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With on-going changes in land use practices from conventional livestock farming to commercial, wildlife-based activities, the interface or interaction between livestock and wildlife is increasing. As part of the wildlife-based activities of ecotourism, breeding and hunting, game farmers are also exploring the utilisation of meat from hunted or harvested game. The expanding interface or increased interaction between livestock and wildlife increases the risk of disease incidence and the emergence of new diseases or the re-emergence of previously diagnosed diseases. The risk is not only related to domestic and wild animal health, but also to the occupational hazards that it poses to animal handlers and the consumers of game meat. This review endeavours to highlight the role that game plays in the spreading of zoonotic diseases to other animals and humans. Examples of zoonotic diseases that have occurred in wild animals in the past, their relevance and risk have been summarised and should function as a quick reference guide for wildlife veterinarians, ecologists, farmers, hunters, slaughter staff, processors and public health professionals.
The progressive expansion of game ranching as an extensive form of game farming on developed (fenced) land in southern Africa has resulted in ranching with endangered and/or rare species which can to a greater or lesser extent, be found in free community with livestock. In many parts of the world, farmers are changing from conventional livestock farming to commercial, wildlife-based activities such as ecotourism, which usually requires a wide diversity of frequently translocated species and adequate populations for tourist viewing (Bengis, Kock & Fisher 2002). With game becoming more valuable and therefore stocked at higher densities on smaller properties, disease prevention has become a very important aspect of game ranch management (Bester & Penzhorn 2002). A survey amongst South African game farmers revealed that 34.3% of these farmers are farming with both domestic and game animals (Bekker 2011). Skinner (1970) expressed concern regarding the dangers that game poses to domestic livestock by acting as reservoir hosts of pathogens of livestock which can cause epizootic disease and also that the handling and management of wild animals in relation to disease control is difficult. In support of this, Bengis et al. (2004) were of opinion that the abovementioned situations will probably enhance and intensify the wildlife-livestock interface and that the potential for ’cross-over‘ of diseases will increase. The cross-over of epizootic outbreaks represents a serious threat both to wildlife and, via reverse spill-over (‘spill-back‘), to sympatric populations of susceptible domesticated animals (Daszak, Cunningham & Hyatt 2000). Bengis et al. (2002) also indicated that foreign animal diseases cycling in livestock may cross the interface and infect wildlife. Wildlife therefore plays an important role in the spreading of transmissible animal diseases. In the United States, the presence of brucellosis amongst elk and bison in the Yellowstone National Park is considered a potential threat to domestic animals grazing in the park (Daszak et al. 2000). Godfroid (2002) was of the opinion that the development of the game farming industry has contributed to the re-emergence of brucellosis. Diseases such as malignant catarrhal fever (MCF) in wild herbivore species often show few clinical signs, but the disease is often deadly to cattle. According to Li et al. (1996), the viruses responsible for MCF are an important obstacle to the propagation of endangered ruminant species in the wild, in captivity, or on game farms. Although the Office Internationale des Epizooties (OIE) has declared that rinderpest has now been eradicated from the surface of the earth and that all 198 countries and territories in the world with rinderpest-susceptible animals are free of the disease (Food and Agricultural Organization [FAO] 2011), Gortázar et al. (2007) have pointed out that true multihost diseases that are regarded as eradicated are the worst, because a single spill-over from wildlife to livestock may have severe consequences for health and the economy. Rinderpest, for example, was eradicated in Nigeria in 1974 after the JP15 campaign, but was reintroduced between 1980 and 1983 into two states of Nigeria from infected cattle to wildlife, and this resulted in the loss of an estimated one million cattle and numbers of wildlife, of which 207 buffalo, 20 warthog, eight waterbuck and two bushbuck carcasses were recovered (Shanthikumar & Atilola 1990). Other examples of multihost diseases include bovine TB (Michel et al. 2006; Phillips et al. 2003), foot and mouth disease (Scoones et al. 2010) and avian influenza (Alexander 2000; Gauthier-Clerc, Lebarbenchon & Thomas 2007).Regarding zoonotic diseases, Cleaveland, Laurenson and Taylor (2001) then already indicated that 61% (868) of the 1415 species of infectious organisms known to be pathogenic to humans were of zoonotic nature. Some of these diseases can be transmitted through the consumption of animal-infected material or through the handling of such material (occupational disease). For the purpose of this review, human tuberculosis as a result of Mycobacterium bovis is briefly discussed. Several publications have already appeared on the prevalence of bovine tuberculosis in African wildlife and elsewhere in the world (e.g. Ayele et al. 2004; Michel 2002; Michel et al. 