of their harvest making it an important source of income, especially where alternative income-generating activities are lacking. The importance of bushmeat in household economies varies across sites and individual hunting households, ranging from 38 % to more than 90 % of the total cash income earned (reviewed in Schulte-Herbrüggen
<xref ref-type="bibr" rid="CR210">2011</xref>
). In rural Gabon, hunting accounts for up to 72 % of household incomes, with the proportion rising in poorer, more remote communities (Starkey
<xref ref-type="bibr" rid="CR223">2004</xref>
). Hunters are also more likely to sell large animals and keep small animals for their own consumption, because the latter fetch a lower price per animal and may be less marketable (van Vliet and Nasi
<xref ref-type="bibr" rid="CR253">2008</xref>
). Finally, households facing income shortages during the agricultural lean season and requiring cash income to pay for urgent expenditures, such as hospital bills, are more likely to sell bushmeat than keep it for own consumption (de Merode et al.
<xref ref-type="bibr" rid="CR56">2004</xref>
).</p>
<p id="Par12">Overall, income from bushmeat sales can be lucrative and compare favorably with alternative work in many rural places. Vega et al. (
<xref ref-type="bibr" rid="CR254">2013</xref>
) found that commercial hunters in Equatorial Guinea generated a mean of US$2000 per year from bushmeat sales. Hunters supplying markets in Central African logging concessions earned twice the income of junior technicians working at a logging company (Tieguhong and Zwolinski
<xref ref-type="bibr" rid="CR238">2009</xref>
). Rural Kenya hunters can earn 2.5 times the average salary in the area (Fitzgibbon et al.
<xref ref-type="bibr" rid="CR70">1995</xref>
), and Ghanaian hunters can earn income similar to that of a graduate entering Wildlife Service, and up to 3.5 times the government minimum wage (Ntiamoa-Baidu
<xref ref-type="bibr" rid="CR176">1998</xref>
). Very successful Zambian hunters have been reported earning just below the mean annual income in a single hunting trip (Brown
<xref ref-type="bibr" rid="CR36">2007</xref>
).</p>
<p id="Par13">The sale of bushmeat historically occurred at a local level, but with increased transportation routes and globalization, the bushmeat trade is expanding to supply urban and international demand. In the past, novel pathogens entering the rural communities may not have spread beyond the community, but this is no longer the case as remote rural areas are connected to urban areas, and increased global trade networks and air travel increases the risk of disease transmission worldwide (Brashares et al.
<xref ref-type="bibr" rid="CR35">2011</xref>
). This expanding trade network links hunters to consumers, and with many people along this commodity chain coming into contact with bushmeat, the opportunity for disease spillover can occur at many points. For example, the commodity chain supplying bushmeat to an urban market in Ghana includes hunters, wholesalers, market traders, restaurant owners, and consumers (Mendelson et al.
<xref ref-type="bibr" rid="CR156">2003</xref>
). The bushmeat commodity chain supplying an urban market in Democratic Republic of the Congo is comprised of hunters, porters who carry the meat to the road, the bicycle traders who transport the meat into town, and the market-stall owners who sell the bushmeat to consumers (de Merode and Cowlishaw
<xref ref-type="bibr" rid="CR55">2006</xref>
). A recent study from Ghana estimates that a minimum of 128,000 bats are sold each year through a commodity chain that stretches up to 400 km and involves multiple vendors (Kamins et al.
<xref ref-type="bibr" rid="CR105">2011a</xref>
). In Zambia, Mozambique, and Malawi, well-developed and complex rural-urban trade supply networks link rural hunters to urban consumers who are willing to pay high prices for bushmeat (Barnett
<xref ref-type="bibr" rid="CR24">1997</xref>
). Understanding commodity chains is important, as pathogens likely remain viable for some period after an animal is killed. For example, Prescott et al. (
<xref ref-type="bibr" rid="CR198">2015</xref>
) demonstrated that Ebola virus remains viable on monkey carcasses for at least seven days, with viral RNA detectable for 10 weeks.</p>
</sec>
<sec id="Sec4">
<title>Scale of Bushmeat Harvest in Sub-Saharan Africa</title>
<p id="Par14">Bushmeat hasbecome a multi-million dollar business due to a growing human population and is now serving both subsistence and trade objectives. Harvest volumes have been estimated at 12,000 tones per year in the Cross-Sanaga rivers region of Nigeria and Cameroon (Fa et al.
<xref ref-type="bibr" rid="CR66">2006</xref>
), 120,000 tones per year in Côte d’Ivoire (Caspary
<xref ref-type="bibr" rid="CR42">1999</xref>
), 385,000 tons per year in Ghana (Ntiamoa-Baidu
<xref ref-type="bibr" rid="CR176">1998</xref>
), and at total of 1–4.9 million tons per year in Central African forests (Wilkie and Carpenter
<xref ref-type="bibr" rid="CR262">1999</xref>
; Fa et al.
<xref ref-type="bibr" rid="CR64">2002</xref>
).</p>
<p id="Par15">However, it is important to recognize that our understanding of the scale of bushmeat harvest is limited by the availability of information and hence current regional harvest estimates might underestimate actual harvest volumes. Despite substantial effort in recent years, our knowledge is still site-specific and data are lacking from many regions. Most surveys have been restricted to relatively small areas or market catchments from which national estimates were extrapolated. Research efforts have focused on Central Africa with some data available for 60 % of countries compared to 30 % of West African countries (Taylor et al.
<xref ref-type="bibr" rid="CR236">2015</xref>
). A large number of sites with detailed bushmeat data are concentrated in the Cross-Sanaga region of Nigeria and Cameroon, where Fa et al. (
<xref ref-type="bibr" rid="CR66">2006</xref>
) collected market data at 86 sites, hence presenting a geographical bias in our understanding of bushmeat harvest. Furthermore, the majority of available data samples (79.3 % and 53.6 %, in West and Central Africa, respectively) identified by Taylor et al. (
<xref ref-type="bibr" rid="CR236">2015</xref>
) come from market surveys with poorly defined catchment areas, compared to offtake and consumption surveys. Strong variation between individual estimates highlights the problems with extrapolation of survey data to national or regional levels and the effects of sampling strategies (hunter versus market surveys), timing of survey (open season versus lean season), survey location, and extrapolation methods. Individual figures should therefore be treated with caution, but the overall message remains: bushmeat is harvested at an enormous scale exposing those involved in the bushmeat commodity chain to zoonotic diseases.</p>
</sec>
<sec id="Sec5">
<title>Drivers of Increased Bushmeat Hunting and Disease Risks</title>
<p id="Par16">The current scale of bushmeat hunting isprimarily the result of socio-demographic changes (Wilkie and Carpenter
<xref ref-type="bibr" rid="CR262">1999</xref>
). Africa’s human population has risen from 0.2 billion in 1950 to 0.9 billion in 2013 and is expected to rise to 2.2 billion by 2050 (United Nations
<xref ref-type="bibr" rid="CR243">2013</xref>
). Where alternative sources of animal protein and income are scarce, human population growth has been linked to increasing hunting intensity (Brashares et al.
<xref ref-type="bibr" rid="CR34">2001</xref>
).</p>
<p id="Par17">Bushmeat has been and remains a staple source of animal protein among the rural poor, yet recent attention has focused on urban consumers of bushmeat as a driver of increased hunting. Urban consumers generally have a range of meat sources from which to choose, but value bushmeat for its taste, cultural connotations, and as a luxury food item (Fa et al.
<xref ref-type="bibr" rid="CR67">2009</xref>
). While urban consumers generally consume less bushmeat than rural consumers (Brashares et al.
<xref ref-type="bibr" rid="CR35">2011</xref>
), urban populations in Africa have increased dramatically from about 15 % of the total population in 1950 to 40 % in 2014 (United Nations
<xref ref-type="bibr" rid="CR244">2014</xref>
) and have created a strong demand for bushmeat and hence market for rural hunters.</p>
<p id="Par18">The increasing demand for bushmeat has been accompanied by changes in hunting technology and improvements in hunting efficiency. Traditional hunting tools, such as nets and bow and arrow, have been replaced with more modern tools of guns and snares. Modern guns have an up to 25-times higher rate of return compared to traditional weapons (Wilkie and Curran
<xref ref-type="bibr" rid="CR263">1991</xref>
), substantially increasing the ease and cost-effectiveness of hunting (Alvard
<xref ref-type="bibr" rid="CR13">1995</xref>
). This enables hunters to catch more animals and sell a larger part of their catch (Bowen-Jones and Pendry
<xref ref-type="bibr" rid="CR32">1999</xref>
; Bowen-Jones et al.
<xref ref-type="bibr" rid="CR33">2003</xref>
; Nasi et al.
<xref ref-type="bibr" rid="CR172">2008</xref>
).</p>
<p id="Par19">Hunting efficiency has also improved as remote forests have become more accessible through the construction of logging roads and improved transportation (Wilkie et al.
<xref ref-type="bibr" rid="CR264">1992</xref>
; Auzel and Wilkie
<xref ref-type="bibr" rid="CR17">2000</xref>
). For example, after the construction of 140 km of logging roads in northern Congo, the average time for a hunting trip was reduced from 12 to 2 hours (Wilkie et al.
<xref ref-type="bibr" rid="CR265">2001</xref>
). Development of rural businesses, such as timber companies, attracts workers and their families to remote locations, increasing bushmeat demand, especially when no hunting regulations are in place and alternative protein sources are not provided (Auzel and Wilkie
<xref ref-type="bibr" rid="CR17">2000</xref>
; Bennett and Gumal
<xref ref-type="bibr" rid="CR25">2001</xref>
; Poulsen et al.
<xref ref-type="bibr" rid="CR193">2009</xref>
). The effect of logging company presence on hunting pressure was documented in Gabon where ape populations decreased 50 % between 1983 and 2000 as a result of hunting (Walsh et al.
<xref ref-type="bibr" rid="CR258">2003</xref>
). In addition, agricultural expansion and mining have exerted a strong force in changing the African landscape and influencing human migration patterns (Norris et al.
<xref ref-type="bibr" rid="CR175">2010</xref>
). Due to increased access, people are brought into closer contact with wildlife, which facilitates accessibility to bushmeat hunting and makes transportation of bushmeat from rural to urban areas easier and more cost-effective (Wolfe et al.
<xref ref-type="bibr" rid="CR269">2005a</xref>
).</p>
<p id="Par20">Along with increased ease of transportation comes the opportunity for bushmeat to be traded on the international market. The international trade in bushmeat has recently gained attention as both a driver of bushmeat hunting and the cross-border spread of zoonotic diseases. Illegal wildlife trade is the second-largest black market worldwide, involving millions of animals and estimated to be worth US$50–150 billion per year (United Nations Environment Programme
<xref ref-type="bibr" rid="CR246">2014</xref>
). Case studies at airports screening passenger luggage for bushmeat estimated that approximately 5tons of bushmeat per week arrive at Paris Roissy-Charles de Gaulle airport (Chaber et al.
<xref ref-type="bibr" rid="CR43">2010</xref>
) and 8.6 tons per year at Zurich and Geneva airports (Falk et al.
<xref ref-type="bibr" rid="CR68">2013</xref>
). As bushmeat hunting, globalization, and human interconnectedness increase, the potential for zoonoses leading to EIDs also increases. This risk was highlighted when retroviruses (e.g., simian foamy virus) and herpesviruses (cytomegalovirus and lymphocryptovirus) were found in confiscated primates at US airports (Smith et al.
<xref ref-type="bibr" rid="CR222">2012</xref>
).</p>
</sec>
</sec>
<sec id="Sec6">
<title>Bushmeat as a Source of Zoonotic Diseases in Sub-Saharan Africa</title>
<p id="Par21">Indisputable evidence of the transmission of pathogens from wildlife to humans exists only for relatively few cases because the standard of proof is very high. Nevertheless, the evidence for spillovers is very strong and many pathogens can be classified as very likely to spillover (Jones et al.
<xref ref-type="bibr" rid="CR103">2008</xref>
; Kilonzo et al.
<xref ref-type="bibr" rid="CR115">2014</xref>
). Furthermore, countless pathogen species of zoonotic potential will likely be discovered as surveillance increases (Taylor et al.
<xref ref-type="bibr" rid="CR235">2001</xref>
; Jones et al.
<xref ref-type="bibr" rid="CR103">2008</xref>
). Our close phylogenetic relationship with nonhuman primates increases the likelihood that pathogen spillover from these animals to humans will cause infection (Childs et al.
<xref ref-type="bibr" rid="CR45">2007</xref>
). Moreover, it is not surprising that many studies have focused on spillover events from nonhuman primates to humans given the high prevalence of these largely diurnal mammals in the bushmeat trade (Taylor et al.
<xref ref-type="bibr" rid="CR236">2015</xref>
). For instance, nonhuman primates of the family Hominidae include the Gorillinae and Paninae, which show a genetic difference of only 2 % or less with humans (Gonzalez et al.
<xref ref-type="bibr" rid="CR81">2013</xref>
), and members of these subfamilies share many morphological, physiological, and ecological features that may have a direct role in the transmission of infectious diseases (Davies and Pedersen
<xref ref-type="bibr" rid="CR52">2008</xref>
). Cleaveland et al. (
<xref ref-type="bibr" rid="CR47">2007</xref>
), in their assessment of the risk of disease emergence by taxa, found that the relative risk of disease emergence was highest for bats, followed closely by primates, then ungulates and rodents. There have been surprisingly few studies of the connection between hunting of birds or other vertebrates and EIDs, especially in Africa, but surveillance for zoonotic pathogens in African birds is strongly needed (e.g., for avian influenza tracking see Simulundu et al.
<xref ref-type="bibr" rid="CR217">2011</xref>
,
<xref ref-type="bibr" rid="CR218">2014</xref>
).</p>
<p id="Par22">The characteristics of different species may render them more or less susceptible to hunting. Behavioral traits such as communal nesting, large-group living, loud acoustic performances, and a diurnal lifestyle—which are found in many primate species—may facilitate the detection and harvesting of several individuals at one time (Bodmer
<xref ref-type="bibr" rid="CR28">1995</xref>
). Taste preferences for certain species influence hunters’ decisions as do attempts to maximize returns by preferring large-bodied animals that provide more food or fetch a higher price when sold than small-bodied species (Bodmer
<xref ref-type="bibr" rid="CR28">1995</xref>
). Bats, especially the larger fruit bats popular in the bushmeat trade, are susceptible to hunting because they are often found in large, sometimes vocal groups that are visible during the day or in high concentrations in caves (Mickleburgh et al.
<xref ref-type="bibr" rid="CR157">2009</xref>
). Increased human encroachment in recent decades (Kamins et al.
<xref ref-type="bibr" rid="CR106">2011b</xref>
) has driven some bat species to become peridomestic (O’Shea et al.
