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Bushmeat and Emerging Infectious Diseases: Lessons from Africa

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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.
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507© Springer International Publishing Switzerland 2016
F.M. Angelici (ed.), Problematic Wildlife, DOI 10.1007/978-3-319-22246-2_24
Chapter 24
Bushmeat and Emerging Infectious Diseases:
Lessons from Africa
Laura A. Kurpiers , Björn Schulte-Herbrüggen , Imran Ejotre ,
and DeeAnn M. Reeder
Introduction
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 1954 ; Hays 2005 ; Steverding 2008 ), whereas
others, such as Ebola virus, Nipah virus, and SARS, emerged more recently (World
Health Organization 1978 ; Chua et al. 2000 ; Guan et al. 2003 ). 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. 2003 ; Jones et al. 2008 ).
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. 2001 ;
Jones et al. 2008 ; Karesh and Noble 2009 ). Although many zoonotic pathogen spill-
overs arise in domestic animals, including livestock, the majority (71.8 %) of zoo-
notic EIDs arise from wildlife species (Jones et al. 2008 ). 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 Pteropus ying foxes are the reservoir host and domestic pigs or horses are
L. A. Kurpiers I. Ejotre D. M. Reeder (*)
Department of Biology , Bucknell University , Lewisburg , PA 17837 , USA
e-mail: Laura.Kurpiers@bucknell.edu; Imran.Ejotre@bucknell.edu;
DeeAnn.Reeder@bucknell.edu
B. Schulte-Herbrüggen
Stockholm Resilience Centre , Stockholm University , 10691 Stockholm , Sweden
e-mail: bjorn.schulte-herbruggen@su.se
508
amplifi er hosts from which spillovers to humans have been documented (Childs et al.
2007 ; Daszak et al. 2007 ). Not surprisingly, the most devastating pandemics in
human history, the Black Death, Spanish infl uenza, and HIV/AIDS, were all caused
by zoonoses from wildlife (Morens et al. 2008 ).
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 fl uids,
tissues, and excrement (Wolfe et al. 2005a ). 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 transmis-
sible between humans (Taylor et al. 2001 ). Of all EIDs, zoonotic spillovers from
wildlife have been identifi ed as the most signifi cant, growing threat to global health
(Cleaveland et al. 2007 ; Jones et al. 2008 ).
Recent evidence highlights the link between infectious diseases and biodiversity
loss, land use changes, and habitat fragmentation (Cleaveland et al. 2007 ; Maganga
et al. 2014 ; Gottdenker et al. 2014 ). Although additional research on the relation-
ship between habitat degradation and EIDs is needed, Gottdenker et al. ( 2014 )
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 infl uencing disease spillover include
disruption of food web structures, changes in host–pathogen interactions, and mix-
ing of pathogen gene pools resulting in increased pathogen genetic diversity (Jones
et al. 2013 ). 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. 2003 ; Gillespie et al. 2005 ; Keesing et al. 2006 ;
Salzer et al. 2007 ; Cottontail et al. 2009 ; Young et al. 2014 ). Specifi cally, the emer-
gence or re-emergence of many zoonotic diseases including yellow fever, Lyme
disease, hantavirus pulmonary syndrome, Nipah virus encephalitis, infl uenza,
rabies, malaria, and human African trypanosomiasis have been linked to anthropo-
genic habitat changes (Jones et al. 2013 ).
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. 2004a ), HIV (Van Heuverswyn and
Peeters 2007 ), and monkeypox (Rimoin et al. 2010 ). Pathogen spillover from bush-
meat can occur through consumption; however, the main risks are associated with
exposure to body fl uids and feces during handling and butchering (Kilonzo et al.
2014 ; Paige et al. 2014 ). 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
L.A. Kurpiers et al.
509
across the globe (LeBreton et al. 2006 ). EIDs cause hundreds of thousands of deaths
annually (Bogich et al. 2012 ). 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.
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. 2008 ). The recent Ebola outbreaks have high-
lighted 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.
Bushmeat
The term “bushmeat” refers to the meat derived from wild animals for human con-
sumption (Milner-Gulland and Bennett 2003 ) (Fig. 24.1 ). It includes a wide range
of animals, such as invertebrates, amphibians, insects, fi sh, reptiles, birds, and
mammals, including as many as 500 species in sub-Saharan Africa (Ape Alliance
2006 ). 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. 2000 ; Karesh and Noble 2009 ). 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 fl uids (LeBreton et al.
2006 ). 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. 2006 ) and butchering involves the use of sharp tools, which may
lead to cuts during the process. Subramanian ( 2012 ) 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 prepara-
tion than men. In discussing the links between bushmeat and disease, we refer to
this all-encompassing suite of risky behaviors as “bushmeat-related activities.”
Nonhuman primates, rodents, and bats have all been linked to the spillover of
zoonotic diseases into humans (Cleaveland et al.
2007 ; Jones et al. 2008 ; Kilonzo
24 Bushmeat and Emerging Infectious Diseases: Lessons from Africa
510
et al. 2014 ). 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. 2015 ). Among mammals, the largest group was primates (48 species)
including western gorillas ( Gorilla gorilla ), bonobos ( Pan paniscus ), and common
chimpanzees ( Pan troglodytes ), 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. ( 2015 ) study is
very comprehensive, it only included studies that: (1) provided a quantitative mea-
sure 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) identifi ed carcasses to the species level; and (4)
recorded either the number of carcasses or the total biomass (kg). For a more inclu-
sive and general review of existing Central African bushmeat studies, see Wilkie
and Carpenter ( 1999 ), and for West African studies, see Schulte-Herbrüggen ( 2011 ).
Fa et al. ( 2006 ) 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 hunt-
ers’ offtake (Bowen-Jones et al. 2003 ; Schulte-Herbrüggen et al. 2013a ).
Fig. 24.1 Bushmeat being
smoked in rural South
Sudan; photo credit Adrian
Garside
L.A. Kurpiers et al.
511
Livelihood Importance
Humans have hunted wild animals for consumption and to protect their crops for
millennia (Shipman et al. 1981 ; Grubb et al. 1998 ; Davies et al. 2007 ), and it remains
an important source of food and income security among rural communities today
(de Merode et al. 2004 ; Brashares et al. 2011 ). 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. 2003 ). 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.
2011 ). 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 2004 ). Similarly, for
rural Equatorial Guinea, Allebone-Webb ( 2008 ) showed that bushmeat consump-
tion 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 1999 ). 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 1989 ,
de Merode et al. 2004 , Schulte-Herbrüggen et al. 2013b ) and during the dry season
when fi sh is not available (Poulsen et al. 2009 ). 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. 2011 ).
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 indi-
vidual hunting households, ranging from 38 % to more than 90 % of the total cash
income earned (reviewed in Schulte-Herbrüggen 2011 ). In rural Gabon, hunting
accounts for up to 72 % of household incomes, with the proportion rising in
poorer, more remote communities (Starkey 2004 ). 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 2008 ). 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. 2004 ).
Overall, income from bushmeat sales can be lucrative and compare favorably with
alternative work in many rural places. Vega et al. ( 2013 ) found that commercial hunt-
ers in Equatorial Guinea generated a mean of US$2000 per year from bushmeat sales.
24 Bushmeat and Emerging Infectious Diseases: Lessons from Africa
512
Hunters supplying markets in Central African logging concessions earned twice the
income of junior technicians working at a logging company (Tieguhong and Zwolinski
2009 ). Rural Kenya hunters can earn 2.5 times the average salary in the area (Fitzgibbon
et al. 1995 ), 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 1998 ). Very successful Zambian hunters have been reported earning
just below the mean annual income in a single hunting trip (Brown 2007 ).
