WILDLIFE AND EMERGING INFECTIOUS DISEASES Carol de Jong et al. 2011

WILDLIFE AND EMERGING INFECTIOUS DISEASES Carol de Jong a, Hume Field a, Scott H. Newman b and Jonathan H. Epstein c In: INVESTIGATING THE ROLE OF BATS IN EMERGING ZOONOSES FAO 2011 Although the current focus on emerging diseases in scientific literature and the popular press might suggest otherwise, novel diseases have occurred throughout history. By definition, every newly identified disease is novel. Today’s endemic disease was yesterday’s novel disease. This observation is not meant to invoke any complacency regarding the inevitability of disease emergence, nor to downplay the need for surveillance or discount the challenges associated with investigating and managing the outbreak of new diseases. Rather, it offers a window into the lessons of history. Emerging infectious diseases (EIDs) are defined as infections that have newly appeared in a population or have existed previously but are rapidly increasing in incidence or geographic range (Morens, Folkers and Fauci, 2004). Emerging infections have been a familiar threat since ancient times, with pandemics of cholera, influenza, smallpox and measles causing the deaths of millions of people worldwide. Since the 1940s, the incidence of EIDs has risen significantly and more than 300 infectious diseases have emerged (Jones et al., 2008), most of which are viruses (Taylor, Latham and Woolhouse, 2001). More than 60 percent of EIDs are of zoonotic origin (Jones et al., 2008), and in the last decade of the twentieth century zoonotic EIDs constituted 52 percent of all EID events (Taylor, Latham and Woolhouse, 2001). Of all EIDs, zoonoses from wildlife represent the most significant, growing threat to global health. Among the zoonotic EIDs to emerge since the 1940s, the majority of EID events have originated in wildlife (71.8 percent) and their incidence has continued to increase (Jones et al., 2008). Emerging zoonotic pathogens have been identified in ungulates, carnivores, rodents, primates, bats and other mammal and non-mammal species (Woolhouse and Gowtage-Sequeria, 2005). The best known EID of modern times, acquired immunodeficiency syndrome (AIDS), emerged from non-human primates around the early twentieth century (Worobey et al., 2008). AIDS, which is caused by infection with one of two types of the human immunodeficiency virus (HIV), now threatens to surpass the Black Death of the fourteenth century and the 1918 to 1920 influenza pandemic, each of which killed 50 million people (Morens, Folkers and Fauci, 2004). Other recently emerged diseases, including Ebola virus, hantavirus, Nipah virus, West Nile virus, severe acute respiratory syndrome (SARS) coronavirus and highly pathogenic avian influenza (HPAI) virus, are examples of emerged or emerging zoonoses that have had (or threaten to have) a significant impact on human health. a The State of Queensland, Department of Employment, Economic Development and Innovation (2011) b Food and Agriculture Organization of the United Nations c EcoHealth Alliance 2 Investigating the role of bats in emerging zoonoses Understanding the factors that lead to pathogens jumping species or to increased contact among wildlife, livestock and humans is critical to understanding how diseases emerge from wildlife. DRIVERS OF EMERGENCE Wildlife populations constitute a large and often unknown reservoir of infectious agents (Chomel, Belotto and Meslin, 2007), playing a key role in emergence by providing a “zoonotic pool” from which previously unknown pathogens may emerge (Morse, 1995). The emergence of many zoonoses can be attributed to predisposing factors such as global travel, trade, agricultural expansion, deforestation and urbanization; such factors increase the interface and/or the rate of contact among human, domestic animal and wildlife populations, thereby creating increased opportunities for spill-over events to occur (Daszak, Cunningham and Hyatt, 2000; 2001). Lederberg, Shope and Oaks (1992) describe these changes as providing an “epidemiological bridge” that facilitates contact between the agent and the naive population. Daszak, Cunningham and Hyatt (2000) suggest that disease emergence from wildlife sources is primarily an ecological process, with emergence frequently resulting from a change in the ecology of the host or the agent or both. They suggest that