<xref ref-type="bibr" rid="CR177">2011</xref>
; Plowright et al.
<xref ref-type="bibr" rid="CR191">2011</xref>
), which renders them easy targets for hunting. Finally, sick animals may be less successful in evading hunters and hence more easily hunted, thereby increasing the risk of disease transmission to hunters.</p>
<p id="Par23">In addition to the behavioral traits that may influence which species are hunted, physiological traits of these species may make them more likely to harbor and transmit diseases. For example, bats, which are present in the bushmeat trade and comprise the highest risk among all wildlife for harboring emerging diseases (Cleaveland et al.
<xref ref-type="bibr" rid="CR47">2007</xref>
), present unique traits that suit them to hosting pathogens. These traits include: (1) relatively long lifespans for their body size (Munshi-South and Wilkinson
<xref ref-type="bibr" rid="CR170">2010</xref>
), which may facilitate pathogen persistence for chronic infections; (2) flight, which allows movement and dispersal over long distances and which creates high body temperatures that may select for co-evolution with viruses that can live at febrile temperatures and are therefore highly virulent in humans (O’Shea et al.
<xref ref-type="bibr" rid="CR178">2014</xref>
); (3) physiological similarity across sympatric species that roost together in high densities enabling pathogens adapted to any of the sympatric species to spillover to others (Streicker et al.
<xref ref-type="bibr" rid="CR226">2010</xref>
); and (4) regulation of their immune systems in such a way as to make them more likely to host, but remain unaffected by viral pathogens, serving as the reservoir host for emerging and highly virulent viruses (Baker et al.
<xref ref-type="bibr" rid="CR22">2013</xref>
).</p>
<p id="Par24">Despite the fact that pathogens are common and often occur in high numbers in basically all animals, only a relatively small proportion of these pathogens will spillover to humans (Cleaveland et al.
<xref ref-type="bibr" rid="CR47">2007</xref>
). That said, when spillover events do occur, they can be not only deadly but costly. For example, the United Nations Development Program (
<xref ref-type="bibr" rid="CR245">2015</xref>
) has estimated that West Africa as a whole may lose US$3.6 billion per year between 2014 and 2017 due to the 2014–2015 Ebola outbreak. This loss stems from the cumulative effects of closed borders, decreased trade, decreased foreign direct investment, and decreased tourism, resulting in increased poverty levels and food insecurity.</p>
<p id="Par25">To understand the dynamics of spillover events and risks in relation to the pathogen, a number of factors must be considered, including: (1) the evolutionary history of the pathogen, (2) how the pathogen is maintained among its wildlife host(s), (3) how the pathogen is transmitted across a species barrier, (4) whether a productive infection is produced in the new host, (5) whether that infection produces significant disease in that host, and (6) whether morbidity and/or mortality levels in the secondary host are sufficient to be considered significant (Childs et al.
<xref ref-type="bibr" rid="CR45">2007</xref>
). From this, it follows that emerging pathogens are not an arbitrary selection of all pathogens. Becoming established in a human host typically requires adaptations, often for increased virulence, as has been documented in HIV (Wain et al.
<xref ref-type="bibr" rid="CR257">2007</xref>
; Etienne et al.
<xref ref-type="bibr" rid="CR62">2013</xref>
). Generalist pathogens have the ability to infect more than one host species and have higher relative emergence risk than pathogens that are very host-specific (Cleaveland et al.
<xref ref-type="bibr" rid="CR47">2007</xref>
); this is especially true for pathogens that can infect species in more than one taxonomic order. One example of this generalist “broad” host range is found in the newly described African henipavirus, which can enter and infect cells of nonhuman primates, bats, and humans (Lawrence et al.
<xref ref-type="bibr" rid="CR122">2014</xref>
).</p>
<p id="Par26">Of particular importance for understanding bushmeat-related spillover events is whether a wildlife species is a natural or incidental pathogen host. Natural or reservoir hosts are a natural part of the pathogen life cycle and may maintain the infectious pathogen for prolonged periods of time, often without showing symptoms. In contrast, an incidental or dead-end host may be infected by the pathogen and may even transmit it, but it is not a part of the normal maintenance cycle of the pathogen and is more likely to be affected by it than natural hosts. For example, contact with sick common chimpanzees and western gorillas has been tightly linked to Ebola virus spillover in several outbreaks (Leroy et al.
<xref ref-type="bibr" rid="CR133">2004b</xref>
). Like their human cousins, these great apes are largely considered incidental or dead-end hosts for this virus and do not maintain it long-term in nature. In the case of this deadly filovirus, understanding what species are true reservoirs (likely fruit bats in the family Pteropodidae; Pourrut et al.
<xref ref-type="bibr" rid="CR194">2007</xref>
,
<xref ref-type="bibr" rid="CR195">2009</xref>
; Hayman et al.
<xref ref-type="bibr" rid="CR90">2010</xref>
,
<xref ref-type="bibr" rid="CR91">2012</xref>
) and the spillover events between these reservoirs and other mammals (including apes, carnivores, and ungulates; Leroy et al.
<xref ref-type="bibr" rid="CR132">2004a</xref>
) will prove critical to mitigating the components of disease transmission that are due to bushmeat-related activities. Unfortunately, it is often difficult to definitively determine the natural host(s) of a particular pathogen as it requires, in descending order of importance, isolation of the agent from individuals of the target species, detection of pathogen-specific nucleic acid sequences from individuals, and serological evidence that an individual has been exposed previously. Indeed, the study of reservoir systems and how infectious agents move between and within them can be complex, requiring rigorous and sophisticated analyses of multiple interrelated variables (Gray and Salemi
<xref ref-type="bibr" rid="CR84">2012</xref>
; Viana et al.
<xref ref-type="bibr" rid="CR255">2014</xref>
).</p>
<p id="Par27">Descriptions of the types of pathogens potentially encountered through bushmeat-related activities can be found below, with several important and well-studied examples described in more detail. In their review of global trends in EIDs, in which they separately listed each antimicrobial pathogen strain that has recently emerged, Jones et al. (
<xref ref-type="bibr" rid="CR103">2008</xref>
) report that the vast majority of pathogens involved in EIDs are bacterial or rickettsial, followed by viral or prion, then protozoa, fungi, and helminths. Other studies have ranked viruses as more prevalent (Taylor et al.
<xref ref-type="bibr" rid="CR235">2001</xref>
; Woolhouse et al.
<xref ref-type="bibr" rid="CR272">2005</xref>
; Cleaveland et al.
<xref ref-type="bibr" rid="CR47">2007</xref>
). In Jones et al.’s (
<xref ref-type="bibr" rid="CR103">2008</xref>
) analysis of 335 EID events between 1940 and 2004, only four EIDs list bushmeat as the driver; other significant drivers were socioeconomic factors such as human population density. These four bushmeat-related EID events were all significant events; all due to viruses (Ebolavirus, human immunodeficiency virus-1, monkeypox virus, and SARS), suggesting that viruses are the most important pathogens in regard to spillover due to bushmeat-related activities (see also Kilonzo et al.
<xref ref-type="bibr" rid="CR115">2014</xref>
). We review the literature from sub-Saharan Africa in relation to bushmeat species by pathogen type (viruses, bacteria, helminths, protozoa, fungi, and prions), noting the significant potential for pathogens not yet associated with bushmeat-related activities to also be involved. Very few studies have considered all of the potential zoonotics in a region or in a taxonomic group. Magwedere et al.’s (
<xref ref-type="bibr" rid="CR141">2011</xref>
) comprehensive study of zoonotics in Namibia is an exception.</p>
<sec id="Sec7">
<title>Overview of Pathogens Related to Bushmeat Activities</title>
<p id="Par28">Table
<xref rid="Tab1" ref-type="table">24.1</xref>
summarizes these pathogens by bushmeat host taxonomic group, conservatively listing only those species/pathogen combinations that have been tied strongly to spillovers from wildlife to humans via bushmeat-related activities and recognizing that this link is often putative and difficult to establish. Thus, Table
<xref rid="Tab1" ref-type="table">24.1</xref>
does not include some of the potential but not demonstrated spillover risks of poorly studied groups such as helminths and protozoans. Furthermore, due to their close genetic relationship with humans, common chimpanzees and western gorillas may share many pathogens of all varieties with humans, but the direction of spillover is not always clear (e.g. tourist interactions may spread disease from humans to apes) and much of these data are not discussed herein. Also not included in the table are studies where pathogens are not determined to species and, consequently, the bushmeat host–human link is unclear, or where exposure would be via an insect vector, which could be encountered when handling bushmeat. While we have attempted a very thorough treatment of pathogens that meet our criteria for inclusion in the table, it is possible that some relevant studies have been missed.
<table-wrap id="Tab1">
<label>Table 24.1</label>
<caption>
<p>Bushmeat speciesand zoonotic pathogens for which strong evidence for spillovers via bushmeat-related activities exists (see criteria for inclusion in text)</p>
</caption>
<table frame="hsides" rules="groups">
<thead>
<tr>
<th>Bushmeat species</th>
<th>Pathogen</th>
<th>Location</th>
<th>References</th>
</tr>
</thead>
<tbody>
<tr>
<td colspan="4">Great Apes (Chimpanzee, Bonobo, Gorilla)
<sup>a</sup>
</td>
</tr>
<tr>
<td rowspan="10">
<italic>troglodytes</italic>
(Common chimpanzee)</td>
<td>Zaire Ebolavirus (V)</td>
<td>Cameroon, Gabon, Republic of Congo</td>
<td>Leroy et al. (
<xref ref-type="bibr" rid="CR132">2004a</xref>
,
<xref ref-type="bibr" rid="CR133">b</xref>
)</td>
</tr>
<tr>
<td>Tai Forest Ebolavirus (V)</td>
<td>Côte d’Ivoire</td>
<td>Le Guenno et al. (
<xref ref-type="bibr" rid="CR123">1995</xref>
), Wyers et al. (
<xref ref-type="bibr" rid="CR275">1999</xref>
)</td>
</tr>
<tr>
<td>HIV-1/SIVcpz (V)</td>
<td>Cameroon, Democratic Republic of the Congo, Tanzania</td>
<td>Santiago et al. (
<xref ref-type="bibr" rid="CR278">2002</xref>
), Worobey et al. (
<xref ref-type="bibr" rid="CR279">2004</xref>
), Van Heuverswyn et al. (
<xref ref-type="bibr" rid="CR251">2007</xref>
)</td>
</tr>
<tr>
<td>HLTV/SLTV-1 (V) </td>
<td>Central & Eastern Africa</td>
<td>Gao et al. (
<xref ref-type="bibr" rid="CR72">1999</xref>
), reviewed in Sharp and Hahn (
<xref ref-type="bibr" rid="CR213">2010</xref>
), Peeters et al. (
<xref ref-type="bibr" rid="CR187">2013</xref>
)</td>
</tr>
<tr>
<td>Simian Foamy Virus (V) </td>
<td>Cameroon, Côte d’Ivoire, Gabon, Republic of Congo, Tanzania</td>
<td>Calattini et al. (
<xref ref-type="bibr" rid="CR37">2006</xref>
), Liu et al. (
<xref ref-type="bibr" rid="CR138">2008</xref>
)</td>
</tr>
<tr>
<td>
<italic>Strongyloides fulleborni</italic>
(H)</td>
<td>Gabon</td>
<td>Mouinga-Ondémé et al. (
<xref ref-type="bibr" rid="CR164">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Entamoeba histolytica</italic>
(P)</td>
<td>Tanzania</td>
<td>Gillespie et al. (