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 com-
munities 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 net-
works and air travel increases the risk of disease transmission worldwide (Brashares
et al. 2011 ). 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 com-
modity chain supplying bushmeat to an urban market in Ghana includes hunters,
wholesalers, market traders, restaurant owners, and consumers (Mendelson et al.
2003 ). 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 own-
ers who sell the bushmeat to consumers (de Merode and Cowlishaw 2006 ). 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 ven-
dors (Kamins et al. 2011a ). In Zambia, Mozambique, and Malawi, well-developed
and complex rural-urban trade supply networks link rural hunters to urban consum-
ers who are willing to pay high prices for bushmeat (Barnett 1997 ). Understanding
commodity chains is important, as pathogens likely remain viable for some period
after an animal is killed. For example, Prescott et al. ( 2015 ) demonstrated that Ebola
virus remains viable on monkey carcasses for at least seven days, with viral RNA
detectable for 10 weeks.
Scale of Bushmeat Harvest in Sub-Saharan Africa
Bushmeat has become a multi-million dollar business due to a growing human pop-
ulation 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. 2006 ), 120,000 tones per year in Côte d’Ivoire
(Caspary 1999 ), 385,000 tons per year in Ghana (Ntiamoa-Baidu 1998 ), and at total
of 1–4.9 million tons per year in Central African forests (Wilkie and Carpenter
1999 ; Fa et al. 2002 ).
However, it is important to recognize that our understanding of the scale of bush-
meat harvest is limited by the availability of information and hence current regional
L.A. Kurpiers et al.
513
harvest estimates might underestimate actual harvest volumes. Despite substantial
effort in recent years, our knowledge is still site-specifi c 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. 2015 ). A large number of sites with
detailed bushmeat data are concentrated in the Cross-Sanaga region of Nigeria and
Cameroon, where Fa et al. ( 2006 ) 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) identifi ed by Taylor et al. ( 2015 ) come from market surveys with
poorly defi ned catchment areas, compared to offtake and consumption surveys.
Strong variation between individual estimates highlights the problems with extrapo-
lation of survey data to national or regional levels and the effects of sampling strate-
gies (hunter versus market surveys), timing of survey (open season versus lean
season), survey location, and extrapolation methods. Individual fi gures 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.
Drivers of Increased Bushmeat Hunting and Disease Risks
The current scale of bushmeat hunting is primarily the result of socio-demographic
changes (Wilkie and Carpenter 1999 ). 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 2013 ). Where alternative sources of animal protein and income are
scarce, human population growth has been linked to increasing hunting intensity
(Brashares et al. 2001 ).
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. 2009 ). While urban consumers generally consume less
bushmeat than rural consumers (Brashares et al. 2011 ), urban populations in Africa
have increased dramatically from about 15 % of the total population in 1950 to 40 %
in 2014 (United Nations 2014 ) and have created a strong demand for bushmeat and
hence market for rural hunters.
The increasing demand for bushmeat has been accompanied by changes in hunting
technology and improvements in hunting effi ciency. 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 tradi-
tional weapons (Wilkie and Curran
1991 ), substantially increasing the ease and
cost-effectiveness of hunting (Alvard 1995 ). This enables hunters to catch more
24 Bushmeat and Emerging Infectious Diseases: Lessons from Africa
514
animals and sell a larger part of their catch (Bowen-Jones and Pendry 1999 ;
Bowen- Jones et al. 2003 ; Nasi et al. 2008 ).
Hunting effi ciency has also improved as remote forests have become more acces-
sible through the construction of logging roads and improved transportation (Wilkie
et al. 1992 ; Auzel and Wilkie 2000 ). 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. 2001 ). Development of rural businesses , such as
timber companies, attracts workers and their families to remote locations, increas-
ing bushmeat demand, especially when no hunting regulations are in place and
alternative protein sources are not provided (Auzel and Wilkie 2000 ; Bennett and
Gumal 2001 ; Poulsen et al. 2009 ). The effect of logging company presence on hunt-
ing pressure was documented in Gabon where ape populations decreased 50 %
between 1983 and 2000 as a result of hunting (Walsh et al. 2003 ). In addition, agri-
cultural expansion and mining have exerted a strong force in changing the African
landscape and infl uencing human migration patterns (Norris et al. 2010 ). Due to
increased access, people are brought into closer contact with wildlife, which facili-
tates accessibility to bushmeat hunting and makes transportation of bushmeat from
rural to urban areas easier and more cost-effective (Wolfe et al. 2005a ).
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 2014 ). Case studies at airports screening
passenger luggage for bushmeat estimated that approximately 5 tons of bushmeat per
week arrive at Paris Roissy-Charles de Gaulle airport (Chaber et al. 2010 ) and 8.6 tons
per year at Zurich and Geneva airports (Falk et al. 2013 ). As bushmeat hunting, global-
ization, 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 con-
scated primates at US airports (Smith et al. 2012 ).
Bushmeat as a Source of Zoonotic Diseases in Sub-Saharan
Africa
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
classifi ed as very likely to spillover (Jones et al. 2008 ; Kilonzo et al. 2014 ).
Furthermore, countless pathogen species of zoonotic potential will likely be discovered
as surveillance increases (Taylor et al.
2001 ; Jones et al. 2008 ). Our close phyloge-
netic relationship with nonhuman primates increases the likelihood that pathogen
spillover from these animals to humans will cause infection (Childs et al. 2007 ).
L.A. Kurpiers et al.
515
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 diur-
nal mammals in the bushmeat trade (Taylor et al. 2015 ). 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. 2013 ), and
members of these subfamilies share many morphological, physiological, and eco-
logical features that may have a direct role in the transmission of infectious diseases
(Davies and Pedersen 2008 ). Cleaveland et al. ( 2007 ), 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 patho-
gens in African birds is strongly needed (e.g., for avian infl uenza tracking see
Simulundu et al. 2011 , 2014 ).
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 1995 ). Taste preferences for certain species infl uence hunters’ deci-
sions 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 1995 ). 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. 2009 ). Increased human encroachment in recent decades (Kamins et al. 2011b )
has driven some bat species to become peridomestic (O’Shea et al. 2011 ; Plowright
et al. 2011 ), which renders them easy targets for hunting. Finally, sick animals may
be less successful in evading hunters and hence more easily hunted, thereby increas-
ing the risk of disease transmission to hunters.
In addition to the behavioral traits that may infl uence which species are hunted,
physiological traits of these species may make them more likely to harbor and trans-
mit diseases. For example, bats, which are present in the bushmeat trade and com-
prise the highest risk among all wildlife for harboring emerging diseases (Cleaveland
et al. 2007 ), present unique traits that suit them to hosting pathogens. These traits
include: (1) relatively long lifespans for their body size (Munshi-South and
Wilkinson 2010 ), which may facilitate pathogen persistence for chronic infections;
(2) fl ight, which allows movement and dispersal over long distances and which cre-
ates 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. 2014 ); (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. 2010 ); 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.
2013 ).
24 Bushmeat and Emerging Infectious Diseases: Lessons from Africa
516
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. 2007 ). That said, when spillover events do
occur, they can be not only deadly but costly. For example, the United Nations
Development Program ( 2015 ) 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 out-
break. 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.
To understand the dynamics of spillover events and risks in relation to the patho-
gen, 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 signifi cant
disease in that host, and (6) whether morbidity and/or mortality levels in the second-
ary host are suffi cient to be considered signifi cant (Childs et al. 2007 ). 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. 2007 ; Etienne
et al. 2013 ). Generalist pathogens have the ability to infect more than one host spe-
cies and have higher relative emergence risk than pathogens that are very host-
specifi c (Cleaveland et al. 2007 ); 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. 2014 ).