most emerging diseases exist within a finely balanced host-agent continuum among wildlife, domestic animal and human populations. Any changes in the environment or host behaviour provide agents with favourable new ecological niches, allowing them to reach and adapt to new hosts and spread more easily between them (Morens, Folkers and Fauci, 2004). FIGURE 1.1 The host-parasite continuum: most emerging diseases exist in a host-parasite continuum among wildlife, domestic animal and human populations Translocation Wildlife EID 􀁴 Human encroachment 􀁴 Ex situ contact 􀁴 Ecological manipulation 􀁴 Encroachment 􀁴 Introduction 􀁴 “Spill-over” and “spill-back” 􀁴 Global travel 􀁴 Urbanization 􀁴 Biomedical manipulation Domestic animal EID Agricultural intensification Technology and industry Human EID Source: Daszak, Cunningham and Hyatt, 2000 Pathogen adaptation and virulence are additional dynamics that have direct linkages to the ecological systems in which they occur. Regardless of whether the system is natural or agricultural, the key to pathogens’ survival is their ability to adapt to the ever-changing environment. In natural systems, loss of biodiversity, changes in landscape ecology, climate change and other variables pose innate adaptation challenges for pathogens. In agricultural settings, farming modifications including intensification, changes in animal density or husbandry practices, use of pharmaceuticals and marketing create the adaptation challenges for pathogens. The pathogens that exist in wildlife or livestock hosts are therefore constantly challenged to adapt to new environmental circumstances for their survival, resulting in the emergence of “super pathogens” that can cross sectors such as the wildlife-livestock interface, and can ultimately infect humans when the opportunity arises. Table 1.1 lists a range of drivers for the emergence of infectious disease identified by Daszak, Cunningham and Hyatt (2000), Morens, Folkers and Fauci (2004), Woolhouse and Gowtage-Sequeria (2005) and Chomel, Belotto and Meslin (2007). At the macro TABLE 1.1 Drivers of emerging zoonoses Human behaviour* Cultural preference and celebrations Food choices (bushmeat, live-animal markets, freshly killed) Traditional medicine Consumption instead of conservation Ecotourism Petting zoos Exotic pet ownership Modifications to natural habitats* Communities and settlement encroaching on natural habitat Development and construction Water resource management (dams, redirecting river or ocean flow patterns) Deforestation Fragmentation of habitat Loss of biodiversity and species Waste and garbage management Climate change Changes in agricultural practices* Expansion of livestock farming and encroachment Intensification of production systems resulting in overcrowding, stress, and faster growing and input/ output periods More wastewater and faecal runoff into the environment Farming of new species, including wildlife, without proper medical care, husbandry or biosecurity Globalized international market chains * The impacts are amplified by human demographics and socio-economic advancement from poverty towards middle income. Source: Adapted from Chomel, Belotto and Meslin, 2007. level, closer human contact with wildlife habitats, primarily caused by human population expansion into and modification of wildlife habitat, is considered a major driver in the emergence of zoonotic infections (Cunningham, 2005). At the microbial level, molecular changes may contribute to emergence, when mutation, recombination or reassortment occur or microbes switch from animal to human hosts (Morens, Folkers and Fauci, 2004). IMPACT OF EIDs EIDs are a significant threat to global public health, particularly considering that more than 25 percent of annual deaths worldwide are estimated to be directly related to infectious diseases (Morens, Folkers and Fauci, 2004). Economic losses associated with livestock morbidity and mortality threaten not only agricultural industries, but also wildlife-based economies such as wildlife tourism or the bushmeat trade (Chomel, Belotto and Meslin, 2007). Historically, wildlife diseases have been considered important only when agriculture or human health are threatened (Daszak, Cunningham and Hyatt, 2000). However EIDs are also a significant threat to species conservation and biodiversity. While wildlife species can be considered reservoirs