<xref ref-type="bibr" rid="CR77">2010</xref>
)</td>
</tr>
<tr>
<td>
<italic>Balantidium coli</italic>
(P) </td>
<td>Central African Republic, Tanzania</td>
<td>Lilly et al. (
<xref ref-type="bibr" rid="CR137">2002</xref>
), Gillespie et al. (
<xref ref-type="bibr" rid="CR77">2010</xref>
)</td>
</tr>
<tr>
<td>
<italic>Giardia intestinalis</italic>
(P)</td>
<td>Guinea Bissau</td>
<td>Sak et al. (
<xref ref-type="bibr" rid="CR205">2013</xref>
)</td>
</tr>
<tr>
<td>
<italic>Bacillus anthracis</italic>
(B) </td>
<td>Côte d’Ivoire</td>
<td>Leendertz et al. (
<xref ref-type="bibr" rid="CR128">2004</xref>
)</td>
</tr>
<tr>
<td>
<italic>Pan paniscus</italic>
(Bonobo)</td>
<td>HTLV/STLV-2, HTLV/STLV-3 (V)</td>
<td>Democratic Republic of the Congo</td>
<td>Ahuka-Mundeke et al. (
<xref ref-type="bibr" rid="CR5">2011</xref>
), Van Brussel et al. (
<xref ref-type="bibr" rid="CR247">1998</xref>
)</td>
</tr>
<tr>
<td rowspan="9">
<italic>Gorilla gorilla</italic>
(Western gorilla) </td>
<td>Zaire Ebolavirus (V)</td>
<td>Cameroon, Gabon</td>
<td>Leroy et al. (
<xref ref-type="bibr" rid="CR132">2004a</xref>
,
<xref ref-type="bibr" rid="CR133">b</xref>
)</td>
</tr>
<tr>
<td>HIV-1/SIVgor (V)</td>
<td>Cameroon</td>
<td>Takehisa et al. (
<xref ref-type="bibr" rid="CR232">2009</xref>
)</td>
</tr>
<tr>
<td>HTLV/STLV-1 (V)</td>
<td>Cameroon</td>
<td>Courgnaud et al. (
<xref ref-type="bibr" rid="CR49">2004</xref>
), Nerrienet et al. (
<xref ref-type="bibr" rid="CR174">2004</xref>
)</td>
</tr>
<tr>
<td>Simian Foamy Virus (V)</td>
<td>Cameroon, Gabon</td>
<td>Wolfe et al. (
<xref ref-type="bibr" rid="CR268">2004b</xref>
), Mouinga-Ondémé et al. (
<xref ref-type="bibr" rid="CR164">2012</xref>
)</td>
</tr>
<tr>
<td>Rabies (V)</td>
<td>Central African Republic, Kenya</td>
<td>Karugah (
<xref ref-type="bibr" rid="CR109">1997</xref>
)</td>
</tr>
<tr>
<td>
<italic>Strongyloides fulleborni</italic>
(H)</td>
<td>Central African Republic</td>
<td>Lilly et al. (
<xref ref-type="bibr" rid="CR137">2002</xref>
)</td>
</tr>
<tr>
<td>
<italic>Entamoeba histolytica</italic>
(P) </td>
<td>Central African Republic</td>
<td>Lilly et al. (
<xref ref-type="bibr" rid="CR137">2002</xref>
)</td>
</tr>
<tr>
<td>
<italic>Balantidium coli</italic>
(P)</td>
<td>Central African Republic</td>
<td>Lilly et al. (
<xref ref-type="bibr" rid="CR137">2002</xref>
)</td>
</tr>
<tr>
<td>
<italic>Giardia intestinalis</italic>
(P) </td>
<td>Central African Republic, Rwanda</td>
<td>Sak et al. (
<xref ref-type="bibr" rid="CR205">2013</xref>
), Hogan et al. (
<xref ref-type="bibr" rid="CR94">2014</xref>
)</td>
</tr>
<tr>
<td colspan="4">Other nonhuman primates</td>
</tr>
<tr>
<td rowspan="3">
<italic>Colobus angolensis</italic>
(Angola colobus) </td>
<td>HTLV/STLV-3 (V)</td>
<td>Democratic Republic of the Congo</td>
<td>Ahuka-Mundeke et al. (
<xref ref-type="bibr" rid="CR6">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Strongyloides fulleborni</italic>
(H)</td>
<td>Uganda</td>
<td>Gillespie et al. (
<xref ref-type="bibr" rid="CR76">2005</xref>
)</td>
</tr>
<tr>
<td>
<italic>Entamoeba histolytica</italic>
(P)</td>
<td>Uganda</td>
<td>Gillespie et al. (
<xref ref-type="bibr" rid="CR76">2005</xref>
)</td>
</tr>
<tr>
<td rowspan="2">
<italic>Colobus guereza</italic>
(Mantled guereza) </td>
<td>
<italic>Strongyloides fulleborni</italic>
(H)</td>
<td>Cameroon, Uganda</td>
<td>Gillespie et al. (
<xref ref-type="bibr" rid="CR76">2005</xref>
), Pourrut et al. (
<xref ref-type="bibr" rid="CR196">2011</xref>
)</td>
</tr>
<tr>
<td>
<italic>Entamoeba histolytica</italic>
(P)</td>
<td>Uganda</td>
<td>Gillespie et al. (
<xref ref-type="bibr" rid="CR76">2005</xref>
)</td>
</tr>
<tr>
<td>
<italic>Piliocolobus badius</italic>
(Western red colobus)</td>
<td>HTLV/STLV-1 (V)</td>
<td>Côte d’Ivoire</td>
<td>Leendertz et al. (
<xref ref-type="bibr" rid="CR129">2010</xref>
)</td>
</tr>
<tr>
<td rowspan="3">
<italic>Piliocolobus tephrosceles</italic>
(Ugandan red colobus) </td>
<td>HTLV/STLV-1 (V)</td>
<td>Uganda</td>
<td>Goldberg et al. (
<xref ref-type="bibr" rid="CR79">2009</xref>
)</td>
</tr>
<tr>
<td>
<italic>Strongyloides fulleborni</italic>
(H)</td>
<td>Uganda</td>
<td>Gillespie et al. (
<xref ref-type="bibr" rid="CR76">2005</xref>
)</td>
</tr>
<tr>
<td>
<italic>Entamoeba histolytica</italic>
(P)</td>
<td>Uganda</td>
<td>Gillespie et al. (
<xref ref-type="bibr" rid="CR76">2005</xref>
)</td>
</tr>
<tr>
<td>
<italic>Piliocolobus tholloni</italic>
(Thollon’s red colobus)</td>
<td>HTLV/STLV-1, HTLV/STLV-3 (V)</td>
<td>Democratic Republic of the Congo</td>
<td>Ahuka-Mundeke et al. (
<xref ref-type="bibr" rid="CR6">2012</xref>
).</td>
</tr>
<tr>
<td rowspan="2">
<italic>Lophocebus albigena</italic>
(Gray-cheeked mangabey) </td>
<td>HTLV/STLV-1, HTLV/STLV-3 (V)</td>
<td>Cameroon</td>
<td>Liégeois et al. (
<xref ref-type="bibr" rid="CR136">2012</xref>
), Locatelli and Peeters (
<xref ref-type="bibr" rid="CR139">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Strongyloides fulleborni</italic>
(H)</td>
<td>Cameroon</td>
<td>Pourrut et al. (
<xref ref-type="bibr" rid="CR196">2011</xref>
)</td>
</tr>
<tr>
<td>
<italic>Lophocebus aterrimus</italic>
(Black crested mangabey)</td>
<td>HTLV/STLV-3 (V)</td>
<td>Democratic Republic of the Congo</td>
<td>Ahuka-Mundeke et al. (
<xref ref-type="bibr" rid="CR6">2012</xref>
)</td>
</tr>
<tr>
<td rowspan="2">
<italic>Papio anubis</italic>
(Olive baboon) </td>
<td>Zaire Ebolavirus (V)</td>
<td>Cameroon</td>
<td>Leroy et al. (
<xref ref-type="bibr" rid="CR133">2004b</xref>
)</td>
</tr>
<tr>
<td>HTLV/STLV-1 (V)</td>
<td>Ethiopia, Kenya</td>
<td>Mahieux et al. (
<xref ref-type="bibr" rid="CR143">1998</xref>
), Meertens et al. (
<xref ref-type="bibr" rid="CR154">2001</xref>
), Takemura et al. (
<xref ref-type="bibr" rid="CR233">2002</xref>
), Locatelli and Peeters (
<xref ref-type="bibr" rid="CR139">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Papio cynocephalus</italic>
(Yellow baboon) </td>
<td>HTLV/STLV-3 (V)</td>
<td>Tanzania</td>
<td>Voevodin et al. (
<xref ref-type="bibr" rid="CR256">1997</xref>
)</td>
</tr>
<tr>
<td>
<italic>Papio hamadryas</italic>
(Hamadryas baboon)</td>
<td>HTLV/STLV-3 (V)</td>
<td>Eritrea, Ethiopia, Senegal</td>
<td>Goubau et al. (
<xref ref-type="bibr" rid="CR83">1994</xref>
), Takemura et al. (
<xref ref-type="bibr" rid="CR233">2002</xref>
), Meertens and Gessain (
<xref ref-type="bibr" rid="CR153">2003</xref>
)</td>
</tr>
<tr>
<td rowspan="2">
<italic>Papio ursinus</italic>
(Chacma baboon) </td>
<td>HTLV/STLV-1 (V)</td>
<td>South Africa</td>
<td>Mahieux et al. (
<xref ref-type="bibr" rid="CR143">1998</xref>
)</td>
</tr>
<tr>
<td>
<italic>Bacillus anthracis</italic>
(B)</td>
<td>Namibia</td>
<td>Magwedere et al. (
<xref ref-type="bibr" rid="CR142">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Papio</italic>
sp. (Baboon sp.)</td>
<td>Rabies (V)</td>
<td>Kenya, Namibia, Zambia</td>
<td>Munang’andu (
<xref ref-type="bibr" rid="CR168">1995</xref>
), Karugah (
<xref ref-type="bibr" rid="CR109">1997</xref>
), Magwedere et al. (
<xref ref-type="bibr" rid="CR142">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Theropithecus gelada</italic>
(Gelada) </td>
<td>HTLV/STLV-3 (V)</td>
<td>Ethiopia</td>
<td>Van Dooren et al. (
<xref ref-type="bibr" rid="CR248">2004</xref>
)</td>
</tr>
<tr>
<td rowspan="4">
<italic>Cercocebus agilis</italic>
(Agile mangabey)</td>
<td>HTLV/STLV-1, HTLV/STLV-3 (V)</td>
<td>Cameroon</td>
<td>Nerrienet et al. (
<xref ref-type="bibr" rid="CR173">2001</xref>
), Courgnaud et al. (
<xref ref-type="bibr" rid="CR49">2004</xref>
), Liégeois et al. (
<xref ref-type="bibr" rid="CR134">2008</xref>
), Sintasath et al. (
<xref ref-type="bibr" rid="CR219">2009a</xref>
), Locatelli and Peeters (
<xref ref-type="bibr" rid="CR139">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Strongyloides fulleborni</italic>
(H)</td>
<td>Cameroon</td>
<td>Pourrut et al. (
<xref ref-type="bibr" rid="CR196">2011</xref>
)</td>
</tr>
<tr>
<td>
<italic>Entamoeba histolytica</italic>
(P)</td>
<td>Central African Republic</td>
<td>Lilly et al. (
<xref ref-type="bibr" rid="CR137">2002</xref>
)</td>
</tr>
<tr>
<td>
<italic>Balantidium coli</italic>
(P) </td>
<td>Central African Republic</td>
<td>Lilly et al. (
<xref ref-type="bibr" rid="CR137">2002</xref>
)</td>
</tr>
<tr>
<td rowspan="2">
<italic>Cercocebus atys</italic>
(Sooty mangabey)</td>
<td>HIV-2/SIVsm (V)</td>
<td>West Africa</td>
<td>Hirsch et al. (
<xref ref-type="bibr" rid="CR93">1989</xref>
), reviewed in Sharp and Hahn (
<xref ref-type="bibr" rid="CR213">2010</xref>
), Peeters et al. (
<xref ref-type="bibr" rid="CR187">2013</xref>
)</td>
</tr>
<tr>
<td>HTLV/STLV-1 (V) </td>
<td>Sierra Leone</td>
<td>Traina-Dorge et al. (
<xref ref-type="bibr" rid="CR242">2005</xref>
)</td>
</tr>
<tr>
<td>
<italic>Cercocebus torquatus</italic>
(Collared mangabey)</td>
<td>HTLV/STLV-1, HTLV/STLV-3 (V)</td>
<td>Cameroon</td>
<td>Meertens et al. (
<xref ref-type="bibr" rid="CR154">2001</xref>
,
<xref ref-type="bibr" rid="CR155">2002</xref>
), Liégeois et al. (
<xref ref-type="bibr" rid="CR134">2008</xref>
,
<xref ref-type="bibr" rid="CR136">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Mandrillus leucophaeus</italic>
(Drill)</td>
<td>Zaire Ebolavirus (V)</td>
<td>Cameroon</td>
<td>Leroy et al. (
<xref ref-type="bibr" rid="CR133">2004b</xref>
)</td>
</tr>
<tr>
<td rowspan="3">
<italic>Mandrillus sphinx</italic>
(Mandrill)</td>
<td>Zaire Ebolavirus (V) </td>
<td>Cameroon</td>
<td>Leroy et al. (
<xref ref-type="bibr" rid="CR133">2004b</xref>
)</td>
</tr>
<tr>
<td>HTLV/STLV-1 (V)</td>
<td>Cameroon</td>
<td>Nerrienet et al. (
<xref ref-type="bibr" rid="CR173">2001</xref>
), Courgnaud et al. (
<xref ref-type="bibr" rid="CR49">2004</xref>
), Liégeois et al. (
<xref ref-type="bibr" rid="CR136">2012</xref>
)</td>
</tr>
<tr>
<td>Simian foamy virus (V) </td>
<td>Cameroon, Gabon</td>
<td>Wolfe et al. (
<xref ref-type="bibr" rid="CR268">2004b</xref>
), Mouinga-Ondémé et al. (
<xref ref-type="bibr" rid="CR163">2010</xref>
)</td>
</tr>
<tr>
<td>
<italic>Allenopithecus nigroviridis</italic>
(Allen’s swamp monkey)</td>
<td>HTLV/STLV-1 (V)</td>
<td>Democratic Republic of the Congo</td>
<td>Meertens et al. (
<xref ref-type="bibr" rid="CR154">2001</xref>
)</td>
</tr>
<tr>
<td rowspan="2">
<italic>Miopithecus ogouensis</italic>
(Gabon talapoin)</td>
<td>HTLV/STLV-1 (V) </td>
<td>Cameroon</td>
<td>Courgnaud et al. (
<xref ref-type="bibr" rid="CR49">2004</xref>
)</td>
</tr>
<tr>
<td>
<italic>Strongyloides fulleborni</italic>
(H)</td>
<td>Cameroon</td>
<td>Pourrut et al. (
<xref ref-type="bibr" rid="CR196">2011</xref>
)</td>
</tr>
<tr>
<td>
<italic>Erythrocebus patas (Patas monkey)</italic>
</td>
<td>HTLV/STLV-1 (V)</td>
<td>Cameroon, Central African Republic, Senegal</td>
<td>Ishikawa et al. (
<xref ref-type="bibr" rid="CR101">1987</xref>
), Saksena et al. (
<xref ref-type="bibr" rid="CR206">1994</xref>
)</td>
</tr>
<tr>
<td rowspan="2">
<italic>Chlorocebus aethiops (Grivet)</italic>
</td>
<td>Marburg virus (V) </td>
<td>Uganda</td>
<td>Smith (
<xref ref-type="bibr" rid="CR221">1982</xref>
)</td>
</tr>
<tr>
<td>HTLV/STLV-1 (V)</td>
<td>Ethiopia, Senegal</td>
<td>Meertens et al. (
<xref ref-type="bibr" rid="CR154">2001</xref>
), Takemura et al. (
<xref ref-type="bibr" rid="CR233">2002</xref>
)</td>
</tr>
<tr>
<td rowspan="2">
<italic>Chlorocebus pygerythrus</italic>
(Vervet monkey)</td>
<td>HTLV/STLV-1 (V)</td>
<td>Kenya</td>
<td>Meertens et al. (
<xref ref-type="bibr" rid="CR154">2001</xref>
)</td>
</tr>
<tr>
<td>
<italic>Leptospira</italic>
(B)</td>
<td>Botswana</td>
<td>Jobbins and Alexander (
<xref ref-type="bibr" rid="CR102">2015</xref>
)</td>
</tr>
<tr>
<td>
<italic>Chlorocebus sabaeus</italic>
(Green monkey)</td>
<td>HTLV/STLV-1 (V) </td>
<td>Senegal</td>