Of particular importance for understanding bushmeat-related spillover events is
whether a wildlife species is a natural or incidental pathogen host. Natural or reser-
voir hosts are a natural part of the pathogen life cycle and may maintain the infec-
tious 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. 2004b ). 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 fi lovirus, under-
standing what species are true reservoirs (likely fruit bats in the family Pteropodidae;
Pourrut et al. 2007 , 2009 ; Hayman et al. 2010 , 2012 ) and the spillover events
between these reservoirs and other mammals (including apes, carnivores, and ungu-
lates; Leroy et al. 2004a ) will prove critical to mitigating the components of disease
transmission that are due to bushmeat-related activities. Unfortunately, it is often
diffi cult to defi nitively 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-specifi c nucleic acid sequences from
L.A. Kurpiers et al.
517
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 2012 ; Viana et al. 2014 ).
Descriptions of the types of pathogens potentially encountered through bushmeat-
related activities can be found below, with several important and well-studied exam-
ples 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. ( 2008 ) report that the vast majority of pathogens involved in EIDs are
bacterial or rickettsial, followed by viral or prion, then protozoa, fungi, and hel-
minths. Other studies have ranked viruses as more prevalent (Taylor et al. 2001 ;
Woolhouse et al. 2005 ; Cleaveland et al. 2007 ). In Jones et al.’s ( 2008 ) analysis of
335 EID events between 1940 and 2004, only four EIDs list bushmeat as the driver;
other signifi cant drivers were socioeconomic factors such as human population
density. These four bushmeat-related EID events were all signifi cant events; all due
to viruses (Ebolavirus, human immunodefi ciency virus-1, monkeypox virus, and
SARS), suggesting that viruses are the most important pathogens in regard to spill-
over due to bushmeat-related activities (see also Kilonzo et al. 2014 ). 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 signifi cant
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 ( 2011 ) comprehensive study of zoonot-
ics in Namibia is an exception.
Overview of Pathogens Related to Bushmeat Activities
Table 24.1 summarizes these pathogens by bushmeat host taxonomic group, conser-
vatively 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 diffi cult to establish. Thus, Table 24.1
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 bush-
meat 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.
24 Bushmeat and Emerging Infectious Diseases: Lessons from Africa
518
Table 24.1 Bushmeat species and zoonotic pathogens for which strong evidence for spillovers via bushmeat-related activities exists (see criteria for inclusion
in text)
Bushmeat species Pathogen Location References
Great Apes (Chimpanzee, Bonobo, Gorilla)
a
Pan troglodytes
(Common chimpanzee) Zaire Ebolavirus (V) Cameroon, Gabon, Republic of
Congo Leroy et al. (
2004a , b )
Tai Forest Ebolavirus (V) Côte d’Ivoire Le Guenno et al. (
1995 ), Wyers et al. ( 1999 )
HIV-1/SIVcpz (V) Cameroon, Democratic Republic of
the Congo, Tanzania Santiago et al. (
2002 ), Worobey et al. ( 2004 ), Van
Heuverswyn et al. (
2007 )
HLTV/SLTV-1 (V) Central & Eastern Africa Gao et al. ( 1999 ), reviewed in Sharp and Hahn ( 2010 ),
Peeters et al. (
2013 )
Simian Foamy Virus (V) Cameroon, Côte d’Ivoire, Gabon,
Republic of Congo, Tanzania Calattini et al. (
2006 ), Liu et al. ( 2008 )
Strongyloides fulleborni (H) Gabon Mouinga-Ondémé et al. (
2012 )
Entamoeba histolytica (P) Tanzania Gillespie et al. (
2010 )
Balantidium coli (P) Central African Republic, Tanzania Lilly et al. ( 2002 ), Gillespie et al. ( 2010 )
Giardia intestinalis (P) Guinea Bissau Sak et al. (
2013 )
Bacillus anthracis (B) Côte d’Ivoire Leendertz et al. ( 2004 )
Pan paniscus (Bonobo) HTLV/STLV-2, HTLV/
STLV-3 (V) Democratic Republic of the Congo Ahuka-Mundeke et al. (
2011 ), Van Brussel et al.
(
1998 )
Gorilla gorilla (Western
gorilla) Zaire Ebolavirus (V) Cameroon, Gabon Leroy et al. (
2004a , b )
HIV-1/SIVgor (V) Cameroon Takehisa et al. (
2009 )
HTLV/STLV-1 (V) Cameroon Courgnaud et al. (
2004 ), Nerrienet et al. ( 2004 )
Simian Foamy Virus (V) Cameroon, Gabon Wolfe et al. (
2004b ), Mouinga-Ondémé et al. ( 2012 )
Rabies (V) Central African Republic, Kenya Karugah (
1997 )
Strongyloides fulleborni (H) Central African Republic Lilly et al. (
2002 )
Entamoeba histolytica (P) Central African Republic Lilly et al. ( 2002 )
Balantidium coli (P) Central African Republic Lilly et al. (
2002 )
Giardia intestinalis (P) Central African Republic, Rwanda Sak et al. ( 2013 ), Hogan et al. ( 2014 )
L.A. Kurpiers et al.
519
(continued)
Bushmeat species Pathogen Location References
Other nonhuman primates
Colobus angolensis
(Angola colobus) HTLV/STLV-3 (V) Democratic Republic of the Congo Ahuka-Mundeke et al. (
2012 )
Strongyloides fulleborni (H) Uganda Gillespie et al. (
2005 )
Entamoeba histolytica (P) Uganda Gillespie et al. (
2005 )
Colobus guereza
(Mantled guereza) Strongyloides fulleborni (H) Cameroon, Uganda Gillespie et al. (
2005 ), Pourrut et al. ( 2011 )
Entamoeba histolytica (P) Uganda Gillespie et al. (
2005 )
Piliocolobus badius
(Western red colobus) HTLV/STLV-1 (V) Côte d’Ivoire Leendertz et al. (
2010 )
Piliocolobus
tephrosceles (Ugandan
red colobus)
HTLV/STLV-1 (V) Uganda Goldberg et al. (
2009 )
Strongyloides fulleborni (H) Uganda Gillespie et al. (
2005 )
Entamoeba histolytica (P) Uganda Gillespie et al. (
2005 )
Piliocolobus tholloni
(Thollon’s red colobus) HTLV/STLV-1, HTLV/
STLV-3 (V) Democratic Republic of the Congo Ahuka-Mundeke et al. (
2012 ).