2006; Parra et al. 2006; Zieger et al. 1998). It was estimated by the World Health Organization (WHO) that M. bovis is the causative bacterium in 3% of all tuberculosis cases (WHO 1994a). Although high priority is placed on the meat inspection function at formally registered abattoirs to identify and remove carcasses with lesions of M. bovis from the food supply chain, asymptomatic animals or localised lesions could pass through the inspection system unnoticed (Van der Merwe et al. 2009). Poor and rural communities, furthermore, often obtain meat from uncontrolled and unregistered slaughter facilities where there is no meat inspection. Regarding game abattoirs, Bekker (2011) showed that in South Africa there are only a few registered game abattoirs, which are mostly used for export purposes, and that the real number and location of game slaughter facilities located on game farms are unknown to the relevant authorities and that almost no meat inspection is done on game farms. According to Cosivi et al. (1998), the intake of uninspected game meat may increase the risk of contracting tuberculosis. A number of authors such as Cosivi et al. (1995), Cosivi et al. (1998), De la Rua-Domenech (2006) and Thoen, Lobue and De Kantor (2006) have reported on human tuberculosis due to M. bovis globally. Some other examples of zoonotic diseases contracted by humans include a cutaneous anthrax outbreak that occurred in rural Paraguay through touching the meat of a sick cow (Harrison et al. 1989); an anthrax occurrence in Mashonaland East province of Zimbabwe due to handling, eating and drinking products of an infected animal (Mwenye, Siziya & Peterson 1996); brucellosis contracted by workers in meat packing plants (Taylor & Perdue 1989; White et al. 1974) and eating of caribou meat (Chan, Baxter & Wenman 1989); human trichinellosis which occurred in northern Italy after eating raw horse meat (Pozio et al. 1988); and the 2010 outbreak of Rift Valley fever (RVF) in South Africa where 172 cases and 15 human deaths after direct contact with RVF-infected livestock were reported by the national health department in South Africa (WHO 2010). Pavlin, Schloegel and Daszak (2009) indicated that the simplest way to minimise the risk of zoonotic disease is the reduction of opportunities for transmission of diseases from wildlife to humans. Although not clear for the neighbouring countries of South Africa, the survey amongst South African game farmers by Bekker (2011) indicated, however, that 41% of farmers with mixed farming systems have no control measures to prevent animal interaction in order to prevent disease spreading between game and domestic animals. Furthermore, specific gaps have been identified in game farming practices insofar as the establishment of written health plans, routine health inspections, screening for zoonotic diseases, provision of quarantine camps and record keeping of health and withdrawal periods as suggested by the GlobalGAP integrated farm assurance standard (GlobalGAP 2007). Furthermore, Liddell and Baily (2001) were of the opinion that the lack of records of animal health treatment undermines the ability to track the inputs used during this animal production stage of the supply chain. This desktop study provides a review of disease control mechanisms by the OIE, Angola, Botswana, Namibia, South Africa and Zimbabwe as well as a summary of the diseases associated with game occurring in the aforementioned countries and the relevance as well as the risk of cross-infections related to some zoonotic diseases that have occurred with game. This review should therefore function as a quick reference guide for wildlife veterinarians, ecologists, farmers, hunters, slaughter staff, processors and public health professionals.
Background
Animal hosts, vectors and the environment in a natural ecosystem are in a dynamic balance, with occasional pathogen emergence and impact, but disease is not frequent when compared to artificial or domesticated animal farming systems. The success of preventing disease on a farm revolves around the abovementioned balance. Pressures on the environment such as the expected increase in human population (1 billion in Africa from 2009 to 2050), rapid urbanisation in developing countries and the global demand for livestock products (requiring higher stock rates) cause multiple animal health problems (Thornton et al. 2009). As an example, both scenarios of overstocking and introducing animals into habitats that they are not adapted to (e.g. lechwe in the Free State Province of South Africa and gemsbok in high rainfall areas) are becoming more common in South Africa. These drivers may cause disease vectors to increase with host species not suited for their habitat (and vice versa) to be affected first by a disease (Bester & Penzhorn 2002).
‘Office Internationale des Epizooties’ controlled diseases
Internationally, the OIE is the intergovernmental organisation responsible for improving animal health worldwide and is recognised as a reference organisation by the World Trade Organization (WTO). With the consideration of international spread, zoonotic potential, significant spread in native populations and emerging diseases as criteria, the OIE keeps a list of so-called ’OIE listed‘ diseases for listing. All the countries relevant to this review (Angola, Botswana, Mozambique, Namibia, South Africa, Zimbabwe) are member countries of the OIE. It is required that all member countries will report to the OIE on incidences of any of the OIE listed diseases (OIE 2011a).