<td>Meertens et al. (
<xref ref-type="bibr" rid="CR154">2001</xref>
), Locatelli and Peeters (
<xref ref-type="bibr" rid="CR139">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Chlorocebus tantalus</italic>
(Tantalus monkey)</td>
<td>HTLV/STLV-1 (V)</td>
<td>Kenya</td>
<td>Meertens et al. (
<xref ref-type="bibr" rid="CR154">2001</xref>
), Locatelli and Peeters (
<xref ref-type="bibr" rid="CR139">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Cercopithecus albogularis</italic>
(Sykes’ monkey)</td>
<td>HTLV/STLV-1 (V)</td>
<td>Kenya</td>
<td>Mwenda et al. (
<xref ref-type="bibr" rid="CR171">1999</xref>
)</td>
</tr>
<tr>
<td rowspan="2">
<italic>Cercopithecus ascanius</italic>
(Red-tailed monkey)</td>
<td>HTLV/STLV-1 (V) </td>
<td>Democratic Republic of the Congo</td>
<td>Ahuka-Mundeke et al. (
<xref ref-type="bibr" rid="CR6">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Strongyloides fulleborni</italic>
(H)</td>
<td>Uganda</td>
<td>Gillespie et al.(
<xref ref-type="bibr" rid="CR75">2004</xref>
)</td>
</tr>
<tr>
<td rowspan="2">
<italic>Cercopithecus cephus</italic>
(Moustached guenon)</td>
<td>HTLV/STLV-1, HTLV/STLV-3 (V)</td>
<td>Cameroon</td>
<td>Courgnaud et al. (
<xref ref-type="bibr" rid="CR49">2004</xref>
), Liégeois et al. (
<xref ref-type="bibr" rid="CR134">2008</xref>
,
<xref ref-type="bibr" rid="CR136">2012</xref>
), Locatelli and Peeters (
<xref ref-type="bibr" rid="CR139">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Strongyloidesfulleborni</italic>
(H) </td>
<td>Cameroon</td>
<td>Pourrut et al. (
<xref ref-type="bibr" rid="CR196">2011</xref>
)</td>
</tr>
<tr>
<td>
<italic>Cercopithecus lhoesti</italic>
(L’Hoest’s monkey)</td>
<td>
<italic>Strongyloides fulleborni</italic>
(H)</td>
<td>Uganda</td>
<td>Gillespie et al. (
<xref ref-type="bibr" rid="CR75">2004</xref>
)</td>
</tr>
<tr>
<td>
<italic>Cercopithecus mitis</italic>
(Blue monkey)</td>
<td>
<italic>Strongyloides fulleborni</italic>
(H)</td>
<td>Kenya, Uganda</td>
<td>Munene et al. (
<xref ref-type="bibr" rid="CR169">1998</xref>
), Gillespie et al. (
<xref ref-type="bibr" rid="CR75">2004</xref>
)</td>
</tr>
<tr>
<td rowspan="2">
<italic>Cercopithecus mona</italic>
(Mona monkey)</td>
<td>HTLV/STLV-1, HTLV/STLV-3 (V) </td>
<td>Cameroon</td>
<td>Meertens et al. (
<xref ref-type="bibr" rid="CR154">2001</xref>
), Sintasath et al. (
<xref ref-type="bibr" rid="CR220">2009b</xref>
), Locatelli and Peeters (
<xref ref-type="bibr" rid="CR139">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Strongyloides fulleborni</italic>
(H)</td>
<td>Cameroon</td>
<td>Pourrut et al. (
<xref ref-type="bibr" rid="CR196">2011</xref>
)</td>
</tr>
<tr>
<td rowspan="4">
<italic>Cercopithecus neglectus</italic>
(De Brazza’s monkey)</td>
<td>Zaire Ebolavirus (V)</td>
<td>Cameroon</td>
<td>Leroy et al. (
<xref ref-type="bibr" rid="CR133">2004b</xref>
)</td>
</tr>
<tr>
<td>HTLV/STLV-1 (V)</td>
<td>Democratic Republic of the Congo</td>
<td>Ahuka-Mundeke et al. (
<xref ref-type="bibr" rid="CR6">2012</xref>
)</td>
</tr>
<tr>
<td>Simian Foamy Virus (V) </td>
<td>Cameroon</td>
<td>Wolfe et al. (
<xref ref-type="bibr" rid="CR268">2004b</xref>
)</td>
</tr>
<tr>
<td>
<italic>Strongyloides fulleborni</italic>
(H)</td>
<td>Cameroon</td>
<td>Pourrut et al. (
<xref ref-type="bibr" rid="CR196">2011</xref>
)</td>
</tr>
<tr>
<td rowspan="2">
<italic>Cercopithecus nictitans</italic>
(Greater spot-nosed monkey)</td>
<td>HTLV/STLV-1, HTLV/STLV-3 (V)</td>
<td>Cameroon</td>
<td>Meertens et al. (
<xref ref-type="bibr" rid="CR154">2001</xref>
), Courgnaud et al. (
<xref ref-type="bibr" rid="CR49">2004</xref>
), Liégeois et al. (
<xref ref-type="bibr" rid="CR134">2008</xref>
,
<xref ref-type="bibr" rid="CR136">2012</xref>
), Sintasath et al. (
<xref ref-type="bibr" rid="CR220">2009b</xref>
)</td>
</tr>
<tr>
<td>
<italic>Strongyloides fulleborni</italic>
(H) </td>
<td>Cameroon</td>
<td>Pourrut et al. (
<xref ref-type="bibr" rid="CR196">2011</xref>
)</td>
</tr>
<tr>
<td rowspan="2">
<italic>Cercopithecus pogonias</italic>
(Crested mona monkey)</td>
<td>HTLV/STLV-1 (V)</td>
<td>Cameroon</td>
<td>Courgnaud et al. (
<xref ref-type="bibr" rid="CR49">2004</xref>
), Liégeois et al. (
<xref ref-type="bibr" rid="CR134">2008</xref>
)</td>
</tr>
<tr>
<td>
<italic>Strongyloides fulleborni</italic>
(H)</td>
<td>Cameroon</td>
<td>Pourrut et al. (
<xref ref-type="bibr" rid="CR196">2011</xref>
)</td>
</tr>
<tr>
<td>
<italic>Cercopithecus wolfi</italic>
(Wolf’s mona monkey)</td>
<td>HTLV/STLV-1 (V)</td>
<td>Democratic Republic of the Congo</td>
<td>Locatelli and Peeters (
<xref ref-type="bibr" rid="CR139">2012</xref>
)</td>
</tr>
<tr>
<td rowspan="2">“Vervet monkey”</td>
<td>Rabies (V) </td>
<td>Zambia</td>
<td>Munang’andu (
<xref ref-type="bibr" rid="CR168">1995</xref>
)</td>
</tr>
<tr>
<td>
<italic>Strongyloides fulleborni</italic>
(H)</td>
<td>Uganda</td>
<td>Gillespie et al. (
<xref ref-type="bibr" rid="CR75">2004</xref>
)</td>
</tr>
<tr>
<td>Unspecified primate sp.</td>
<td>Rabies (V)</td>
<td>Ethiopia, Ghana, Kenya, Malawi, Mozambique; Namibia, Sudan, Uganda, Zimbabwe</td>
<td>See summary and discussion in Gautret et al. (
<xref ref-type="bibr" rid="CR73">2014</xref>
)</td>
</tr>
<tr>
<td colspan="4">Bats</td>
</tr>
<tr>
<td rowspan="3">
<italic>Eidolon helvum</italic>
(African straw-colored fruit bat)</td>
<td>Zaire Ebolavirus (V) </td>
<td>Ghana</td>
<td>Hayman et al. (
<xref ref-type="bibr" rid="CR90">2010</xref>
)</td>
</tr>
<tr>
<td>Lagos bat virus (V)</td>
<td>Ghana, Kenya, Nigeria, Senegal</td>
<td>Boulger and Porterfield (
<xref ref-type="bibr" rid="CR31">1958</xref>
), Institut Pasteur (
<xref ref-type="bibr" rid="CR100">1985</xref>
), Hayman et al. (
<xref ref-type="bibr" rid="CR89">2008</xref>
,
<xref ref-type="bibr" rid="CR90">2010</xref>
), Kuzmin et al. (
<xref ref-type="bibr" rid="CR118">2008</xref>
)</td>
</tr>
<tr>
<td>Henipaviruses (V) </td>
<td>Cameroon, Ghana, Republic of Congo, Zambia</td>
<td>Hayman et al. (
<xref ref-type="bibr" rid="CR89">2008</xref>
), Drexler et al. (
<xref ref-type="bibr" rid="CR60">2009</xref>
), Baker et al. (
<xref ref-type="bibr" rid="CR21">2012</xref>
), Weiss et al. (
<xref ref-type="bibr" rid="CR260">2012</xref>
), Muleya et al. (
<xref ref-type="bibr" rid="CR167">2014</xref>
), Pernet et al. (
<xref ref-type="bibr" rid="CR188">2014</xref>
)</td>
</tr>
<tr>
<td rowspan="2">
<italic>Hypsignathus monstrosus</italic>
(Hammer-headed fruit bat)</td>
<td>Marburgvirus (V)</td>
<td>Gabon, Republic of Congo</td>
<td>Pourrut et al. (
<xref ref-type="bibr" rid="CR195">2009</xref>
)</td>
</tr>
<tr>
<td>Zaire Ebolavirus (V) </td>
<td>Ghana, Gabon, Republic of Congo</td>
<td>Pourrut et al. (
<xref ref-type="bibr" rid="CR194">2007</xref>
,
<xref ref-type="bibr" rid="CR195">2009</xref>
), Hayman et al. (
<xref ref-type="bibr" rid="CR91">2012</xref>
)</td>
</tr>
<tr>
<td rowspan="2">
<italic>Epomops franqueti</italic>
(Franquet’s epauletted fruit bat)</td>
<td>Marburgvirus (V)</td>
<td>Gabon, Republic of Congo</td>
<td>Pourrut et al. (
<xref ref-type="bibr" rid="CR195">2009</xref>
)</td>
</tr>
<tr>
<td>Zaire Ebolavirus (V)</td>
<td>Ghana, Gabon, Republic of Congo</td>
<td>Pourrut et al. (
<xref ref-type="bibr" rid="CR194">2007</xref>
,
<xref ref-type="bibr" rid="CR195">2009</xref>
), Hayman et al. (
<xref ref-type="bibr" rid="CR91">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Epomophorus gambianus</italic>
(Gambian epauletted fruit bat)</td>
<td>Zaire Ebolavirus (V) </td>
<td>Ghana</td>
<td>Hayman et al. (
<xref ref-type="bibr" rid="CR91">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Epomophorus wahlbergi</italic>
(Wahlberg’s epauletted fruit bat)</td>
<td>Lagos Bat Virus (V)</td>
<td>South Africa</td>
<td>Markotter et al. (
<xref ref-type="bibr" rid="CR145">2006</xref>
)</td>
</tr>
<tr>
<td rowspan="3">
<italic>Micropteropus pusillus</italic>
(Peters’s lesser epauletted fruit bat)</td>
<td>Marburgvirus (V)</td>
<td>Gabon, Republic of Congo</td>
<td>Pourrut et al. (
<xref ref-type="bibr" rid="CR195">2009</xref>
)</td>
</tr>
<tr>
<td>Zaire Ebolavirus (V)</td>
<td>Gabon, Republic of Congo</td>
<td>Pourrut et al. (
<xref ref-type="bibr" rid="CR195">2009</xref>
)</td>
</tr>
<tr>
<td>Lagos Bat Virus (V) </td>
<td>Central African Republic</td>
<td>Sureau et al. (
<xref ref-type="bibr" rid="CR228">1980</xref>
)</td>
</tr>
<tr>
<td rowspan="3">
<italic>Rousettus aegyptiacus</italic>
(Egyptian rousette)</td>
<td>Marburgvirus (V)</td>
<td>Democratic Republic of the Congo, Gabon, Kenya, Republic of Congo, Uganda</td>
<td>Swanepoel et al. (
<xref ref-type="bibr" rid="CR229">2007</xref>
), Towner et al. (
<xref ref-type="bibr" rid="CR240">2007</xref>
,
<xref ref-type="bibr" rid="CR241">2009</xref>
), Pourrut et al. (
<xref ref-type="bibr" rid="CR195">2009</xref>
), Kuzmin et al. (
<xref ref-type="bibr" rid="CR120">2010b</xref>
), Amman et al. (
<xref ref-type="bibr" rid="CR14">2012</xref>
)</td>
</tr>
<tr>
<td>Zaire Ebolavirus (V) </td>
<td>Gabon, Republic of Congo</td>
<td>Pourrut et al. (
<xref ref-type="bibr" rid="CR195">2009</xref>
)</td>
</tr>
<tr>
<td>Lagos Bat Virus (V)</td>
<td>Kenya</td>
<td>Kuzmin et al. (
<xref ref-type="bibr" rid="CR118">2008</xref>
)</td>
</tr>
<tr>
<td>
<italic>Myonycteris torquata</italic>
(Little collared fruit bat)</td>
<td>Zaire Ebolavirus (V)</td>
<td>Gabon, Republic of Congo</td>
<td>Pourrut et al. (
<xref ref-type="bibr" rid="CR194">2007</xref>
,
<xref ref-type="bibr" rid="CR195">2009</xref>
)</td>
</tr>
<tr>
<td>
<italic>Nanonycteris veldkampii</italic>
(Veldkamp’s dwarf epauletted fruit bat)</td>
<td>Zaire Ebolavirus (V) </td>
<td>Ghana</td>
<td>Hayman et al. (
<xref ref-type="bibr" rid="CR91">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Rhinolophus eloquens</italic>
(Eloquent horseshoe bat)</td>
<td>Marburgvirus (V) </td>
<td>Democratic Republic of the Congo</td>
<td>Swanepoel et al. (
<xref ref-type="bibr" rid="CR229">2007</xref>
)</td>
</tr>
<tr>
<td>
<italic>Miniopterus inflatus</italic>
(Greater long-fingered bat)</td>
<td>Marburgvirus (V)</td>
<td>Democratic Republic of the Congo</td>
<td>Swanepoel et al. (
<xref ref-type="bibr" rid="CR229">2007</xref>
)</td>
</tr>
<tr>
<td>
<italic>Miniopterus schreibersii</italic>
(Schreibers’s long-fingered bat)</td>
<td>Duvengahe virus (V)</td>
<td>South Africa</td>
<td>Paweska et al. (
<xref ref-type="bibr" rid="CR181">2006</xref>
)</td>
</tr>
<tr>
<td>
<italic>Nycteris gambiensis</italic>
(Gambian slit-faced bat)</td>
<td>Lagos Bat Virus</td>
<td>Senegal</td>
<td>Institut Pasteur (
<xref ref-type="bibr" rid="CR100">1985</xref>
)</td>
</tr>
<tr>
<td>
<italic>Mops condylurus</italic>
(Angolan free-tailed bat)</td>
<td>Zaire Ebolavirus (V) </td>
<td>Gabon</td>
<td>Pourrut et al. (
<xref ref-type="bibr" rid="CR195">2009</xref>
)</td>
</tr>
<tr>
<td>Unspecified bat sp.</td>
<td>Duvengahe virus (V)</td>
<td>Kenya</td>
<td>van Thiel et al. (
<xref ref-type="bibr" rid="CR252">2009</xref>
)</td>
</tr>
<tr>
<td colspan="4">Rodents</td>
</tr>
<tr>
<td>
<italic>Funisciurus anerythrus</italic>
(Thomas’s rope squirrel)</td>
<td>Monkeypox virus (V)</td>
<td>Democratic Republic of the Congo</td>
<td>Khodakevich et al. (
<xref ref-type="bibr" rid="CR114">1986</xref>
)</td>
</tr>
<tr>
<td>
<italic>Funisciurus sp.</italic>
(African striped squirrel sp.)</td>
<td>Monkeypox virus (V)</td>
<td>Ghana</td>
<td>Reynolds et al. (
<xref ref-type="bibr" rid="CR199">2010</xref>
)</td>
</tr>
<tr>
<td>
<italic>Heliosciurus gambianus</italic>
(Gambian sun squirrel)</td>
<td>Monkeypox virus (V) </td>
<td>Ghana</td>
<td>Reynolds et al. (
<xref ref-type="bibr" rid="CR199">2010</xref>
)</td>
</tr>
<tr>
<td>
<italic>Paraxerus cepapi</italic>
(Smith’s bush squirrel)</td>
<td>
<italic>Leptospira</italic>
(B)</td>
<td>Botswana</td>
<td>Jobbins and Alexander (