Lophocebus albigena
(Gray- cheeked
mangabey)
HTLV/STLV-1, HTLV/
STLV-3 (V) Cameroon Liégeois et al. (
2012 ), Locatelli and Peeters ( 2012 )
Strongyloides fulleborni (H) Cameroon Pourrut et al. (
2011 )
Lophocebus aterrimus
(Black crested
mangabey)
HTLV/STLV-3 (V) Democratic Republic of the Congo Ahuka-Mundeke et al. (
2012 )
Papio anubis (Olive
baboon) Zaire Ebolavirus (V) Cameroon Leroy et al. (
2004b )
HTLV/STLV-1 (V) Ethiopia, Kenya Mahieux et al. (
1998 ), Meertens et al. ( 2001 ),
Takemura et al. (
2002 ), Locatelli and Peeters ( 2012 )
Papio cynocephalus
(Yellow baboon) HTLV/STLV-3 (V) Tanzania Voevodin et al. (
1997 )
Papio hamadryas
(Hamadryas baboon) HTLV/STLV-3 (V) Eritrea, Ethiopia, Senegal Goubau et al. (
1994 ), Takemura et al. ( 2002 ),
Meertens and Gessain (
2003 )
Papio ursinus (Chacma
baboon) HTLV/STLV-1 (V) South Africa Mahieux et al. (
1998 )
Bacillus anthracis (B) Namibia Magwedere et al. (
2012 )
24 Bushmeat and Emerging Infectious Diseases: Lessons from Africa
520
Table 24.1 (continued)
Bushmeat species Pathogen Location References
Papio sp. (Baboon sp.) Rabies (V) Kenya, Namibia, Zambia Munang’andu (
1995 ), Karugah ( 1997 ), Magwedere
et al. (
2012 )
Theropithecus gelada
(Gelada) HTLV/STLV-3 (V) Ethiopia Van Dooren et al. (
2004 )
Cercocebus agilis (Agile
mangabey) HTLV/STLV-1, HTLV/
STLV-3 (V) Cameroon Nerrienet et al. (
2001 ), Courgnaud et al. ( 2004 ),
Liégeois et al. (
2008 ), Sintasath et al. ( 2009a ),
Locatelli and Peeters (
2012 )
Strongyloides fulleborni (H) Cameroon Pourrut et al. (
2011 )
Entamoeba histolytica (P) Central African Republic Lilly et al. (
2002 )
Balantidium coli (P) Central African Republic Lilly et al. ( 2002 )
Cercocebus atys (Sooty
mangabey) HIV-2/SIVsm (V) West Africa Hirsch et al. (
1989 ), reviewed in Sharp and Hahn
(
2010 ), Peeters et al. ( 2013 )
HTLV/STLV-1 (V) Sierra Leone Traina-Dorge et al. ( 2005 )
Cercocebus torquatus
(Collared mangabey) HTLV/STLV-1, HTLV/
STLV-3 (V) Cameroon Meertens et al. (
2001 , 2002 ), Liégeois et al. ( 2008 ,
2012 )
Mandrillus leucophaeus
(Drill) Zaire Ebolavirus (V) Cameroon Leroy et al. (
2004b )
Mandrillus sphinx
(Mandrill) Zaire Ebolavirus (V) Cameroon Leroy et al. ( 2004b )
HTLV/STLV-1 (V) Cameroon Nerrienet et al. (
2001 ), Courgnaud et al. ( 2004 ),
Liégeois et al. (
2012 )
Simian foamy virus (V) Cameroon, Gabon Wolfe et al. (
2004b ), Mouinga-Ondémé et al. ( 2010 )
Allenopithecus
nigroviridis (Allen’s
swamp monkey)
HTLV/STLV-1 (V) Democratic Republic of the Congo Meertens et al. (
2001 )
Miopithecus ogouensis
(Gabon talapoin) HTLV/STLV-1 (V) Cameroon Courgnaud et al. ( 2004 )
Strongyloides fulleborni (H) Cameroon Pourrut et al. (
2011 )
L.A. Kurpiers et al.
521
Bushmeat species Pathogen Location References
Erythrocebus patas
(Patas monkey) HTLV/STLV-1 (V) Cameroon, Central African Republic,
Senegal Ishikawa et al. ( 1987 ), Saksena et al. ( 1994 )
Chlorocebus aethiops
(Grivet) Marburg virus (V) Uganda Smith ( 1982 )
HTLV/STLV-1 (V) Ethiopia, Senegal Meertens et al. (
2001 ), Takemura et al. ( 2002 )
Chlorocebus pygerythrus
(Vervet monkey) HTLV/STLV-1 (V) Kenya Meertens et al. (
2001 )
Leptospira (B) Botswana Jobbins and Alexander ( 2015 )
Chlorocebus sabaeus
(Green monkey) HTLV/STLV-1 (V) Senegal Meertens et al. ( 2001 ), Locatelli and Peeters ( 2012 )
Chlorocebus tantalus
(Tantalus monkey) HTLV/STLV-1 (V) Kenya Meertens et al. (
2001 ), Locatelli and Peeters ( 2012 )
Cercopithecus
albogularis (Sykes’
monkey)
HTLV/STLV-1 (V) Kenya Mwenda et al. (
1999 )
Cercopithecus ascanius
(Red- tailed monkey) HTLV/STLV-1 (V) Democratic Republic of the Congo Ahuka-Mundeke et al. (
2012 )
Strongyloides fulleborni (H) Uganda Gillespie et al.( 2004 )
Cercopithecus cephus
(Moustached guenon) HTLV/STLV-1, HTLV/
STLV-3 (V) Cameroon Courgnaud et al. (
2004 ), Liégeois et al. ( 2008 , 2012 ),
Locatelli and Peeters (
2012 )
Strongyloidesfulleborni (H) Cameroon Pourrut et al. ( 2011 )
Cercopithecus lhoesti
(L’Hoest’s monkey) Strongyloides fulleborni (H) Uganda Gillespie et al. (
2004 )
Cercopithecus mitis
(Blue monkey) Strongyloides fulleborni (H) Kenya, Uganda Munene et al. (
1998 ), Gillespie et al. ( 2004 )
Cercopithecus mona
(Mona monkey) HTLV/STLV-1, HTLV/
STLV-3 (V) Cameroon Meertens et al. (
2001 ), Sintasath et al. ( 2009b ),
Locatelli and Peeters (
2012 )
Strongyloides fulleborni (H) Cameroon Pourrut et al. (
2011 )
Cercopithecus neglectus
(De Brazza’s monkey) Zaire Ebolavirus (V) Cameroon Leroy et al. (
2004b )
HTLV/STLV-1 (V) Democratic Republic of the Congo Ahuka-Mundeke et al. (
2012 )
Simian Foamy Virus (V) Cameroon Wolfe et al. ( 2004b )
Strongyloides fulleborni (H) Cameroon Pourrut et al. (
2011 ) (continued)
24 Bushmeat and Emerging Infectious Diseases: Lessons from Africa
522
Table 24.1 (continued)
Bushmeat species Pathogen Location References
Cercopithecus nictitans
(Greater spot-nosed
monkey)
HTLV/STLV-1, HTLV/
STLV-3 (V) Cameroon Meertens et al. (
2001 ), Courgnaud et al. ( 2004 ),
Liégeois et al. (
2008 , 2012 ), Sintasath et al. ( 2009b )
Strongyloides fulleborni (H) Cameroon Pourrut et al. ( 2011 )
Cercopithecus pogonias
(Crested mona monkey) HTLV/STLV-1 (V) Cameroon Courgnaud et al. (
2004 ), Liégeois et al. ( 2008 )
Strongyloides fulleborni (H) Cameroon Pourrut et al. (
2011 )
Cercopithecus wolfi
(Wolf’s mona monkey) HTLV/STLV-1 (V) Democratic Republic of the Congo Locatelli and Peeters (
2012 )
“Vervet monkey” Rabies (V) Zambia Munang’andu ( 1995 )
Strongyloides fulleborni (H) Uganda Gillespie et al. (
2004 )
Unspecifi ed primate sp. Rabies (V) Ethiopia, Ghana, Kenya, Malawi,
Mozambique; Namibia, Sudan,
Uganda, Zimbabwe
See summary and discussion in Gautret et al. (
2014 )
Bats
Eidolon helvum (African
straw- colored fruit bat) Zaire Ebolavirus (V) Ghana Hayman et al. ( 2010 )
Lagos bat virus (V) Ghana, Kenya, Nigeria, Senegal Boulger and Porterfi eld (
1958 ), Institut Pasteur ( 1985 ),
Hayman et al. (
2008 , 2010 ), Kuzmin et al. ( 2008 )
Henipaviruses (V) Cameroon, Ghana, Republic of
Congo, Zambia Hayman et al. (
2008 ), Drexler et al. ( 2009 ), Baker
et al. (
2012 ), Weiss et al. ( 2012 ), Muleya et al. ( 2014 ),
Pernet et al. (
2014 )
Hypsignathus
monstrosus (Hammer-
headed fruit bat)
Marburgvirus (V) Gabon, Republic of Congo Pourrut et al. (
2009 )
Zaire Ebolavirus (V) Ghana, Gabon, Republic of Congo Pourrut et al. (
2007 , 2009 ), Hayman et al. ( 2012 )
Epomops franqueti
(Franquet’s epauletted
fruit bat)
Marburgvirus (V) Gabon, Republic of Congo Pourrut et al. (
2009 )
Zaire Ebolavirus (V) Ghana, Gabon, Republic of Congo Pourrut et al. (
2007 , 2009 ), Hayman et al. ( 2012 )
Epomophorus
gambianus (Gambian
epauletted fruit bat)
Zaire Ebolavirus (V) Ghana Hayman et al. ( 2012 )
L.A. Kurpiers et al.