Disease control in Angola, Botswana, Mozambique, Namibia, South Africa, Zimbabwe
Policies and legislation normally form part of governmental animal health and food and meat control systems with the aim to prevent or control the spreading of disease to animals and humans. Regarding Southern Africa, Thomson and Penrith (2011) reported comprehensively on the animal health policy, legislation and trade in beef in the five participating states of the Kavango-Zambezi transfrontier conservation area (KAZA TFCA) which include Angola, Botswana, Namibia, Zambia and Zimbabwe and of which, Botswana, Namibia and Zimbabwe are neighboring countries of South Africa. Thomson and Penrith (2011) also list some trade related protocols of the Southern African Development Community (SADC) dealing with rules of origin for products to be traded between the member states of the SADC, sanitary and phytosanitary (SPS) rules, and technical barriers to trade (TBT). The following two tables provide non-exhaustive summaries of existing legislation in Angola, Botswana, Namibia, South Africa and Zimbabwe on the control of animal diseases and zoonosis (Table 1) and trade in meat and meat products (Table 2).
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Disease occurrence in game in Angola, Botswana, Namibia, South Africa and Zimbabwe
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Wildlife diseases have become more important in recent years and have led to an explosion of related knowledge (Gortázar et al. 2007). A non-exhaustive summary of zoonotic diseases that have occurred in wildlife animals in Angola, Botswana, Namibia, South Africa and Zimbabwe is therefore presented (Table 3).
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TABLE 1:
Summary of some legislation governing animal diseases in Angola, Botswana, Namibia, South Africa and Zimbabwe.
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TABLE 2:
Summary of some legislation governing trade in meat and meat products in Angola, Botswana, Namibia, South Africa and Zimbabwe.
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Overview of some zoonotic diseases associated with game
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Several worldwide outbreaks of animal related diseases such as bovine spongiform encephalopathy (BSE), avian influenza, RVF, et cetera and the associated media declarations have alerted consumers about the safety of meat in general. Because of these disease outbreaks, consumers are more informed and concerned about the safety and quality of meat products (Hoffman et al. 2005; Radder & Le Roux 2005). The industry has a moral responsibility towards the consumer in this regard. Gregory (2000) pointed out that the public puts their faith in the food authorities and the food industry to provide them with safe products. To achieve this, Gortázar et al. (2007) suggest that there should be close cooperation between multidisciplinary professionals such as wildlife ecologists, veterinarians and public health professionals. Regarding game meat production, certainly the game farmer, game hunting associations, processors (including those on farms), wholesale and retail markets and consumer interest groups should join in this multidisciplinary team. According to Bekker (2011), treatment of sick game animals is mostly done by veterinarians (59.5%) followed by trained farm staff (31.4%) and untrained farm staff (9.1%). From a veterinary health perspective, Blaha (1999) indicated that food animal practitioners play an important part in animal health management in general. In addition to veterinarians and other animal practitioners, veterinary public health practitioners can also play a role to ensure animal health and the provision of safe meat derived from slaughter animals to the consumer. Resulting from a desk top study, a non-exhaustive summary of the relevance as well as the risk of cross infections related to some of the zoonotic diseases that have occurred in the wild animals listed in Table 3 is also provided (Table 4).