<xref ref-type="bibr" rid="CR102">2015</xref>
)</td>
</tr>
<tr>
<td>
<italic>Xerus</italic>
sp. (African ground squirrel sp.)</td>
<td>Monkeypox virus (V)</td>
<td>Ghana</td>
<td>Reynolds et al. (
<xref ref-type="bibr" rid="CR199">2010</xref>
)</td>
</tr>
<tr>
<td>Unspecified squirrel sp.</td>
<td>Rabies (V) </td>
<td>Namibia, Zimbabwe</td>
<td>Pfukenyi et al. (
<xref ref-type="bibr" rid="CR189">2009</xref>
), Magwedere et al. (
<xref ref-type="bibr" rid="CR142">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Lophuromys sikapusi</italic>
(Rusty-bellied brush-furred rat)</td>
<td>Mokola virus (V) </td>
<td>Central African Republic</td>
<td>Saluzzo et al. (
<xref ref-type="bibr" rid="CR207">1984</xref>
)</td>
</tr>
<tr>
<td>
<italic>Mastomys natalensis</italic>
(Natal mastomys)</td>
<td>Lassa Fever (V)</td>
<td>Guinea</td>
<td>Ter Meulen et al. (
<xref ref-type="bibr" rid="CR237">1996</xref>
)</td>
</tr>
<tr>
<td>
<italic>Rattus norvegicus</italic>
(Brown rat)</td>
<td>
<italic>Leptospira</italic>
(B)</td>
<td>Botswana</td>
<td>Jobbins and Alexander (
<xref ref-type="bibr" rid="CR102">2015</xref>
)</td>
</tr>
<tr>
<td>Unspecified “rat species”</td>
<td>Rabies (V)</td>
<td>Namibia</td>
<td>Magwedere et al. (
<xref ref-type="bibr" rid="CR142">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Cricetomys sp.</italic>
(Giant pouched rat sp.)</td>
<td>Monkeypox virus (V) </td>
<td>Ghana</td>
<td>Reynolds et al. (
<xref ref-type="bibr" rid="CR199">2010</xref>
)</td>
</tr>
<tr>
<td>
<italic>Atherurus africanus</italic>
(African brush-tailed porcupine)</td>
<td>Salmonella (B)</td>
<td>Gabon</td>
<td>Bachand et al. (
<xref ref-type="bibr" rid="CR20">2012</xref>
)</td>
</tr>
<tr>
<td colspan="4">Aardvark</td>
</tr>
<tr>
<td>
<italic>Orycteropus afer</italic>
(Aardvark)</td>
<td>
<italic>Leptospira</italic>
(B) </td>
<td>Botswana</td>
<td>Jobbins and Alexander (
<xref ref-type="bibr" rid="CR102">2015</xref>
)</td>
</tr>
<tr>
<td colspan="4">Ungulates</td>
</tr>
<tr>
<td>
<italic>Equus burchellii</italic>
(Burchell’s zebra)</td>
<td>
<italic>Bacillus anthracis</italic>
(B)</td>
<td>Namibia</td>
<td>Magwedere et al. (
<xref ref-type="bibr" rid="CR142">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Phacochoerus aethiopicus</italic>
(Desert warthog)</td>
<td>Rabies (V) </td>
<td>Namibia</td>
<td>Magwedere et al. (
<xref ref-type="bibr" rid="CR142">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Phacochoerus africanus</italic>
(Common warthog)</td>
<td>
<italic>Leptospira</italic>
(B)</td>
<td>Botswana</td>
<td>Jobbins and Alexander (
<xref ref-type="bibr" rid="CR102">2015</xref>
)</td>
</tr>
<tr>
<td rowspan="2">
<italic>Alcelaphus buselaphus</italic>
(Hartebeest)</td>
<td>Rabies (V)</td>
<td>Namibia</td>
<td>Magwedere et al. (
<xref ref-type="bibr" rid="CR142">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Bacillus anthracis</italic>
(B)</td>
<td>Namibia</td>
<td>Magwedere et al. (
<xref ref-type="bibr" rid="CR142">2012</xref>
)</td>
</tr>
<tr>
<td rowspan="2">
<italic>Connochaetes taurinus</italic>
(Blue wildebeest)</td>
<td>Rabies (V) </td>
<td>Namibia</td>
<td>Magwedere et al. (
<xref ref-type="bibr" rid="CR142">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Bacillus anthracis</italic>
(B)</td>
<td>Namibia, Tanzania</td>
<td>Lembo et al. (
<xref ref-type="bibr" rid="CR130">2011</xref>
), Magwedere et al. (
<xref ref-type="bibr" rid="CR142">2012</xref>
)</td>
</tr>
<tr>
<td rowspan="3">
<italic>Antidorcas marsupialis</italic>
(Springbok)</td>
<td>Rabies (V)</td>
<td>Namibia</td>
<td>Magwedere et al. (
<xref ref-type="bibr" rid="CR142">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Bacillus anthracis</italic>
(B)</td>
<td>Namibia</td>
<td>Magwedere et al. (
<xref ref-type="bibr" rid="CR142">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Brucella</italic>
(B) </td>
<td>Namibia</td>
<td>Magwedere et al. (
<xref ref-type="bibr" rid="CR141">2011</xref>
)</td>
</tr>
<tr>
<td rowspan="2">
<italic>Syncerus caffer</italic>
(African buffalo)</td>
<td>
<italic>Bacillus anthracis</italic>
(B)</td>
<td>Tanzania</td>
<td>Lembo et al. (
<xref ref-type="bibr" rid="CR130">2011</xref>
)</td>
</tr>
<tr>
<td>
<italic>Brucella</italic>
(B)</td>
<td>Botswana, Mozambique</td>
<td>Alexander et al. (
<xref ref-type="bibr" rid="CR8">2012</xref>
), Tanner et al. (
<xref ref-type="bibr" rid="CR234">2014</xref>
)</td>
</tr>
<tr>
<td rowspan="2">
<italic>Taurotragus oryx</italic>
(Common eland)</td>
<td>Rabies (V) </td>
<td>Namibia, Zimbabwe</td>
<td>Pfukenyi et al. (
<xref ref-type="bibr" rid="CR189">2009</xref>
), Magwedere et al. (
<xref ref-type="bibr" rid="CR142">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Bacillus anthracis</italic>
(B)</td>
<td>Namibia</td>
<td>Magwedere et al. (
<xref ref-type="bibr" rid="CR142">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Tragelaphus strepsiceros</italic>
(Greater kudu)</td>
<td>Rabies (V)</td>
<td>Namibia, Zimbabwe</td>
<td>Pfukenyi et al. (
<xref ref-type="bibr" rid="CR189">2009</xref>
), Magwedere et al. (
<xref ref-type="bibr" rid="CR142">2012</xref>
)</td>
</tr>
<tr>
<td>
<italic>Cephalophus</italic>
sp. (Duiker sp.)</td>
<td>Zaire Ebolavirus (V)</td>
<td>Gabon</td>
<td>Leroy et al. (
<xref ref-type="bibr" rid="CR132">2004a</xref>
)</td>
</tr>
<tr>
<td>
<italic>Sylvicapra grimmia</italic>
(Bush duiker)</td>
<td>Rabies (V) </td>
<td>Zimbabwe</td>
<td>Pfukenyi et al. (
<xref ref-type="bibr" rid="CR189">2009</xref>
)</td>
</tr>
<tr>
<td>
<italic>Hippotragus niger</italic>
(Sable antelope)</td>
<td>Rabies (V)</td>
<td>Zimbabwe</td>
<td>Pfukenyi et al. (
<xref ref-type="bibr" rid="CR189">2009</xref>
)</td>
</tr>
<tr>
<td>
<italic>Oryx gazelle</italic>
(Gemsbok)</td>
<td>Rabies (V)</td>
<td>Namibia</td>
<td>Magwedere et al. (
<xref ref-type="bibr" rid="CR142">2012</xref>
)</td>
</tr>
<tr>
<td>Unspecified “oryx,” “antelope,” “duiker” </td>
<td>Rabies (V)</td>
<td>Namibia</td>
<td>Magwedere et al. (
<xref ref-type="bibr" rid="CR142">2012</xref>
)</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<p>
<italic>V virus</italic>
,
<italic>H</italic>
helminth,
<italic>P</italic>
protozoan,
<italic>B</italic>
bacteria</p>
<p>
<sup>a</sup>
See text for further discussions of pathogens in great apes, including uncertainty as to whether apes or humans are the source of spillovers</p>
</table-wrap-foot>
</table-wrap>
</p>
</sec>
<sec id="Sec8">
<title>Viral Pathogens</title>
<p id="Par29">Viruses are obligatoryintracellular parasites characterized primarily by the nature of their nucleic acids (DNA or RNA; single or double stranded, etc.). They are the most abundant form of life on earth; many viruses are recognized as important disease-causing agents, and they are subject to frequent mutation and thus evolution. The advent of modern molecular techniqueshas advanced our understanding of viral diversity and pathogenesis in both animal and human hosts. For example, in relation to bushmeat, it is now clear that many virus variants are present in hunted nonhuman primate species, which have received most of the research attention, and that these variants have crossed between nonhuman primates and humans on multiple occasions (Peeters and Delaporte
<xref ref-type="bibr" rid="CR185">2012</xref>
; Table
<xref rid="Tab1" ref-type="table">24.1</xref>
). Bats and rodentsare also major zoonotic virus carriers (Meerburg et al.
<xref ref-type="bibr" rid="CR152">2009</xref>
; Baker et al.
<xref ref-type="bibr" rid="CR22">2013</xref>
); other taxonomic groups are less studied, at least in sub-Saharan Africa. Several sub-Saharan African viruses of importance are vector-borne, including Rift Valley Fever and Crimean-Congo hemorrhagic fever. While one presumes that this would make them unlikely to spread via bushmeat-related activities, the possibility remains that animal handling could present a risk (Magwedere et al.
<xref ref-type="bibr" rid="CR142">2012</xref>
). However, no significant links between vector-borne viruses and bushmeat hunting have been made, and we will not include a discussion of these viruses here.</p>
<p id="Par30">: Themost notable virus to emerge from the bushmeat interface is human immunodeficiency virus (HIV). While the origin of HIV was long obscured, Human HIV-1 and HIV-2 are believed to have evolved from strains of simian immunodeficiency virus (SIV) (Hahn et al.
<xref ref-type="bibr" rid="CR87">2000</xref>
; Lemey et al.
<xref ref-type="bibr" rid="CR131">2003</xref>
; Van Heuverswyn and Peeters
<xref ref-type="bibr" rid="CR249">2007</xref>
; Sharp and Hahn
<xref ref-type="bibr" rid="CR213">2010</xref>
; Peeters and Delaporte
<xref ref-type="bibr" rid="CR185">2012</xref>
; Peeters et al.
<xref ref-type="bibr" rid="CR187">2013</xref>
; Kazanji et al.
<xref ref-type="bibr" rid="CR110">2015</xref>
). Evidence suggests that SIV crossed over to humans by blood contact when hunters had an exposed open wound or injured themselves during the butchering of nonhuman primates (Hahn et al.
<xref ref-type="bibr" rid="CR87">2000</xref>
; Wolfe et al.
<xref ref-type="bibr" rid="CR267">2004a</xref>
,
<xref ref-type="bibr" rid="CR268">b</xref>
; Karesh and Noble
<xref ref-type="bibr" rid="CR108">2009</xref>
). The closest relatives of HIV-1 found among nonhuman primates are SIVcpz and SIVgor, from common chimpanzees and western gorillas in west central Africa (Gao et al.
<xref ref-type="bibr" rid="CR72">1999</xref>
; Sharp et al.
<xref ref-type="bibr" rid="CR214">2005</xref>
; Keele et al.
<xref ref-type="bibr" rid="CR111">2006</xref>
; Van Heuverswyn et al.
<xref ref-type="bibr" rid="CR250">2006</xref>
,
<xref ref-type="bibr" rid="CR251">2007</xref>
; Takehisa et al.
<xref ref-type="bibr" rid="CR232">2009</xref>
) and at least four separate spillovers have occurred (Peeters et al.
<xref ref-type="bibr" rid="CR187">2013</xref>
). HIV-2 is derived from SIVsmm from sooty mangabeys (
<italic>Cercocebus atys</italic>
) in West Africa (Apetrei et al.
<xref ref-type="bibr" rid="CR16">2005</xref>
; Hirsch et al.
<xref ref-type="bibr" rid="CR93">1989</xref>
; Gao et al.
<xref ref-type="bibr" rid="CR71">1992</xref>
; Ayouba et al.
<xref ref-type="bibr" rid="CR18">2013</xref>
), where high viral genetic diversity exists and where transmission is believed to have occurred at least eight times.</p>
<p id="Par31">The potential for future and continued spillovers from SIVs is high, and multiple species-specific variants exist. For example, Peeters et al. (
<xref ref-type="bibr" rid="CR186">2002</xref>
) and Peeters (
<xref ref-type="bibr" rid="CR184">2004</xref>
) estimated that more than 20 % of nonhuman primates hunted for food are infected with a variant of SIV; Locatelli and Peeters (
<xref ref-type="bibr" rid="CR139">2012</xref>
) and Peeters et al. (
<xref ref-type="bibr" rid="CR187">2013</xref>
) noted that at least 45 species-specific variants of SIV from at least 45 primate species are currently recognized. Aghokeng et al. (
<xref ref-type="bibr" rid="CR4">2010</xref>
) sampled 1856 nonhuman primate carcasses from 11 species found in bushmeat markets in Cameroon. They documented low overall prevalence of SIV (only 2.93 % of carcasses), with the lowest prevalence found among the most common species in the market. However, they did find SIVvariants in about 70 % of the tested primate species. In total, serological evidence of SIV infection has been documented for at least 40 different primate species (Aghokeng et al.
<xref ref-type="bibr" rid="CR4">2010</xref>
; Liégeois et al.
<xref ref-type="bibr" rid="CR135">2011</xref>
,
<xref ref-type="bibr" rid="CR136">2012</xref>
). Cross-species transmission of strains and co-infection with more than one strain have been documented, sometimes followed by genetic recombination (Hahn et al.