523
Bushmeat species Pathogen Location References
Epomophorus wahlbergi
(Wahlberg’s epauletted
fruit bat)
Lagos Bat Virus (V) South Africa Markotter et al. (
2006 )
Micropteropus pusillus
(Peters’s lesser
epauletted fruit bat)
Marburgvirus (V) Gabon, Republic of Congo Pourrut et al. (
2009 )
Zaire Ebolavirus (V) Gabon, Republic of Congo Pourrut et al. (
2009 )
Lagos Bat Virus (V) Central African Republic Sureau et al. ( 1980 )
Rousettus aegyptiacus
(Egyptian rousette) Marburgvirus (V) Democratic Republic of the Congo,
Gabon, Kenya, Republic of Congo,
Uganda
Swanepoel et al. (
2007 ), Towner et al. ( 2007 , 2009 ),
Pourrut et al. (
2009 ), Kuzmin et al. ( 2010b ), Amman
et al. (
2012 )
Zaire Ebolavirus (V) Gabon, Republic of Congo Pourrut et al. (
2009 )
Lagos Bat Virus (V) Kenya Kuzmin et al. (
2008 )
Myonycteris torquata
(Little collared fruit bat) Zaire Ebolavirus (V) Gabon, Republic of Congo Pourrut et al. (
2007 , 2009 )
Nanonycteris veldkampii
(Veldkamp’s dwarf
epauletted fruit bat)
Zaire Ebolavirus (V) Ghana Hayman et al. ( 2012 )
Rhinolophus eloquens
(Eloquent horseshoe bat) Marburgvirus (V) Democratic Republic of the Congo Swanepoel et al. (
2007 )
Miniopterus infl atus
(Greater long-fi ngered
bat)
Marburgvirus (V) Democratic Republic of the Congo Swanepoel et al. (
2007 )
Miniopterus schreibersii
(Schreibers’s long-
ngered bat)
Duvengahe virus (V) South Africa Paweska et al. (
2006 )
Nycteris gambiensis
(Gambian slit-faced bat) Lagos Bat Virus Senegal Institut Pasteur ( 1985 )
Mops condylurus
(Angolan free-tailed bat) Zaire Ebolavirus (V) Gabon Pourrut et al. ( 2009 )
Unspecifi ed bat sp. Duvengahe virus (V) Kenya van Thiel et al. (
2009 )
(continued)
24 Bushmeat and Emerging Infectious Diseases: Lessons from Africa
524
Table 24.1 (continued)
Bushmeat species Pathogen Location References
Rodents
Funisciurus anerythrus
(Thomas’s rope squirrel) Monkeypox virus (V) Democratic Republic of the Congo Khodakevich et al. (
1986 )
Funisciurus sp. (African
striped squirrel sp.) Monkeypox virus (V) Ghana Reynolds et al. (
2010 )
Heliosciurus gambianus
(Gambian sun squirrel) Monkeypox virus (V) Ghana Reynolds et al. ( 2010 )
Paraxerus cepapi
(Smith’s bush squirrel) Leptospira (B) Botswana Jobbins and Alexander ( 2015 )
Xerus sp. (African
ground squirrel sp.) Monkeypox virus (V) Ghana Reynolds et al. (
2010 )
Unspecifi ed squirrel sp. Rabies (V) Namibia, Zimbabwe Pfukenyi et al. (
2009 ), Magwedere et al. ( 2012 )
Lophuromys sikapusi
(Rusty- bellied brush-
furred rat)
Mokola virus (V) Central African Republic Saluzzo et al. ( 1984 )
Mastomys natalensis
(Natal mastomys) Lassa Fever (V) Guinea Ter Meulen et al. (
1996 )
Rattus norvegicus
(Brown rat) Leptospira (B) Botswana Jobbins and Alexander ( 2015 )
Unspecifi ed “rat species” Rabies (V) Namibia Magwedere et al. (
2012 )
Cricetomys sp. (Giant
pouched rat sp.) Monkeypox virus (V) Ghana Reynolds et al. ( 2010 )
Atherurus africanus
(African brush-tailed
porcupine)
Salmonella (B) Gabon Bachand et al. (
2012 )
Aardvark
Orycteropus afer
(Aardvark) Leptospira (B) Botswana Jobbins and Alexander ( 2015 )
L.A. Kurpiers et al.
525
Bushmeat species Pathogen Location References
Ungulates
Equus burchellii
(Burchell’s zebra) Bacillus anthracis (B) Namibia Magwedere et al. (
2012 )
Phacochoerus
aethiopicus
(Desert warthog)
Rabies (V) Namibia Magwedere et al. ( 2012 )
Phacochoerus africanus
(Common warthog) Leptospira (B) Botswana Jobbins and Alexander ( 2015 )
Alcelaphus buselaphus
(Hartebeest) Rabies (V) Namibia Magwedere et al. (
2012 )
Bacillus anthracis (B) Namibia Magwedere et al. (
2012 )
Connochaetes taurinus
(Blue wildebeest) Rabies (V) Namibia Magwedere et al. ( 2012 )
Bacillus anthracis (B) Namibia, Tanzania Lembo et al. (
2011 ), Magwedere et al. ( 2012 )
Antidorcas marsupialis
(Springbok) Rabies (V) Namibia Magwedere et al. (
2012 )
Bacillus anthracis (B) Namibia Magwedere et al. (
2012 )
Brucella (B) Namibia Magwedere et al. ( 2011 )
Syncerus caffer (African
buffalo) Bacillus anthracis (B) Tanzania Lembo et al. (
2011 )
Brucella (B) Botswana, Mozambique Alexander et al. (
2012 ), Tanner et al. ( 2014 )
Taurotragus oryx
(Common eland) Rabies (V) Namibia, Zimbabwe Pfukenyi et al. ( 2009 ), Magwedere et al. ( 2012 )
Bacillus anthracis (B) Namibia Magwedere et al. (
2012 )
Tragelaphus strepsiceros
(Greater kudu) Rabies (V) Namibia, Zimbabwe Pfukenyi et al. (
2009 ), Magwedere et al. ( 2012 )
Cephalophus sp.