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Emerging and re-emerging zoonotic diseases
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Sleeman (2006) raised a concern that the handling and eating of game meat by humans will expose them to new micro-organisms and contaminants and will result in the emergence of new diseases. Over the past years, emerging diseases have frequently hit the headlines, of which most have a zoonotic foundation. Emerging and re-emerging zoonotic diseases are those that are newly identified, newly evolved or have occurred previously, but have more recently shown an increase in incidence or expansion into a new geographical area, host or vector range (Bengis et al. 2004; Paulsen & Smulders 2004). Though not zoonotic, an outbreak of African swine fever (ASF) has for example recently occurred in the eastern parts of the Gauteng Province and the western parts of the Mpumalanga Province of South Africa. Both these areas fall outside South Africa’s ASF control area (GDARD 2012). Although the sources of these outbreaks are still unknown, the southward distribution and expansion of warthogs and tampans associated with the species could also contribute to the spreading of ASF beyond the borders of the ASF control areas (RMRDSA 2010). Although Daszak, Cunningham and Hyatt (2000) in their description of the relationship between wildlife, domestic animal and humans indicated that most emerging diseases impact on almost all groups, Pavlin, Schloegel and Daszak (2009) were of the opinion that most emerging infectious diseases are associated with wild animal zoonotic diseases. Infectious pathogens in wild animals as possible reservoirs have become increasingly important due to their substantial impacts on human health, domestic animal production, wildlife-based economies, wildlife conservation and global biodiversity (Bengis et al. 2004; Daszak et al. 2000; Paulsen & Smulders 2004). According to the FAO (2010), ± 60% of emerging infectious diseases of humans are zoonotic, of which 72% originate from wildlife. In addition, Christensen (1996) indicated that food of animal origin holds a threat to human health due to the diseases that it may transfer to humans and other animals.Risk factors influencing the occurrence of diseases in wild animals are based on (1) the movements or translocations of wild or domestic animals and animal products, (2) the result of wildlife surplus, (3) the changing agricultural practices to farming with wild animals that support the transmission of pathogens between wild and domestic animals, (4) host and vector expansion, (5) the association with ’spill-over‘ from domestic animals to wildlife populations living in the same proximity, (6) the relation to human intervention, (7) diseases with no overt human or animal involvement, (8) the increase in human population and their relation to local and international travel and contact with wildlife populations and their products, (9) adaptations of pathogens themselves to certain situations, (10) changes in the environment and ecosystems that increase the transmission of infectious agents through open-air breeding and (11) enhancement of diagnostic and epidemiological techniques which assist in early detection of emerging or re-emerging infective agents (Bengis et al. 2004; Daszak et al. 2000; Gortázar et al. 2007). Bengis et al. (2004) warned that the geographical expansion of pathogens and/or their vectors as a result of global warming and other associated climatic changes and the continued collision between human populations and wildlife in the human endeavour to advance into new habitats and ecosystems will increase the risk of new emerging diseases in years to come. They also pointed out that the most likely populations to be affected are those in less developed countries and poorer communities. Several opportunities exist for diseases to spread from one animal to another as they move around and associate with each other. Diseased animals, for example, die and are left to scavengers to clean, which in turn are infected and they spread the disease further. This process implies, however, that there may be some extent of dilution which will make the organisms responsible for disease less abundant and less likely to persist. Dilution occurs when other hosts in a community are also exposed instead of only being present in one highly competent reservoir host species alone (Begon 2008). Ogden and Tsao (2009) indicated that this method of dilution will result in fewer new infections and thereby reduce the basic reproductive number (R0) of the pathogen. In their study on Lyme disease, however, they also indicated that the extent of amplification or dilution of the disease is dependent on the mechanisms of completion, host contact rates and host resistance. Bengis et al. (2002) indicated that the most probable transmission mechanisms include (1) aerosols contaminating feed, water and range and (2) flightless vectors such as ticks, and winged vectors such as mosquitoes, and that one of the most important factors in disease transmission between livestock and wildlife is the creation of new interfaces. In addition to this, the increase in the distribution of game meat may also now be seen as a possible risk in the spreading of diseases.
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TABLE 3:
Summary of some zoonotic diseases reported to have occurred in game in Angola, Botswana, Namibia, South Africa and Zimbabwe.
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Disease surveillance and management
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From a study by Bekker (2011), there is evidence of minimal disease surveillance and management amongst game farmers. According to Paskin (1999) the early detection of disease increases the chance to arrest the disease prior to it causing damage. Detection requires that a surveillance system must be in place as required by the GlobalGAP integrated farm assurance standard (GlobalGAP 2007). Surveillance activities can be defined as:All regular activities aimed at ascertaining the health status of a given population with the aim of early detection and control of animal diseases of importance to national economies, food security and trade. (Paskin 1999) Disease surveillance is not a haphazard activity and therefore requires proper planning and techniques. A summary of aspects that Bengis et al. (2002) have provided as guidance in this regard is presented here (Table 5). From an economic perspective, it also makes sense to have proper prevention measures in place. The OIE (2006b) indicated in a report that dealt with an economical analysis of the costs of prevention versus the costs of outbreak, that the benefits accrued from improved prevention and control measures outweigh the costs of prevention and control investment. As an example, Tambi et al. (1999) proved that rinderpest control in Africa through the implementation of the Pan-African Rinderpest Campaign (PARC) in 1986 has been a wise public investment decision and that both producers and consumers gained from it economically.