<xref ref-type="bibr" rid="CR87">2000</xref>
; Bibollet-Ruche et al.
<xref ref-type="bibr" rid="CR27">2004</xref>
; Aghokeng et al.
<xref ref-type="bibr" rid="CR3">2007</xref>
; Gogarten et al.
<xref ref-type="bibr" rid="CR78">2014</xref>
), a recipe for future spillovers into humans (Locatelli and Peeters
<xref ref-type="bibr" rid="CR139">2012</xref>
).</p>
<p id="Par32">
<italic>Human T-Cell Lymphotropic Virus (HTLV)</italic>
: Similar to HIV, human T-lymphotropic viruses (HTLV) are related to simian viral lineages in which significant diversity has been found (Ahuka-Mundeke et al.
<xref ref-type="bibr" rid="CR6">2012</xref>
; Peeters and Delaporte
<xref ref-type="bibr" rid="CR185">2012</xref>
). All three sub-Saharan great apes and 30 additional nonhuman primates have been documented to have STLV/HTLV variants and a variety of HTLV viruses have been documented in wildlife and in central African hunters (Calattini et al.
<xref ref-type="bibr" rid="CR39">2009</xref>
,
<xref ref-type="bibr" rid="CR40">2011</xref>
; Courgnaud et al.
<xref ref-type="bibr" rid="CR49">2004</xref>
; Sintasath et al.
<xref ref-type="bibr" rid="CR219">2009a</xref>
,
<xref ref-type="bibr" rid="CR220">b</xref>
; Wolfe et al.
<xref ref-type="bibr" rid="CR270">2005b</xref>
; Zheng et al.
<xref ref-type="bibr" rid="CR277">2010</xref>
; Locatelli and Peeters
<xref ref-type="bibr" rid="CR139">2012</xref>
). Similar to HIV/SIV, dual infections with more than one variant have been documented in nonhuman primates (Agile mangabeys,
<italic>Cercocebus agilis</italic>
; Courgnaud et al.
<xref ref-type="bibr" rid="CR49">2004</xref>
) and in humans (Calattini et al.
<xref ref-type="bibr" rid="CR40">2011</xref>
; Wolfe et al.
<xref ref-type="bibr" rid="CR270">2005b</xref>
).</p>
<p id="Par33">
<italic>Simian Foamy Virus</italic>
: Simian foamy retroviruses ( SFV) areendemic in most African primates (Hussain et al.
<xref ref-type="bibr" rid="CR96">2003</xref>
; Switzer et al.
<xref ref-type="bibr" rid="CR231">2005</xref>
; Peeters and Delaporte
<xref ref-type="bibr" rid="CR185">2012</xref>
) and are known to transmit to humans (Sandstrom et al.
<xref ref-type="bibr" rid="CR209">2000</xref>
; Switzer et al.
<xref ref-type="bibr" rid="CR230">2004</xref>
; Calattini et al.
<xref ref-type="bibr" rid="CR38">2007</xref>
; Mouinga-Ondémé et al.
<xref ref-type="bibr" rid="CR163">2010</xref>
,
<xref ref-type="bibr" rid="CR164">2012</xref>
). Like the other retroviruses discussed above (HIV and HTLV), SFV is genetically diverse and relatively host species-specific. In Cameroon, Wolfe et al. (
<xref ref-type="bibr" rid="CR268">2004b</xref>
) documented three geographically independent SFV infections, which could be traced to De Brazza’s monkey (
<italic>Cercopithecus neglectus</italic>
), mandrill (
<italic>Mandrillus sphinx</italic>
), and western gorilla. Likewise, in Gabon, Mouinga-Ondémé et al. (
<xref ref-type="bibr" rid="CR163">2010</xref>
,
<xref ref-type="bibr" rid="CR164">2012</xref>
) documented human spillover events involving multiple strains of SFV, with infected humans having been bitten by common chimpanzees, western gorillas, or mandrills infected with their respective variant of SFV.</p>
<p id="Par34">
<italic>Ebola and Marburg Viruses</italic>
: There are sevenspecies of filoviruses currently identified, five of which occur in sub-Saharan Africa—Genus
<italic>Ebolavirus</italic>
: Tai forest ebolavirus (TAFV), Sudan ebolavirus (SUDV), Zaire ebolavirus (EBOV), Bundibugyo virus (BDBV); Genus
<italic>Marburgvirus:</italic>
Marburg virus ( MARV) . These pathogens are periodically emerging viruses, typically from single spillover events, which cause hemorrhagic fevers (reviewed by Olival and Hayman
<xref ref-type="bibr" rid="CR179">2014</xref>
; Rougeron et al.
<xref ref-type="bibr" rid="CR203">2015</xref>
(but note that Rougeron’s listing for a single case of SUDV in Sudan in 2011 is erroneous)). The 2014–2015 West Africa outbreak of EBOV is still ongoing at the time of this writing (Labouba and Leroy
<xref ref-type="bibr" rid="CR121">2015</xref>
). While the zoonotic source of this outbreak is unknown, three initial outbreaks of the Ebola virus in the Democratic Republic of the Congo from 1976 to 1979 involved victims who were reported to have handled western gorilla or common chimpanzee carcasses or to have had physical contact with people who touched the animals (Leroy et al.
<xref ref-type="bibr" rid="CR132">2004a</xref>
,
<xref ref-type="bibr" rid="CR133">b</xref>
). Similarly, Marburgvirus was first identified in laboratory workers who had dissected imported grivet (
<italic>Chlorocebus aethiops</italic>
) (Martini et al.
<xref ref-type="bibr" rid="CR148">1968</xref>
; Siegert et al.
<xref ref-type="bibr" rid="CR216">1968</xref>
). Both western gorillas and common chimpanzees have suffered significant mortality from filovirus outbreaks (Walsh et al.
<xref ref-type="bibr" rid="CR258">2003</xref>
; Leroy et al.
<xref ref-type="bibr" rid="CR132">2004a</xref>
,
<xref ref-type="bibr" rid="CR133">b</xref>
; Bermejo et al.
<xref ref-type="bibr" rid="CR26">2006</xref>
; Rizkalla et al.
<xref ref-type="bibr" rid="CR201">2007</xref>
) and antibodies to EBOV were documented in several other primate species by Leroy et al. (
<xref ref-type="bibr" rid="CR133">2004b</xref>
). The single case of TAFV occurred in an ethnologist likely infected while performing a necropsy of a dead common chimpanzee following a rash of common chimpanzee deaths in the Tai National Park in Côte d’Ivoire (Le Guenno et al.
<xref ref-type="bibr" rid="CR123">1995</xref>
; Wyers et al.
<xref ref-type="bibr" rid="CR275">1999</xref>
). Beyond primates, other incidental hosts in the wild are possible, as was demonstrated for duikers (
<italic>Cephalophus</italic>
spp.) (Leroy et al.
<xref ref-type="bibr" rid="CR132">2004a</xref>
; Rouquet et al.
<xref ref-type="bibr" rid="CR204">2005</xref>
). As reviewed by Weingartl et al. (
<xref ref-type="bibr" rid="CR259">2013</xref>
), both dogs (naturally) and pigs (at least experimentally) can also be infected. During the 2001–2002 EBOV outbreak in Gabon, Allela et al. (
<xref ref-type="bibr" rid="CR11">2005</xref>
) found over 30 % seroprevalence in dogs living in villages with EBOV human and animal cases. Those dogs appeared to be asymptomatic and were presumed to be exposed by scavenging wild animals.</p>
<p id="Par35">Although incidental hosts likely play important roles in the ecology of these viruses, especially when moribund or dead animals are consumed, strong evidence suggests that bats are thenatural reservoir hosts for at least Marburgvirus and EBOV. For Marburgvirus, the cave dwelling and densely packed Egyptian rousette fruit bat (
<italic>Rousettus aegyptiacus</italic>
) is now well-documented as areservoir host (Towner et al.
<xref ref-type="bibr" rid="CR241">2009</xref>
; Amman et al.
<xref ref-type="bibr" rid="CR14">2012</xref>
), but antibodies against the virus and/or the presence of viral RNA have been found in several other species (see Table
<xref rid="Tab1" ref-type="table">24.1</xref>
). The strong association of Marburgvirus with the Egyptian rousette makes sense in light of the outbreaks of this virus in people visiting tourist caves or working in mines (Adjemian et al.
<xref ref-type="bibr" rid="CR2">2011</xref>
; Timen et al.
<xref ref-type="bibr" rid="CR239">2009</xref>
; Towner et al.
<xref ref-type="bibr" rid="CR241">2009</xref>
; Amman et al.
<xref ref-type="bibr" rid="CR14">2012</xref>
). The picture for EBOV is less clear, but evidence of infection has been found in at least eight sub-Saharan bat species (Pourrut et al.
<xref ref-type="bibr" rid="CR194">2007</xref>
,
<xref ref-type="bibr" rid="CR195">2009</xref>
; Hayman et al.
<xref ref-type="bibr" rid="CR90">2010</xref>
,
<xref ref-type="bibr" rid="CR91">2012</xref>
; Table
<xref rid="Tab1" ref-type="table">24.1</xref>
). Of the ten bat species listed in Table
<xref rid="Tab1" ref-type="table">24.1</xref>
for Marburgvirus and EBOV, seven are fruit bats, which are relatively larger and more visible, and thus targets of bushmeat hunters. That said, bushmeat hunting of these bats is not ubiquitous throughout their range and cannot solely explain filovirus spillovers. Mari Saéz et al. (
<xref ref-type="bibr" rid="CR144">2015</xref>
) unconvincingly suggested the non-fruit bat,
<italic>Mops condylurus,</italic>
might have been the source of the 2014–2015 West African Ebola outbreak. Pourrut et al. (
<xref ref-type="bibr" rid="CR195">2009</xref>
) found evidence of antibodies against ZEBOV in this species, but there is no real evidence that this free-tailed bat played a role in the 2014–2015 outbreak. To date, no bat host has been identified for BDBV, SUDV, or TAFV and broader surveillance for indications of these viruses in bats and other hosts should be conducted.</p>
<p id="Par36">
<italic>Henipaviruses and Other Paramyxoviruses</italic>
: Hendra virus and Nipah virus (HNVs) are paramyxoviruses in the genus
<italic>Henipavirus</italic>
that emerged in Australia and southeast Asia, respectively, with fruitbats in the genus
<italic>Pteropus</italic>
(family Pteropodidae) as reservoir hosts (reviewed by Croser and Marsh
<xref ref-type="bibr" rid="CR50">2013</xref>
). However, recent studies have identified
<italic>Henipavirus</italic>
and Henipa-like viruses in sub-Saharan African fruit bats, which are a phylogenetically distinct clade of pteropodid bats that do not overlap distributionally with any
<italic>Pteropus</italic>
species. Documentation of
<italic>Henipavirus</italic>
and related RNA (Drexler et al.
<xref ref-type="bibr" rid="CR60">2009</xref>
; Muleya et al.
<xref ref-type="bibr" rid="CR167">2014</xref>
; Baker et al.
<xref ref-type="bibr" rid="CR21">2012</xref>
) and anti-
<italic>Henipavirus</italic>
antibodies (Hayman et al.
<xref ref-type="bibr" rid="CR89">2008</xref>
; Pernet et al.
<xref ref-type="bibr" rid="CR188">2014</xref>
) in the African straw-colored fruit bat (
<italic>Eidolon helvum</italic>
) clearly show that this deadly and diverse viral group is present in sub-Saharan Africa. This bat species is a frequent target of hunters and a significant protein source where it is found (Kamins et al.
<xref ref-type="bibr" rid="CR106">2011b</xref>
). Weiss et al. (
<xref ref-type="bibr" rid="CR260">2012</xref>
) documented the presence of this group of viruses in these bats found live in bushmeat markets. Strong evidence of spillover to humans was documented by Pernet et al. (
<xref ref-type="bibr" rid="CR188">2014</xref>
) who found antibodies against HNVs in human samples from Cameroon. These seropositive human samples were found almost exclusively in individuals who reported butchering these bats. This bat is also a long-distance migrator with significant panmixia across the continent, which could facilitate viral transmission between bats (Peel et al.
<xref ref-type="bibr" rid="CR183">2013</xref>
).</p>
<p id="Par37">The paramyxovirus story in sub-Saharan Africa is still unfolding. Both Drexler et al. (
<xref ref-type="bibr" rid="CR61">2012</xref>
) and Baker et al. (
<xref ref-type="bibr" rid="CR21">2012</xref>
) describe great diversity in paramyxoviruses from sub-Saharan bats. In their comprehensive study of the evolutionary history of this virus family, Drexler et al. (
<xref ref-type="bibr" rid="CR61">2012</xref>
) found that the
<italic>Henipavirus</italic>
lineage originated in Africa and identified bats as the likely origin of this large family of viruses. A precautionary tale from sub-Saharan Africa comes from the recent discovery and naming of the Sosuga virus from a wildlife researcher who became very ill after handling and dissecting hundreds of bats and rodents in Uganda and South Sudan (Albariño et al.
<xref ref-type="bibr" rid="CR7">2014</xref>
). This virus is most closely related to Tuhoko virus 3, a rubula-like virus recently isolated from the Leschenault’s Rousette fruit bat (
<italic>Rousettus leschenaultii</italic>
) in southern China. Amman et al. (
<xref ref-type="bibr" rid="CR15">2015</xref>
) subsequently found Sosuga virus in
<italic>R. aegyptiacus</italic>
captured from multiple locations in Uganda; the researcher infected by this virus handled this species extensively in her studies.</p>
<p id="Par38">
<italic>Rabies and Other Lyssaviruses</italic>
: Rabies is theoldest known zoonotic EID, recorded as early as the twenty-third century BC (Steele and Fernandez
<xref ref-type="bibr" rid="CR224">1991</xref>
). An estimated 25,000 people die in Africa each year from rabies (Dodet et al.
<xref ref-type="bibr" rid="CR59">2015</xref>
), some portion of which may be from exposure that occurs in bushmeat-related activities, although most human cases can be attributed to domestic dogs. Rabies virus (RABV) is in the
<italic>Lyssavirus</italic>
genus. It is joined in Africa by at least five additional species: Lagos bat virus (LBV), Mokola virus (MOKV), Duvenhage virus (DUVV), Shimoni bat virus (SHIBV), and the newly proposed Ikoma lyssavirus (IKOV). These viruses have bat(s) astheir reservoir host (Banyard et al.
<xref ref-type="bibr" rid="CR23">2014</xref>
) with two exceptions. The Mokola virus is found in shrews (
<italic>Crocidura</italic>
spp.), rusty-bellied brush-furred rat (
<italic>Lophuromys sikapusi</italic>
; Saluzzo et al.