(Duiker sp.) Zaire Ebolavirus (V) Gabon Leroy et al. (
2004a )
Sylvicapra grimmia
(Bush duiker) Rabies (V) Zimbabwe Pfukenyi et al. ( 2009 )
Hippotragus niger
(Sable antelope) Rabies (V) Zimbabwe Pfukenyi et al. (
2009 )
Oryx gazelle (Gemsbok) Rabies (V) Namibia Magwedere et al. (
2012 )
Unspecifi ed “oryx,”
“antelope,” “duiker” Rabies (V) Namibia Magwedere et al. (
2012 )
V virus , H helminth, P protozoan, B bacteria
a See text for further discussions of pathogens in great apes, including uncertainty as to whether apes or humans are the source of spillovers
24 Bushmeat and Emerging Infectious Diseases: Lessons from Africa
526
Viral Pathogens
Viruses are obligatory intracellular 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 evolu-
tion. The advent of modern molecular techniques has 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 2012 ; Table 24.1 ). Bats and rodents are also major
zoonotic virus carriers (Meerburg et al. 2009 ; Baker et al. 2013 ); 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 han-
dling could present a risk (Magwedere et al. 2012 ). However, no signifi cant links
between vector-borne viruses and bushmeat hunting have been made, and we will
not include a discussion of these viruses here.
HIV/SIV : The most notable virus to emerge from the bushmeat interface is human
immunodefi ciency 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 immunodefi -
ciency virus (SIV) (Hahn et al. 2000 ; Lemey et al. 2003 ; Van Heuverswyn and
Peeters 2007 ; Sharp and Hahn 2010 ; Peeters and Delaporte 2012 ; Peeters et al.
2013 ; Kazanji et al. 2015 ). Evidence suggests that SIV crossed over to humans by
blood contact when hunters had an exposed open wound or injured themselves dur-
ing the butchering of nonhuman primates (Hahn et al. 2000 ; Wolfe et al. 2004a , b ;
Karesh and Noble 2009 ). 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. 1999 ; Sharp et al. 2005 ; Keele et al. 2006 ; Van
Heuverswyn et al. 2006 , 2007 ; Takehisa et al. 2009 ) and at least four separate spill-
overs have occurred (Peeters et al. 2013 ). HIV-2 is derived from SIVsmm from
sooty mangabeys ( Cercocebus atys ) in West Africa (Apetrei et al. 2005 ; Hirsch
et al. 1989 ; Gao et al. 1992 ; Ayouba et al. 2013 ), where high viral genetic diversity
exists and where transmission is believed to have occurred at least eight times.
The potential for future and continued spillovers from SIVs is high, and multiple
species-specifi c variants exist. For example, Peeters et al. ( 2002 ) and Peeters ( 2004 )
estimated that more than 20 % of nonhuman primates hunted for food are infected
with a variant of SIV; Locatelli and Peeters ( 2012 ) and Peeters et al. ( 2013 ) noted
that at least 45 species-specifi c variants of SIV from at least 45 primate species are
currently recognized. Aghokeng et al. ( 2010 ) sampled 1856 nonhuman primate car-
casses 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
L.A. Kurpiers et al.
527
found among the most common species in the market. However, they did fi nd SIV
variants 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. 2010 ; Liégeois et al. 2011 , 2012 ). Cross-species transmission of
strains and co-infection with more than one strain have been documented, some-
times followed by genetic recombination (Hahn et al. 2000 ; Bibollet-Ruche et al.
2004 ; Aghokeng et al. 2007 ; Gogarten et al. 2014 ), a recipe for future spillovers into
humans (Locatelli and Peeters 2012 ).
Human T-Cell Lymphotropic Virus (HTLV) : Similar to HIV, human T-lymphotropic
viruses (HTLV) are related to simian viral lineages in which signifi cant diversity has
been found (Ahuka-Mundeke et al. 2012 ; Peeters and Delaporte 2012 ). 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. 2009 , 2011 ; Courgnaud
et al. 2004 ; Sintasath et al. 2009a , b ; Wolfe et al. 2005b ; Zheng et al. 2010 ; Locatelli
and Peeters 2012 ). Similar to HIV/SIV, dual infections with more than one variant
have been documented in nonhuman primates (Agile mangabeys, Cercocebus agilis ;
Courgnaud et al. 2004 ) and in humans (Calattini et al. 2011 ; Wolfe et al. 2005b ).
Simian Foamy Virus : Simian foamy retroviruses ( SFV ) are endemic in most African
primates (Hussain et al. 2003 ; Switzer et al. 2005 ; Peeters and Delaporte 2012 ) and
are known to transmit to humans (Sandstrom et al. 2000 ; Switzer et al. 2004 ;
Calattini et al. 2007 ; Mouinga-Ondémé et al. 2010 , 2012 ). Like the other retrovi-
ruses discussed above (HIV and HTLV), SFV is genetically diverse and relatively
host species-specifi c. In Cameroon, Wolfe et al. ( 2004b ) documented three geo-
graphically independent SFV infections, which could be traced to De Brazza’s
monkey ( Cercopithecus neglectus ), mandrill ( Mandrillus sphinx ), and western
gorilla. Likewise, in Gabon, Mouinga-Ondémé et al. ( 2010 , 2012 ) 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.
Ebola and Marburg Viruses : There are seven species of fi loviruses currently identi-
ed, fi ve of which occur in sub-Saharan Africa—Genus Ebolavirus : Tai forest ebo-
lavirus (TAFV), Sudan ebolavirus (SUDV), Zaire ebolavirus (EBOV), Bundibugyo
virus (BDBV); Genus Marburgvirus: Marburg virus ( MARV ) . These pathogens are
periodically emerging viruses, typically from single spillover events, which cause
hemorrhagic fevers (reviewed by Olival and Hayman 2014 ; Rougeron et al. 2015
(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 2015 ). 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 phys-
ical contact with people who touched the animals (Leroy et al.
2004a , b ). Similarly,
24 Bushmeat and Emerging Infectious Diseases: Lessons from Africa
528
Marburgvirus was fi rst identifi ed in laboratory workers who had dissected
imported grivet ( Chlorocebus aethiops ) (Martini et al. 1968 ; Siegert et al. 1968 ).
Both western gorillas and common chimpanzees have suffered signifi cant mortality
from fi lovirus outbreaks (Walsh et al. 2003 ; Leroy et al. 2004a , b ; Bermejo et al.
2006 ; Rizkalla et al. 2007 ) and antibodies to EBOV were documented in several
other primate species by Leroy et al. ( 2004b ). 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. 1995 ; Wyers et al. 1999 ). Beyond primates,
other incidental hosts in the wild are possible, as was demonstrated for duikers
( Cephalophus spp.) (Leroy et al. 2004a ; Rouquet et al. 2005 ). As reviewed by
Weingartl et al. ( 2013 ), both dogs (naturally) and pigs (at least experimentally) can
also be infected. During the 2001–2002 EBOV outbreak in Gabon, Allela et al.
( 2005 ) 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.
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 the natural reservoir hosts for at least Marburgvirus and
EBOV. For Marburgvirus, the cave dwelling and densely packed Egyptian rousette
fruit bat ( Rousettus aegyptiacus ) is now well-documented as a reservoir host (Towner
et al. 2009 ; Amman et al. 2012 ), but antibodies against the virus and/or the presence
of viral RNA have been found in several other species (see Table 24.1 ). 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. 2011 ; Timen et al. 2009 ; Towner et al. 2009 ; Amman et al. 2012 ). 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. 2007 , 2009 ; Hayman et al. 2010 , 2012 ; Table
24.1 ). Of the ten bat species listed in Table 24.1 for Marburgvirus and EBOV, seven
are fruit bats, which are relatively larger and more visible, and thus targets of bush-
meat hunters. That said, bushmeat hunting of these bats is not ubiquitous throughout
their range and cannot solely explain fi lovirus spillovers. Mari Saéz et al. ( 2015 )
unconvincingly suggested the non-fruit bat, Mops condylurus, might have been the
source of the 2014–2015 West African Ebola outbreak. Pourrut et al. ( 2009 ) 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 identifi ed for BDBV, SUDV, or TAFV and broader surveillance for
indications of these viruses in bats and other hosts should be conducted.