of pathogens with the potential to infect humans and livestock, wildlife populations are themselves also threatened by introduced pathogens. Spill-over of infectious agents to wildlife populations is a particular threat to endangered species, where the presence of infected reservoir hosts can lower the pathogen’s threshold density and lead to local population extinction (Daszak, Cunningham and Hyatt, 2000). For example, white nose syndrome, an emerging fungal pathogen of hibernating bats in northeastern North America first observed in 2006, has caused unprecedented bat mortality leading to losses of up to 95 percent in some hibernacula (Blehert et al., 2009; Wibbelt et al., 2010). Another (non-bat) example of the impact of EIDs on wildlife populations is high-pathogenicity avian influenza. While low pathogenic avian influenza was probably introduced from free-ranging waterfowl into poultry, the change from low to high pathogenicity occurred in poultry and spill-back into wildlife populations. This scenario has been responsible for a population-level impact on bar-headed geese (Anser indicus), as more than 6 000 individuals died during a single outbreak at Qinghai Lake in 2005 (Chen et al., 2006; Zhou et al., 2006). BATS AND EIDs In recent years, bats have been implicated in numerous EID events and are increasingly recognized as important reservoir hosts for viruses that can cross species barriers to infect humans and other domestic and wild mammals (Calisher et al., 2006). Bats are second only to rodents in numbers of living genera and species, and are the largest order of mammals in overall abundance (Sulkin and Allen, 1974). They are unique in their vagility (potential for long-distance travel), and often aggregate in very large colonies (Turmelle and Olival, 2010). However, despite their abundance, relatively little is known about the species from which zoonotic viruses emerge to cause human disease (Calisher et al., 2006). Much of the information gathered on the role of bats in the maintenance and spread of viruses has been from species of Microchiroptera (insectivorous bats), and there is relatively little information available for members of the suborder Megachiroptera (flying foxes and fruit bats) (Mackenzie, Field and Guyatt, 2003). The role of bats in viral disease is well established (Sulkin and Allen, 1974), particularly their role as hosts for alpahviruses, flavirviruses, rhabdoviruses and arenaviruses (Mackenzie,Field and Guyatt, 2003). Calisher et al. (2006) report on 66 viruses that have been isolated from or detected in bat tissues of 74 species (Table 1.2). Some viruses have been isolated from bats of only one species, and one from bats of 14 species. There are also many viral infections for which only serological evidence is available. Perhaps one of the highest-profile EID events in recent years – for which flying foxes have been identified as the natural host – is Nipah virus, which was identified as the cause of a major outbreak of disease in pigs and humans, resulting in 265 human cases of viral encephalitis (with a 38 percent mortality rate) and the eventual culling of 1.1 million pigs (Chua et al., 2000). It is recognized that this catastrophic disease event was probably the result of several major ecological and environmental changes associated with deforestation and the expansion of non-industrial pig farming in association with the production of fruit-bearing trees. This combination created circumstances that led to the infection of pigs following indirect exposure to virus shed from fruit bats (Chomel, Belotto and Meslin, 2007). The highly infectious virus subsequently led to human cases (Daszak, Cunningham and Hyatt, 2001), most of which involved pig farmers or people associated with pig farming. Bats possess certain characteristics that may maximize their effectiveness as reservoir hosts for viruses. Natural history features such as high species diversity, long life span, the capacity for long-distance dispersal, dense roosting aggregations (colony size), social behaviours and population structure, the use of torpor and hibernation, unique immunology and spatial population structure (Calisher et al., 2006; Turmelle and Olival, 2009) have been suggested for the association of bats and EIDs. Evolutionary adaptations such as conserved their natural flying fox hosts, in whose populations