<xref ref-type="bibr" rid="CR207">1984</xref>
), and companion animals (Delmas et al.
<xref ref-type="bibr" rid="CR58">2008</xref>
; Kgaladi et al.
<xref ref-type="bibr" rid="CR113">2013</xref>
). The Ikoma virus has thus far only been documented in African civets (
<italic>Civettictis civetta</italic>
; Table
<xref rid="Tab1" ref-type="table">24.1</xref>
, Marston et al.
<xref ref-type="bibr" rid="CR147">2012</xref>
). A variety of wildlife species can be secondary hosts of rabies (e.g., in Botswana, see Moagabo et al.
<xref ref-type="bibr" rid="CR159">2009</xref>
) and rabies has been documented to occur in a number of nonhuman primate species, including those encountered in the bushmeat trade (Gautret et al.
<xref ref-type="bibr" rid="CR73">2014</xref>
). Lyssaviruses are found worldwide, but the greatest genetic diversity is in Africa and Lagos bat virus may be more than one species (Delmas et al.
<xref ref-type="bibr" rid="CR58">2008</xref>
; Markotter et al.
<xref ref-type="bibr" rid="CR146">2008</xref>
; Kuzmin et al.
<xref ref-type="bibr" rid="CR119">2010a</xref>
). While most human cases are due to rabies virus, Duvenhage virus has been documented in human fatalities associated with bat scratches that likely transmitted the virus (van Thiel et al.
<xref ref-type="bibr" rid="CR252">2009</xref>
; Paweska et al.
<xref ref-type="bibr" rid="CR181">2006</xref>
). Mokolo virus has been detected in two human cases without mortality (Kgaladi et al.
<xref ref-type="bibr" rid="CR113">2013</xref>
).</p>
<p id="Par39">The lyssavirus story in Africa will continue to emerge due to increased surveillance and improved molecular techniques. The 2012 discovery of Ikoma virus in an African civet in Serengeti National Park in Tanzania, where domestic dogs are largely absent and detection in bat hosts is nonexistent (Marston et al.
<xref ref-type="bibr" rid="CR147">2012</xref>
; Horton et al.
<xref ref-type="bibr" rid="CR95">2014</xref>
), highlights the likelihood that many more lyssaviruses exist in a variety of host species. The true diversity of lyssaviruses in Africa, and the potential for human spillover via bushmeat-related activities, remains to be discovered.</p>
<p id="Par40">
<italic>Lassa and Other Arenaviruses</italic>
: Arenaviruses include a number of zoonotic species, typically transmitted from rodents to humans. Lassa virus is the best known of the viral hemorrhagic arenaviruses in Africa and is well-documented in West Africa, especially Guinea, Sierra Leone, Nigeria, and Liberia. As with some of the bacterial pathogens described below, the primary risk comes from peridomestic exposure to the rodent host, the natal mastomys (
<italic>Mastomys natalensis</italic>
), via exposure to urine or fecal materials. However, Ter Meulen et al. (
<xref ref-type="bibr" rid="CR237">1996</xref>
) found a strong association between hunting of peridomestic rodents and antibodies to and symptoms of Lassa virus, tying bushmeat-related activities to the spillover of this virus to humans.</p>
<p id="Par41">
<italic>Human Monkeypox Virus</italic>
: Contrary to its moniker, thereservoir hostsof human monkeypox virus (MPX) are neither monkeys nor humans, but rather rodents. The first case of human monkeypox was identified in 1970 in the Democratic Republic of the Congo, with subsequent outbreaks in Liberia, Sierra Leone, Côte d’Ivoire, Nigeria, and Democratic Republic of the Congo (reviewed by Reynolds et al.
<xref ref-type="bibr" rid="CR199">2010</xref>
; Rimoin et al.
<xref ref-type="bibr" rid="CR200">2010</xref>
). Recent MPX increases in the Democratic Republic of the Congo and elsewhere have been attributed to cessation of the human smallpox vaccine, which conferred some immunity to other pox viruses (Rimoin et al.
<xref ref-type="bibr" rid="CR200">2010</xref>
). Human and nonhuman primate infections are suspected to result from wildlife exposure such as would occur in bushmeat-related activities; infected species include squirrels (e.g., Thomas’s rope squirrel,
<italic>Funisciurus anerythrus</italic>
; Khodakevich et al.
<xref ref-type="bibr" rid="CR114">1986</xref>
; African ground squirrels;
<italic>Xerus</italic>
sp.; Reynolds et al.
<xref ref-type="bibr" rid="CR199">2010</xref>
), dormice (
<italic>Graphiurus</italic>
sp.; Reynolds et al.
<xref ref-type="bibr" rid="CR199">2010</xref>
), and giant pouched rats (
<italic>Cricetomys</italic>
sp.; Reynolds et al.
<xref ref-type="bibr" rid="CR199">2010</xref>
). The outbreak that occurred in the USA in 2007 after exposure to rodents in the illegal pet trade also linked human monkeypox to rope squirrels, dormice, and pouched rats (Hutson et al.
<xref ref-type="bibr" rid="CR97">2007</xref>
). While dormice are small and not likely to be the target of hunting, the diurnal and highly visible squirrels and the giant pouched rats are routinely hunted (Taylor et al.
<xref ref-type="bibr" rid="CR236">2015</xref>
), making the spillover to humans highly plausible.</p>
</sec>
<sec id="Sec9">
<title>Bacteria</title>
<p id="Par42">Jones et al. (
<xref ref-type="bibr" rid="CR103">2008</xref>
) list 54.3 % of EID events asbeing caused by bacteria and there is good evidence to suggest that bacterial pathogens have the potential to be just as important as viruses when it comes to those that may spillover due to bushmeat-related activities, but in this capacity they have received far less attention (Cantas and Suer
<xref ref-type="bibr" rid="CR41">2014</xref>
). Transmission pathways for bacterial pathogens can occur through direct exposure to body fluids or feces, but they can also possibly be transferred indirectly through exposure to disease vectors such as fleas and ticks when handling animals. In a rare survey of bacterial pathogens that might spillover via bushmeat-related activities, Bachand et al. (
<xref ref-type="bibr" rid="CR20">2012</xref>
) sampled muscle from 128 bushmeat carcasses from multiple species at markets in Gabon for the presence of
<italic>Campylobacter</italic>
,
<italic>Salmonella</italic>
, and
<italic>Shigella</italic>
. While they only recorded the presence of
<italic>Salmonella</italic>
, the potential for contamination and thus spillover of enteric pathogens from carcass handling remains high, especially in the days after purchase when pathogens continue to replicate. Bacteria in the genus
<italic>Leptospira</italic>
are endemic sub-Saharan African pathogens that have a high risk of spillover during bushmeat-related activities as they are shed in urine. Jobbins and Alexander (
<xref ref-type="bibr" rid="CR102">2015</xref>
) documented their widespread presence in wild mammals, birds, and reptiles, highlighting the role that wildlife may play in leptospirosis. The bushmeat interface may also play a role in human cases of anthrax, caused by
<italic>Bacillis anthracis</italic>
, which is largely a disease of grazing herbivorous mammals, but to which common chimpanzees are also susceptible (Leendertz et al.
<xref ref-type="bibr" rid="CR128">2004</xref>
). If bushmeat includes not only the hunting of apparently healthy animals but also sick animals or salvage of contaminated carcasses, the risk of human outbreaks increases (Hang’ombe et al.
<xref ref-type="bibr" rid="CR88">2012</xref>
).</p>
<p id="Par43">A number of bacterial pathogens are vector-borne, which at face value would make them unlikely to spread via bushmeat-related activities. However, especially for bacteria with flea or tick as vectors, as opposed to mosquitoes for example, one can envision that animal handling could present a risk. The most frightening among the vector-borne bacterial pathogens is plague, caused by the bacteria
<italic>Yersinia pestis</italic>
and transmitted through the infected fleas of rodents. Africa remains an endemicregion of importance for this pathogen (World Health Organization
<xref ref-type="bibr" rid="CR274">2005</xref>
; Davis et al.
<xref ref-type="bibr" rid="CR54">2006</xref>
). Fleas and ticks are also responsible for transmitting rickettsial pathogens, such as
<italic>Rickettsia africae</italic>
, which causes African tick-bite fever ( ATBF) . Mediannikov et al. (
<xref ref-type="bibr" rid="CR151">2012</xref>
) collected ticks from duikers and a pangolin that were living in close proximity to humans in Guinea and found
<italic>R. africae</italic>
in 10 % of ticks collected from the tree pangolin (
<italic>Manis tricuspis</italic>
), suggesting the potential for spillover with the close handling of these animals. Further research is clearly and urgently needed to fully assess the potential for bacterial disease spillovers viabushmeat-related activities.</p>
</sec>
<sec id="Sec10">
<title>Helminths</title>
<p id="Par44">The helminths or “worm-like” animalsinclude many parasites of zoonotic potential, although Taylor et al. (
<xref ref-type="bibr" rid="CR235">2001</xref>
) found helminthes less likely to cause EIDs. Humans engaging in bushmeat-related activities are likely exposed to these pathogens via exposure to fecal material in which eggs are shed, from transcutaneous exposure to infectious larvae, or from consumption of uncooked meat (McCarthy and Moore
<xref ref-type="bibr" rid="CR150">2000</xref>
). Several studies have examined the prevalence of helminths in animals from bushmeat markets and found high rates of multiple species. For example, Adejinmi and Emikpe (
<xref ref-type="bibr" rid="CR1">2011</xref>
) collected fecal samples from greater cane rats (
<italic>Thryonomys swinderianus</italic>
) and bush duikers (
<italic>Sylvicapra grimmia</italic>
) in bushmeat markets in Nigeria and documented high prevalence rates (83.3 % and 53.8 %, respectively) of helminth ova in feces as well as larvae from fecal cultures. Likewise, Magwedere et al. (
<xref ref-type="bibr" rid="CR142">2012</xref>
) and Mukaratirwa et al. (
<xref ref-type="bibr" rid="CR166">2013</xref>
) reviewed the evidence for
<italic>Trichinella</italic>
infection in humans, livestock, and wildlife in sub-Saharan Africa and noted that bush-pigs (
<italic>Potamochoerus</italic>
spp.) and desert warthogs (
<italic>Phacochoerus aethiopicus</italic>
) are a source for human infection. As is the case with many other pathogens, humans and nonhuman primates share susceptibility to many parasitic helminth species (Pedersen et al.
<xref ref-type="bibr" rid="CR182">2005</xref>
; Pourrut et al.
<xref ref-type="bibr" rid="CR196">2011</xref>
). Pourrut et al. (
<xref ref-type="bibr" rid="CR196">2011</xref>
) sampled gastrointestinal parasites from 78 wild monkeys of 9 species collected from bushmeat markets in Cameroon and documented high helminth loads, including species known to infect humans. Gillespie et al. (
<xref ref-type="bibr" rid="CR77">2010</xref>
) had similar findings from common chimpanzee fecal samples. Overall, the available evidence suggests that spillover of many of these pathogens during bushmeat-related activities is likely.</p>
</sec>
<sec id="Sec11">
<title>Protozoan</title>
<p id="Par45">Protozoans are a paraphyleticgroup of eukaryotic organisms that are neither animals, plants, nor fungi and include amoebas and giardia. The risk of protozoan spillover from bushmeat-related activities is similar to that for helminths and bacteria in that exposure to feces, bodily fluids, and even potentially to meat could transmit disease to a permissive human host (Pourrut et al.
<xref ref-type="bibr" rid="CR196">2011</xref>
). A number of protozoans are important pathogens with zoonotic potential (Taylor et al.
<xref ref-type="bibr" rid="CR235">2001</xref>
). Perhaps the best example are the amoebozoa, which cause diarrheal disease and which are documented in a variety of animals, including bushmeat species such as nonhuman primates (Gillespie et al.
<xref ref-type="bibr" rid="CR77">2010</xref>
; Pourrut et al.
<xref ref-type="bibr" rid="CR196">2011</xref>
). Gillespie et al. (
<xref ref-type="bibr" rid="CR77">2010</xref>
) documented the amoeba
<italic>Entamoeba histolytica</italic>
and the ciliated protozoan
<italic>Balantidium coli</italic>
in common chimpanzees; both are human pathogens (although the direction of spillover is uncertain, as common chimpanzees and other primates may have obtained this parasite from humans). Indeed, Lilly et al. (
<xref ref-type="bibr" rid="CR137">2002</xref>
) documented both protozoans in common chimpanzees, western gorillas, agile mangabeys, and humans living in the same region in Central African Republic. A number of other nonhuman primates have had documented
<italic>E. histolytica</italic>
infections as well (see Table
<xref rid="Tab1" ref-type="table">24.1</xref>
). Other protozoan examples include
<italic>Toxoplasma gondii</italic>
, which causes the disease toxoplasmosis, but could not be detected during a recent, albeit small scale, survey of bushmeat (Prangé et al.
<xref ref-type="bibr" rid="CR197">2009</xref>
) and water/foodborne parasites such as
<italic>Giardia.</italic>
Recent studies have documented
<italic>Giardia</italic>
in a variety of species that exist in the bushmeat trade, including western gorilla and African buffalo (
<italic>Syncerus caffer</italic>
) (Hogan et al.
<xref ref-type="bibr" rid="CR94">2014</xref>
).</p>
</sec>
<sec id="Sec12">
<title>Fungi</title>
<p id="Par46">Fungi are increasingly beingrecognized as important pathogens that may emerge, even in humans (Jones et al.
<xref ref-type="bibr" rid="CR103">2008</xref>
; Fisher et al.
<xref ref-type="bibr" rid="CR69">2012</xref>
), and a number of fungi are considered medically important. In particular, fungal infections are problematic for people who are immunosuppressed (e.g., from HIV infection), in which case their immune systems are unable to adequately fight the infection. Nonetheless, we have uncovered no examples of EIDs in Africa caused by fungal pathogens not related to human immunosuppression, as even the 1950s outbreak of cryptococcal meningitis in the Democratic Republic of the Congo has been likely linked to co-infection by HIV (Molez
<xref ref-type="bibr" rid="CR160">1998</xref>
; Jones et al.
<xref ref-type="bibr" rid="CR103">2008</xref>
).</p>
</sec>
<sec id="Sec13">
<title>Prions</title>
<p id="Par47">Only 5 % of prion diseasesare acquired (as opposed to inherited), but these include the well-publicized outbreaks of scrapie, bovine spongiform encephalopathy (BSE, or “mad cow disease”), and chronic wasting disease (CWD) in ungulates from Europe and North America. Of these, only BSE has been detected in humans and in captive-held primates (Imran and Mahmood
<xref ref-type="bibr" rid="CR98">2011a</xref>
,
<xref ref-type="bibr" rid="CR99">b</xref>
; Bons et al.