Henipaviruses and Other Paramyxoviruses : Hendra virus and Nipah virus (HNVs)
are paramyxoviruses in the genus Henipavirus that emerged in Australia and south-
east Asia, respectively, with fruit bats in the genus Pteropus (family Pteropodidae)
as reservoir hosts (reviewed by Croser and Marsh 2013 ). However, recent studies
have identifi ed Henipavirus 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 Pteropus species. Documentation of Henipavirus and
L.A. Kurpiers et al.
529
related RNA (Drexler et al. 2009 ; Muleya et al. 2014 ; Baker et al. 2012 ) and anti-
Henipavirus antibodies (Hayman et al. 2008 ; Pernet et al. 2014 ) in the African
straw-colored fruit bat ( Eidolon helvum ) 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 signifi cant protein source where it is found (Kamins et al. 2011b ).
Weiss et al. ( 2012 ) documented the presence of this group of viruses in these bats
found live in bushmeat markets. Strong evidence of spillover to humans was docu-
mented by Pernet et al. ( 2014 ) who found antibodies against HNVs in human sam-
ples 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 signifi cant panmixia across the continent, which could
facilitate viral transmission between bats (Peel et al. 2013 ).
The paramyxovirus story in sub-Saharan Africa is still unfolding. Both Drexler
et al. ( 2012 ) and Baker et al. ( 2012 ) describe great diversity in paramyxoviruses
from sub-Saharan bats. In their comprehensive study of the evolutionary history of
this virus family, Drexler et al. ( 2012 ) found that the Henipavirus lineage originated
in Africa and identifi ed 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. 2014 ). This virus is most closely related to Tuhoko virus 3, a rubula-
like virus recently isolated from the Leschenault’s Rousette fruit bat ( Rousettus
leschenaultii ) in southern China. Amman et al. ( 2015 ) subsequently found Sosuga
virus in R. aegyptiacus captured from multiple locations in Uganda; the researcher
infected by this virus handled this species extensively in her studies.
Rabies and Other Lyssaviruses : Rabies is the oldest known zoonotic EID, recorded
as early as the twenty-third century BC (Steele and Fernandez 1991 ). An estimated
25,000 people die in Africa each year from rabies (Dodet et al. 2015 ), 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
Lyssavirus genus. It is joined in Africa by at least fi ve 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) as their reservoir host (Banyard et al. 2014 ) with two exceptions. The Mokola
virus is found in shrews ( Crocidura spp.), rusty-bellied brush-furred rat ( Lophuromys
sikapusi ; Saluzzo et al. 1984 ), and companion animals (Delmas et al. 2008 ; Kgaladi
et al. 2013 ). The Ikoma virus has thus far only been documented in African civets
( Civettictis civetta ; Table 24.1 , Marston et al. 2012 ). A variety of wildlife species can
be secondary hosts of rabies (e.g., in Botswana, see Moagabo et al. 2009 ) and rabies
has been documented to occur in a number of nonhuman primate species, including
those encountered in the bushmeat trade (Gautret et al. 2014 ). 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. 2008 ; Markotter et al. 2008 ; Kuzmin et al. 2010a ).
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
24 Bushmeat and Emerging Infectious Diseases: Lessons from Africa
530
(van Thiel et al. 2009 ; Paweska et al. 2006 ). Mokolo virus has been detected in two
human cases without mortality (Kgaladi et al. 2013 ).
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. 2012 ; Horton
et al. 2014 ), 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.
Lassa and Other Arenaviruses : 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 ( Mastomys natalensis ), via exposure to urine or
fecal materials. However, Ter Meulen et al. ( 1996 ) 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.
Human Monkeypox Virus : Contrary to its moniker, the reservoir hosts of human
monkeypox virus (MPX) are neither monkeys nor humans, but rather rodents. The
rst case of human monkeypox was identifi ed 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. 2010 ;
Rimoin et al. 2010 ). 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. 2010 ). 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, Funisciurus anerythrus ; Khodakevich et al. 1986 ; African
ground squirrels; Xerus sp.; Reynolds et al. 2010 ), dormice ( Graphiurus sp.;
Reynolds et al. 2010 ), and giant pouched rats ( Cricetomys sp.; Reynolds et al. 2010 ).
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. 2007 ). While dormice are small and not likely to be the target of hunt-
ing, the diurnal and highly visible squirrels and the giant pouched rats are routinely
hunted (Taylor et al. 2015 ), making the spillover to humans highly plausible.
Bacteria
Jones et al. ( 2008 ) list 54.3 % of EID events as being 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
L.A. Kurpiers et al.
531
bushmeat- related activities, but in this capacity they have received far less attention
(Cantas and Suer 2014 ). Transmission pathways for bacterial pathogens can occur
through direct exposure to body fl uids or feces, but they can also possibly be trans-
ferred indirectly through exposure to disease vectors such as fl eas and ticks when
handling animals. In a rare survey of bacterial pathogens that might spillover via
bushmeat- related activities, Bachand et al. ( 2012 ) sampled muscle from 128 bush-
meat carcasses from multiple species at markets in Gabon for the presence of
Campylobacter , Salmonella , and Shigella . While they only recorded the presence of
Salmonella , 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 Leptospira 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 ( 2015 ) 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 Bacillis anthracis , which is largely a
disease of grazing herbivorous mammals, but to which common chimpanzees are
also susceptible (Leendertz et al. 2004 ). If bushmeat includes not only the hunting
of apparently healthy animals but also sick animals or salvage of contaminated car-
casses, the risk of human outbreaks increases (Hang’ombe et al. 2012 ).
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 fl ea 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 Yersinia pes-
tis and transmitted through the infected fl eas of rodents. Africa remains an endemic
region of importance for this pathogen (World Health Organization 2005 ; Davis
et al. 2006 ). Fleas and ticks are also responsible for transmitting rickettsial patho-
gens, such as Rickettsia africae , which causes African tick-bite fever ( ATBF ) .
Mediannikov et al. ( 2012 ) collected ticks from duikers and a pangolin that were
living in close proximity to humans in Guinea and found R. africae in 10 % of ticks
collected from the tree pangolin ( Manis tricuspis ), 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 via
bushmeat- related activities.
Helminths
The helminths or “worm-like” animals include many parasites of zoonotic potential,
although Taylor et al. ( 2001 ) 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 2000 ).
24 Bushmeat and Emerging Infectious Diseases: Lessons from Africa
532
Several studies have examined the prevalence of helminths in animals from bush-
meat markets and found high rates of multiple species. For example, Adejinmi and
Emikpe ( 2011 ) collected fecal samples from greater cane rats ( Thryonomys swind-
erianus ) and bush duikers ( Sylvicapra grimmia ) 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. ( 2012 )
and Mukaratirwa et al. ( 2013 ) reviewed the evidence for Trichinella infection in
humans, livestock, and wildlife in sub-Saharan Africa and noted that bush-pigs
( Potamochoerus spp.) and desert warthogs ( Phacochoerus aethiopicus ) are a source
for human infection. As is the case with many other pathogens, humans and nonhu-
man primates share susceptibility to many parasitic helminth species (Pedersen
et al. 2005 ; Pourrut et al. 2011 ). Pourrut et al. ( 2011 ) sampled gastrointestinal para-
sites 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. ( 2010 ) had similar fi ndings from common chimpanzee fecal
samples. Overall, the available evidence suggests that spillover of many of these
pathogens during bushmeat-related activities is likely.