they have long circulated. They remained primarily confined to these hosts until some change (or more probably sequence of changes) precipitated their emergence. As already mentioned, data on many fruit bat species suggest that populations in Australia and Southeast Asia are declining because of disruptions throughout their ranges. In Southeast Asia, anthropogenic activities (primarily habitat loss and hunting) have been identified as constituting the major threats. Deforestation for agricultural land, commercial logging or urban development is widespread, and results in loss or abandonment of roosting sites and loss of feeding habitats. Habitat loss from clearing is commonly exacerbated by tropical storms, as remnant forest is particularly prone to high wind damage. Hunting for consumption or crop protection, on both subsistence and commercial scales, results in the abandonment of roost and feeding sites (Mickleburgh, Hutson and Racey, 1992). In the scenario that emerges, flying fox populations are under stress, foraging and behavioural patterns are altered, niches expand, and livestock and humans come into closer contact. In Australia, this has been paralleled in recent decades by the geographic redistribution of flying fox camps into urban areas (L. Hall, personal communication), as the habitat loss and fragmentation associated with land-use change fundamentally alter the historical resource landscape. MANAGEMENT STRATEGIES The emergence and spread of infectious diseases in recent years has resulted in a major awakening of public health services. The involvement of veterinarians and other wildlife TABLE 1.2 (Cont.) Virus Bat species (common name) Family Paramyxoviridae, genus Rubulavirus Mapuera virus Sturnira lilium (yellow epauletted bat) Menangle virus Pteropus poliocephalus (grey-headed flying fox) Tioman virus Pteropus hypomelanus (variable flying fox) Family Paramyxoviridae, genus undetermined A parainfluenza virus Rousettus leschenaultii (Leschenault’s rousette) Family Coronaviridae, SARS coronavirus Rhinolophus sinicus (Chinese horseshoe bat), Rhinolophus pearsonii (Pearson’s horseshoe bat), Rhinolophus macrotis (big-eared horseshoe bat), Rhinolophus ferrumequinum (greater horseshoe bat) Family Togaviridae, genus Alphavirus Chikungunya virusb Scotophilus sp., Rousettus aegyptiacus (Egyptian rousette), Hipposideros caffer (Sundevall’s leaf-nosed bat), Chaerephon pumilus (little free-tailed bat) Sindbis virus Rhinolophidae sp., Hipposideridae sp. Venezuelan equine encephalitis virus Desmodus rotundus (vampire bat), Uroderma bilobatum (tentmaking bat), Artibeus phaeotis (pygmy fruit-eating bat) Family Flaviviridae, genus Flavivirus Bukalasa bat virus Chaerephon pumilus (little free-tailed bat), Tadarida condylura (Angola free-tailed bat) Carey Island virus Cynopterus brachiotis (lesser short-nosed fruit bat), Macroglossus minimus (lesser long-tongued fruit bat) Central European encephalitis virus Unidentified bat Dakar bat virus Chaerephon pumilus (little free-tailed bat), Taphozous perforatus (Egyptian tomb bat), Scotophilus sp., Mops condylurus (Angola freetailed bat) Entebbe bat virus Chaerephon pumilus (little free-tailed bat), Mops condylurus (Angola free-tailed bat) Japanese encephalitis virus Hipposideros armiger terasensis (great roundleaf bat, also known as Formosan leaf-nosed bat), Miniopterus schreibersii (Schreiber’s longfingered bat), Rhinolophus cornutus (little Japanese horseshoe bat) Jugra virus Cynopterus brachiotis (lesser short-nosed fruit bat) Kyasanur Forest disease virus Rhinolophus rouxi (rufous horseshoe bat), Cynopterus sphinx (greater short-nosed fruit bat) Montana myotis leucoencephalitis virus Myotis lucifugus (little brown bat) Phnom-Penh bat virus Eonycteris spelaea (lesser dawn bat), Cynopterus brachyotis (lesser short-nosed fruit bat) Rio Bravo virus Tadarida brasiliensis mexicana (Mexican free-tailed bat), Eptesicus fuscus (big brown bat) St. Louis encephalitis virus Tadarida brasiliensis mexicana (Mexican free-tailed bat) Saboya virus Nycteris gambiensis (Gambian slit-faced bat) Sokuluk virus Vespertilio pipistrellus (probably Pipistrellus pipistrellus, common pipistrelle) Tamana bat virus Pteronotus parnellii (Parnell’s moustached bat) (Cont.) emergence, such as habitat loss, land-use change and demographic shifts. 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