This review shows that game plays an important role in animal disease spreading to other domesticated and wild animals and provides summaries of the occurrence of some zoonotic diseases in game in Angola, Botswana, Namibia, South Africa and Zimbabwe, current disease and meat (food) control legislation in these countries and the relevance as well as the risk of cross-infections related to some zoonotic diseases that have occurred with game. Of particular concern to game meat safety are the zoonotic diseases that can be transmitted through the consumption of meat and meat products. The consumer has to be safeguarded from possible infection (zoonosis) and therefore meat inspection of game carcasses is essential (Skinner 1970). However, as previously indicated, several of the zoonotic diseases are also an occupational hazard as farmers, farm workers, hunters, slaughter staff, veterinarians, processors, et cetera , can become infected whilst handling the animals or meat thereof.
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TABLE 4:
Summary of relevance as well as the risk of cross infections related to some zoonotic diseases that have occurred in wild animals.
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TABLE 5:
Factors to consider with disease detection and management.
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Pavlin et al. (2009) indicated that the simplest way to minimise the risk of zoonotic disease is the reduction of opportunities for transmission of diseases from wildlife to humans. To achieve this, Gortázar et al. (2007) suggested a multidisciplinary approach of wildlife ecologists, veterinarians and public health professionals. In addition, Oberem and Oberem (2011) pointed out the importance of disease-causing investigations carried out on dead animals by experts who will know how to prevent further spreading of the diseases, especially zoonotic diseases. In this regard, the animal disease investigation laboratories also play an important role as they can assist with the carrying out of routine investigations and surveillance programmes (especially notifiable, controlled and zoonotic diseases and research on animal disease and related issues) (Geering, Roeder & Obi 1999). The implementation of a comprehensive surveillance plan should be of critical importance to veterinary authorities (Gortázar et al. 2007) and will require innovative measures to improve vigilance (Bengis et al. 2004). In this regard, the South African Department of Agriculture, Forestry and Fisheries (DAFF), for example, have an epidemiology division whose mandate is contained in the Animal Diseases Act (Act No. 35 of 1984) (as amended) (South African Government 1984) and its main functions include (Ungerer 2008):• developing, analysing and auditing policies for the surveillance of animal diseases and diseases that can be transmitted from animals to humans • developing, analysing and auditing policies on disease reporting in the different provinces of South Africa • conducting risk assessments at a national level • acting as contact point for communicating risk and the occurrence of animal diseases in South Africa to foreign governments and international bodies • managing animal disease information and reporting thereof to the World Organization for Animal Health (OIE), Southern African Development Community (SADC) and the African Union (AU) • managing of animal disease information by using a Geographic Information System • managing of animal disease early warning systems (SADC, nationally and internationally) • ensuring that there are adequate government veterinary laboratory services at provincial level and elsewhere, for example in the Kruger National Park, and by
working in collaboration with the Onderstepoort Veterinary Institute of the Agricultural Research Council • enforcement of quality systems in diagnostic veterinary laboratories • auditing the enforcement of policy for reference laboratories. However, these measures will only be effective if wild game ranchers follow the correct procedures in contacting the relevant authorities. Bekker (2011), however, has illustrated negligence in certain farming practices and a lack of knowledge of farmers that may impact negatively on a country’s surveillance plan. To prevent a situation where farmers and other stakeholders may not place a high value on participating in achieving the main objectives of a surveillance plan, it is recommended that policy makers and law enforcers at all levels of government in collaboration with other wildlife industry stakeholders such as wildlife veterinarians, ecologists, farmers, hunters, slaughter staff, processors and public health professionals establish strategies to ensure that all stakeholders are adequately trained in the role that they play in the control of zoonotic diseases in game. Industry organisations such as farmer and hunting associations as ’bridging organisations‘ have a role to play with the provision of information or knowledge by (1) encouraging dialogue between governmental policy makers and industry, (2) acting as channels for policy makers to direct and apply new strategies at the industry-level, (3) assisting with the bottom-up flow of information at industry level and (4) providing platforms for information exchange (Berkes 2009; Tarnoczi & Berkes 2010). In addition, bridging organisations can provide a platform for trust building, sense making, learning, vertical and horizontal collaboration, and conflict resolution (Hahn et al. 2006). Meaningful knowledge is most likely to result in concept development, attitudinal change and positive behaviour.
We would like to thank the library and information services of the Tshwane University of Technology library for their support in obtaining information used in this review. This study was also partly funded by Stellenbosch University Overarching Strategic Plan Food Security Initiative.
Competing interests
The authors declare that they have no financial or personal relationship(s) which may have inappropriately influenced them in writing this paper.
Authors’ contributions
This manuscript forms part of a PhD study where the student J.L.B. (Tshwane University of Technology) was mainly responsible for the compilation of the review published on zoonotic diseases. L.C.H. (Stellenbosch University) was the first study promoter and P.J.J. (Tshwane University of Technology) was the second study promoter.
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