Protozoan
Protozoans are a paraphyletic group of eukaryotic organisms that are neither ani-
mals, plants, nor fungi and include amoebas and giardia. The risk of protozoan
spillover from bushmeat-related activities is similar to that for helminths and bac-
teria in that exposure to feces, bodily fl uids, and even potentially to meat could
transmit disease to a permissive human host (Pourrut et al. 2011 ). A number of
protozoans are important pathogens with zoonotic potential (Taylor et al. 2001 ).
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. 2010 ; Pourrut et al. 2011 ). Gillespie et al.
( 2010 ) documented the amoeba Entamoeba histolytica and the ciliated protozoan
Balantidium coli 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. ( 2002 ) docu-
mented both protozoans in common chimpanzees, western gorillas, agile mang-
abeys, and humans living in the same region in Central African Republic. A number
of other nonhuman primates have had documented E. histolytica infections as well
(see Table 24.1 ). Other protozoan examples include Toxoplasma gondii , which
causes the disease toxoplasmosis, but could not be detected during a recent, albeit
small scale, survey of bushmeat (Prangé et al. 2009 ) and water/foodborne parasites
such as Giardia. Recent studies have documented Giardia in a variety of species
that exist in the bushmeat trade, including western gorilla and African buffalo
( Syncerus caffer ) (Hogan et al.
2014 ).
L.A. Kurpiers et al.
533
Fungi
Fungi are increasingly being recognized as important pathogens that may emerge,
even in humans (Jones et al. 2008 ; Fisher et al. 2012 ), 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 fi ght 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 1998 ; Jones et al. 2008 ).
Prions
Only 5 % of prion diseases are 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 2011a , b ; Bons et al. 1999 ; Lee et al.
2013 ), 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.
Local Knowledge and Perception of Disease Risk
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 transmis-
sion from animals to humans (Subramanian 2012 ). Similarly, 23 % of rural–urban
hunters and traders in Ghana perceived a disease risk from a bat-bushmeat activity,
with signifi cantly more respondents associating risk with bat consumption than bat
preparation or hunting (Kamins et al. 2014 ). Individuals who participate in butcher-
ing wild animals typically associate less risk to meat preparation and consumption
than those who do not participate in butchering (Kamins et al. 2014 ) (Fig. 24.2 ).
24 Bushmeat and Emerging Infectious Diseases: Lessons from Africa
534
LeBreton et al. ( 2006 ) found that hunters and butchers who perceived personal risks
were signifi cantly 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. 2014 ). In con-
trast, a large-scale survey among rural Central African population showed that the
majority (74 %) of respondents perceived contact with bushmeat blood or body
uids as dangerous (LeBreton et al. 2006 ). Unfortunately, studies in this fi eld can be
challenging, as reported perceptions may differ from actual or ‘revealed’ behaviors
and beliefs (Wilkie 2006 ).
Although there seems to be some level of risk awareness in certain human popu-
lations, several studies report a distinct lack of precautionary behavior, resulting in
hunters, butchers, and consumers exposing themselves to zoonotic diseases.
LeBreton et al. (
2006 ) found that only 4 % of hunters and 2 % of people reporting
butchering indicated that they took precautions against contact with animal blood
and fl uids 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. ( 2014 ) examined human–animal
Fig. 24.2 A pangolin
being prepared in rural
Ghana; photo credit Laura
Kurpiers
L.A. Kurpiers et al.
535
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 com-
monly 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. 2014 ).
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. 2006 ). This is especially true,
since the current rate of hunting wild animals will likely continue—at least until
domestic animal production increases and can support the protein needs of the
local people.
The Way Forward
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 dis-
ease outbreaks is often costly economically and in terms of human well-being
(Childs and Gordon 2009 ; United Nations Development Program 2015 ). Increased
pre-spillover surveillance measures along with quantifi cation of spillover risk is
critically needed. For example, Wolfe et al. ( 2004b , 2005b ) 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.
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. 2010 ; Gebreyes et al. 2014 ). 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 2006 ).
The education and enforcement necessary to implement such a restriction must con-
sider the cultural and economic contexts surrounding individual communities.
Consider, for example, the problems with enforcement of access restrictions and the
24 Bushmeat and Emerging Infectious Diseases: Lessons from Africa
536
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 dis-
eases 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. 2015 ).
A more realistic strategy may be to concentrate 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 impor-
tant to incorporate collaborative and interdisciplinary approaches between veterinary
researchers, ecologists, microbiologists, public health researchers, and anthropolo-
gists 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. 2014 ).
Education
The risk of disease transmission could be reduced through community education
that focuses on people with high levels of exposure to wild animals (Wolfe et al.
2007 ). 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 dur-
ing hunting and butchering as this may be overlooked by some hunters (LeBreton
et al. 2006 ). Because the risk perception of hunters and those engaging in butcher-
ing wild animals has a negative association with the level of participation in meat
preparation and consumption (Kamins et al. 2014 ), this may reduce current levels of
pathogen exposure and transmission, if not by discouraging individuals to partici-
pate in preparation and consumption, then by encouraging those individuals to more
proactively consider safety and preventative measures.
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. 2012 ). 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 fl uids of wild animals. Hunters are urged
to redirect hunting efforts away from apes and monkeys and towards less risky spe-
cies such as antelope and rodents, while also being discouraged from butchering
animals when there are cuts or injuries on their hands and limbs.
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
L.A. Kurpiers et al.
537
this knowledge promotes a change in behavior (McCaffrey 2004 ). 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. 2014 ). When asked about what would change their behavior, partici-
pants responded; becoming ill from zoonotic disease followed by alternative liveli-
hoods and stricter laws. Because awareness is not directly related to behavior,
Monroe and Willcox ( 2006 ) 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 to protect themselves.
Surveillance
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. 2012 ) and
improve systematic global monitoring efforts. This could help detect, defi ne, and
control local human emergence while it is still locally confi ned 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. 2012 ). Bushmeat hunters
would be an important target group, as they are in contact with bodily fl uids from
animals and are at risk for transmission and infection from novel pathogens.
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 2013 ). In order to track and provide data for EIDs, this effort coordinates
the collection of fi lter-paper blood samples from both hunted animals and people
who hunt and butcher wild animals. Early results have shown that this type of sur-
veillance can assist in early detection of new diseases by offering insight into patho-
gen origin. It would also help describe the spillover dynamics of new or existing
diseases. Such data are valuable for developing a detailed, mechanistic understand-
ing 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. 2007 ). 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 sustainable mechanism to reduce or control disease
spillover risks (Daszak et al.
2007 ).
24 Bushmeat and Emerging Infectious Diseases: Lessons from Africa
538
Call for Research
The social and environmental issues 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 holis-
tic manner, by integrating multiple efforts to achieve common objectives. Although
much progress has been made not only in addressing the problems concerning bush-
meat harvest and zoonotic disease spillover, there is much work to be done. Research
that would pave the way for future efforts would include the quantifi cation 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 quantifi cation 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 asso-
ciated with bushmeat harvest, and help understand in what circumstances zoonotic
disease spillover events occur.
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, educa-
tion, or aid. The study of zoonotic spillover events related to viruses, while not com-
pletely developed, has received far more attention than the related fi elds of spillover
from bacterial or other non-virus pathogens. There is signifi cant interest in pursuing
these lines, as they represent an underdeveloped body of knowledge that could have
signifi cant impacts related to human health and disease ecology.
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