<xref ref-type="bibr" rid="CR30">1999</xref>
; Lee et al.
<xref ref-type="bibr" rid="CR127">2013</xref>
), likely due to consumption of contaminated meat products. The authors have found no descriptions of infectious prion diseases in Africa, but this poorly studied pathogen type may well be present in the world’s second largest continent. As it relates to bushmeat-related practices, prions can be found in nearly all tissues and are resistant to degradation, even by cooking, rendering them a potential pathogen worth watching.</p>
</sec>
</sec>
<sec id="Sec14">
<title>Local Knowledge and Perception of Disease Risk</title>
<p id="Par48">The risk of disease spillover from bushmeat to hunters is highest during butchering and especially if no precautions are taken. Whether hunters take precautions may depend on their knowledge and perception of disease risk. There is increasing evidence that the perception of and knowledge about zoonotic diseases is generally low but varies strongly between sites. A survey among rural bushmeat hunters and traders in Sierra Leone showed that 24 % reported knowledge of disease transmission from animals to humans (Subramanian
<xref ref-type="bibr" rid="CR227">2012</xref>
). Similarly, 23 % of rural–urban hunters and traders in Ghana perceived a disease risk from a bat-bushmeat activity, with significantly more respondents associating risk with bat consumption than bat preparation or hunting (Kamins et al.
<xref ref-type="bibr" rid="CR107">2014</xref>
). Individuals who participate in butchering wild animals typically associate less risk to meat preparation and consumption than those who do not participate in butchering (Kamins et al.
<xref ref-type="bibr" rid="CR107">2014</xref>
) (Fig.
<xref rid="Fig2" ref-type="fig">24.2</xref>
). LeBreton et al. (
<xref ref-type="bibr" rid="CR124">2006</xref>
) found that hunters and butchers who perceived personal risks were significantly less likely to butcher wild animals, but that risk perception was not associated with hunting and eating bushmeat. Thirty-three percent of bushmeat consumers in a Ghanaian market were not aware that zoonotic diseases could be transmitted from bushmeat to humans. Those who were aware gave Ebola (48 %) and anthrax (16 %) as examples of zoonotic diseases (Kuukyi et al.
<xref ref-type="bibr" rid="CR117">2014</xref>
). In contrast, a large-scale survey among rural Central African population showed that the majority (74 %) of respondents perceived contact with bushmeat blood or body fluids as dangerous (LeBreton et al.
<xref ref-type="bibr" rid="CR124">2006</xref>
). Unfortunately, studies in this field can be challenging, as reported perceptions may differ from actual or ‘revealed’ behaviors and beliefs (Wilkie
<xref ref-type="bibr" rid="CR261">2006</xref>
).
<fig id="Fig2">
<label>Fig. 24.2</label>
<caption>
<p>A pangolinbeing prepared in rural Ghana; photo credit Laura Kurpiers</p>
</caption>
<graphic xlink:href="332204_1_En_24_Fig2_HTML" id="MO2"></graphic>
</fig>
</p>
<p id="Par49">Although there seems to be some level of risk awareness in certain human populations, several studies report a distinct lack of precautionary behavior, resulting in hunters, butchers, and consumers exposing themselves to zoonotic diseases. LeBreton et al. (
<xref ref-type="bibr" rid="CR124">2006</xref>
) found that only 4 % of hunters and 2 % of people reporting butchering indicated that they took precautions against contact with animal blood and fluids while hunting and butchering. Furthermore, the few that took precautions may not have protected themselves adequately, as the most common response was “generally being careful.” This was followed by “washing hands,” and the least number of participants reporting “avoiding contact with blood, draining blood from carcasses and wearing suitable clothing.” Paige et al. (
<xref ref-type="bibr" rid="CR180">2014</xref>
) examined human–animal interactions in western Uganda and found that nearly 20 % of participants reported either being injured by an animal or having contact with a primate. The most commonly reported animal injuries were bites (72.9 %) and scratches (23.2 %). In a separate study, it was also shown that although Ghanaian hunters generally handle live bats, they do not typically use protective measures such as gloves, and thereby come into contact with blood through scratches and bites (Kamins et al.
<xref ref-type="bibr" rid="CR107">2014</xref>
). Given the lack of awareness and precautionary measures taken among people who come into contact with bushmeat, the opportunity for new zoonotic pathogens to spillover into humans remains high (LeBreton et al.
<xref ref-type="bibr" rid="CR124">2006</xref>
). This is especially true, since the current rate of hunting wild animals will likely continue—at least until domestic animal production increases and cansupport the protein needs of the local people.</p>
</sec>
<sec id="Sec15">
<title>The Way Forward</title>
<p id="Par50">Current global disease control efforts focus almost exclusively on responding long after a spillover event has occurred, which increases the risk of a single spillover event causing an epidemic or pandemic. This retroactive response to emerging disease outbreaks is often costly economically and in terms of human well-being (Childs and Gordon
<xref ref-type="bibr" rid="CR44">2009</xref>
; United Nations Development Program
<xref ref-type="bibr" rid="CR245">2015</xref>
). Increased pre-spillover surveillance measures along with quantification of spillover risk is critically needed. For example, Wolfe et al. (
<xref ref-type="bibr" rid="CR268">2004b</xref>
,
<xref ref-type="bibr" rid="CR270">2005b</xref>
) found that 1 % of rural Cameroonians are infected with wild primate variants of T-lymphotropic viruses and another 1 % are infected with wild primate variants of simian foamy virus. These sorts of data are simply lacking for most emergent disease systems. Here we will discuss the regulatory and educational measures that could be taken to mitigate the risk of a zoonotic spillover event and spread. Such efforts should be undertaken as a part of a comprehensive response to other sub-Saharan public health crises so as to not divert scarce resources. For example, increases in EID surveillance efforts and in post-emergence management go hand in hand with the improved healthcare infrastructure that must become a priority for sub-Saharan Africa.</p>
<p id="Par51">At face value, the risk of disease transmission would be reduced if people stopped harvesting bushmeat; however, this scenario is not realistic given the importance of bushmeat in many communities in Africa for which there is limited affordable access to alternate protein sources (Pike et al.
<xref ref-type="bibr" rid="CR190">2010</xref>
; Gebreyes et al.
<xref ref-type="bibr" rid="CR74">2014</xref>
). A more practical option may be to restrict hunting of nonhuman primates, as many zoonotic EIDs have come from them, and instead allow communities to hunt smaller-bodied mammals with higher reproductive rates. Any intervention aiming to restrict access to wildlife should involve community leaders and stakeholders during public outreach to reduce the risk of alienating communities (Monroe and Willcox
<xref ref-type="bibr" rid="CR161">2006</xref>
). The education and enforcement necessary to implement such a restriction must consider the cultural and economic contexts surrounding individual communities. Consider, for example, the problems with enforcement of access restrictions and the history of antagonistic relationships due to exclusion from protected areas between conservationists and local communities. Without proper educational outreach, this could result in backlash from local communities. Furthermore, using zoonotic diseases to enforce hunting restrictions runs the risk of demonizing species considered to be the main disease carriers. Nonhuman primates could then become targets and their populations could be decimated (Pooley et al.
<xref ref-type="bibr" rid="CR192">2015</xref>
).</p>
<p id="Par52">A more realistic strategy may be toconcentrate on preventing future zoonotic spillover events through culturally appropriate education and preventing the spread of diseases through better disease surveillance. In that effort, it would also be important to incorporate collaborative and interdisciplinary approaches between veterinary researchers, ecologists, microbiologists, public health researchers, and anthropologists to develop surveillance and research approaches that will be both culturally appropriate and improve detection of zoonotic diseases tied to bushmeat hunting (Kilonzo et al.
<xref ref-type="bibr" rid="CR115">2014</xref>
).</p>
<sec id="Sec16">
<title>Education</title>
<p id="Par53">The risk of diseasetransmission could be reduced through community education that focuses on people with high levels of exposure to wild animals (Wolfe et al.
<xref ref-type="bibr" rid="CR271">2007</xref>
). Communicating with hunters and butchers about the risks associated with bushmeat and promoting awareness of safer techniques may reduce current levels of pathogen exposure and transmission. To enhance the effectiveness of prevention campaigns, it is particularly important to reinforce the potential for infections during hunting and butchering as this may be overlooked by some hunters (LeBreton et al.
<xref ref-type="bibr" rid="CR124">2006</xref>
). Because the risk perception of hunters and those engaging in butchering wild animals has a negative association with the level of participation in meat preparation and consumption (Kamins et al.
<xref ref-type="bibr" rid="CR107">2014</xref>
), this may reduce current levels of pathogen exposure and transmission, if not by discouraging individuals to participate in preparation and consumption, then by encouraging those individuals to more proactively consider safety and preventative measures.</p>
<p id="Par54">Global Viral Forecasting (GVF; now “Global Viral” and “Metabiota”) has been pivotal in educating vulnerable populations in rural central Africa by providing information on the risk of zoonotic disease transmission from hunting wild animals (LeBreton et al.
<xref ref-type="bibr" rid="CR125">2012</xref>
). Hunters are informed about disease risks associated with different species, what steps can be taken to avoid infections, and how they can reduce their contact with blood and body fluids of wild animals. Hunters are urged to redirect hunting efforts away from apes and monkeys and towards less risky species such as antelope and rodents, while also being discouraged from butchering animals when there are cuts or injuries on their hands and limbs.</p>
<p id="Par55">Of course, a common aspect of such attempts at social outreach and education is that even when it is possible to promote awareness, individuals may not believe the hazard is important or that it could affect them. Some authors have even found that when people do believe the risk is real and relevant, there is often little evidence that this knowledge promotes a change in behavior (McCaffrey
<xref ref-type="bibr" rid="CR149">2004</xref>
). For example, a pilot education program among Ghanaian hunters resulted in substantially improved understanding of disease risk, yet largely failed to change peoples’ behavior (Kamins et al.
<xref ref-type="bibr" rid="CR107">2014</xref>
). When asked about what would change their behavior, participants responded; becoming ill from zoonotic disease followed by alternative livelihoods and stricter laws. Because awareness is not directly related to behavior, Monroe and Willcox (
<xref ref-type="bibr" rid="CR161">2006</xref>
) suggest that campaigns should not rely on the threat of infection to change behavior, but should rather use community leaders to change cultural norms associated with hunting and educate people involved in butchering about best practices of how toprotect themselves.</p>
</sec>
<sec id="Sec17">
<title>Surveillance</title>
<p id="Par56">With the increasing prevalence of zoonotic disease emergence and the associated risk for public health, we have to improve our understanding of the dynamics of spillover events of pathogens from animal to human hosts (Rostal et al.
<xref ref-type="bibr" rid="CR202">2012</xref>
) and improve systematic global monitoring efforts. This could help detect, define, and control local human emergence while it is still locally confined and before it has a chance to spread globally. Improved detection and surveillance will lead to a better prioritization of public health efforts. One of the most effective strategies in terms of early detection of an emergent pathogenic threat would be to focus surveillance efforts among people who are highly exposed to at-risk animals and on the animal populations to which they are exposed (LeBreton et al.
<xref ref-type="bibr" rid="CR125">2012</xref>
). Bushmeat hunters would be an important target group, as they are in contact with bodily fluids from animals and are at risk for transmission and infection from novel pathogens.</p>
<p id="Par57">As an example, GVF has established monitoring programs at multiple sites throughout Central Africa to detect the moment of a pathogen spillover, which can then be used to predict and ultimately prevent zoonotic disease emergences (Evans and Wolfe
<xref ref-type="bibr" rid="CR63">2013</xref>
). In order to track and provide data for EIDs, this effort coordinates the collection of filter-paper blood samples from both hunted animals and people who hunt and butcher wild animals. Early results have shown that this type of surveillance can assist in early detection of new diseases by offering insight into pathogen origin. It would also help describe the spillover dynamics of new or existing diseases. Such data are valuable for developing a detailed, mechanistic understanding of the processes that drive disease emergence and prevent spillovers from spreading in early stages of an outbreak. Contextualizing the relative or actual risks of spillovers would be vital for the preferential allocation of resources to high-risk regions or humans who perform high-risk activities (Daszak et al.
<xref ref-type="bibr" rid="CR51">2007</xref>
). As part of these efforts, improved knowledge of how anthropogenic environmental changes and sociological or demographic factors affect the risk of disease emergence will likely be a cost-effective and sustainablemechanism to reduce or control disease spillover risks (Daszak et al.
<xref ref-type="bibr" rid="CR51">2007</xref>
).</p>
</sec>
<sec id="Sec18">
<title>Call for Research</title>
<p id="Par58">The social and environmentalissues surrounding bushmeat represent a complex problem for conservation, global public health, and sustainable development, as it is often the poorest and most vulnerable populations who depend on bushmeat for income or food security. Accordingly, the challenge should be addressed in a holistic manner, by integrating multiple efforts to achieve common objectives. Although much progress has been made not only in addressing the problems concerning bushmeat harvest and zoonotic disease spillover, there is much work to be done. Research that would pave the way for future efforts would include the quantification of social response to environmental policy change (e.g., in the context of harvest restriction), development of a more representative picture of bushmeat consumption in Africa, a broader exploration of the many classes of pathogens within wildlife, and more thorough understanding and quantification of the dynamics behind spillover events and the risks to humans. Such efforts could facilitate the development of policy and infrastructure that would help curb the dependency on bushmeat, reduce risks associated with bushmeat harvest, and help understand in what circumstances zoonotic disease spillover events occur.</p>
<p id="Par59">There is still uncertainty as to how education should be implemented in different regions and what features of such education would be most valuable for local people. Such an effort might consist of surveying rural bushmeat-harvesting populations across Africa and using the resulting data to contextualize priorities and goals in a way that could help standardize education approaches. While some locations in Africa have had extensive research in the scope and impact of bushmeat harvest, much of Africa has been neglected in those efforts. A more developed understanding of the location, scale, and structure of bushmeat harvest throughout the continent would help researchers and policy-makers prioritize efforts related to disease surveillance, education, or aid. The study of zoonotic spillover events related to viruses, while not completely developed, has received far more attention than the related fields of spillover from bacterial or other non-virus pathogens. There is significant interest in pursuing these lines, as they represent an underdeveloped bodyof knowledge that could have significant impacts related to human health and disease ecology.</p>
</sec>
</sec>
</body>
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<name>
<surname>Diffo Jle</surname>
<given-names>D</given-names>
</name>
<etal></etal>
</person-group>
<article-title>Emergence of a novel and highly divergent HTLV-3 in a primate hunter in Cameroon</article-title>
<source>Virology</source>
<year>2010</year>
<volume>401</volume>
<fpage>137</fpage>
<lpage>145</lpage>
<pub-id pub-id-type="doi">10.1016/j.virol.2010.03.010</pub-id>
<pub-id pub-id-type="pmid">20353873</pub-id>
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