Invited reviewNavigating parasite webs and parasite flow: Emerging and re-emerging parasitic zoonoses of wildlife origin
Introduction
Historically, appreciation of the ubiquity and significance of links between infectious diseases in human and animal hosts developed slowly, and domestic animals were naturally the initial focus of interest as sources of zoonoses (Hardy, 2003). More recently, however, with ongoing discoveries of new infectious agents and diseases, it has become clear that free-ranging animals and birds are a major source of emerging human pathogens (Daszak et al., 2000).
Among the emerging and re-emerging infectious agents that people can acquire from wildlife, viruses and bacteria are the subject of intensive study because of their frequently severe clinical effects in people and because of the complexities of treatment and control. For parasites, other than major pathogens, including Trypanosoma, Leishmania and Cryptosporidium, there seems less global concern. This may be because while some of these parasites have high regional prevalence, their effects are less dramatic, with fewer sudden outbreaks involving substantial human mortality. Interestingly, of two recently published overviews of wildlife and emerging zoonoses, one included no parasites (Bengis et al., 2004), and the second mentioned only Echinococcus multilocularis (Kruse et al., 2004).
The aims of this paper are: (i) to discuss definitions of ‘emerging’ and ‘re-emerging’ as they apply to zoonotic parasites derived from wildlife; (ii) to identify parasites for which wildlife have been reported as sources of human infection; (iii) to review new information on interesting wildlife-derived emerging and re-emerging zoonoses not included elsewhere in this issue: and (iv) to review recent literature on fundamental themes for the associations between emerging and re-emerging zoonotic parasites, their human and wildlife hosts, and the ecosystems in which they co-exist.
Section snippets
Towards definitions for emerging and re-emerging
Persistent among the published definitions of ‘emerging infections’ is that from the 1992 US Institute of Medicine (IOM) report Emerging Infectious Diseases: Microbial Threats to Health in the United States, which states that they are: “those whose incidence in humans has increased within the past two decades or threatens to increase in the near future. Emergence may be due to the spread of a new agent, to the recognition of an infection that has been present in the population but has gone
Wildlife as sources of zoonotic parasites
For most of the emerging and re-emerging parasitic zoonoses reviewed in this issue, wildlife are known to be a potential source of human infection, and for some are among the more important sources (Table 1, Table 2, Table 3, Table 4). For example: cougars may have contributed to the 1994 water-borne outbreak of human toxoplasmosis in Victoria, BC (Bowie et al., 1997); wildlife are important reservoirs for human leishmaniasis (Jacobson et al., 2003) and for Trypanosoma cruzi (Rodrigues Coura et
Routes of zoonotic transmission: parasite webs and parasite flow
The presence of parasites in any ecosystem generates complex parasite webs within the system, and it is through these webs that zoonotic parasites move from wildlife to people (Fig. 1). Typically, each species of parasite has its own web, parts of which may be shared with other parasites, for example, multiple tick-transmitted pathogens infecting a host species within a geographic area. Some parasite webs include alternative transmission routes, and which of these is used in a particular
A global context
The landmark paper by Daszak et al. (2000) reviewed an array of emerging infectious diseases (EIDs) affecting people and discussed some of the mechanisms underlying emergence and the potential consequences of EIDs for human, domestic animal and wildlife health, and for biodiversity. Of the 18 EIDs identified, only three are parasitic: cryptosporidiosis, sarcoptic mange, and avian malaria. Of these only the first is considered a zoonosis of major importance, but the significance of wildlife
Drivers of emergence and re-emergence
In 2003 the IOM updated its 1992 report on emerging infectious diseases, and included 13 ‘factors in emergence’: microbial adaptation and change; human vulnerability; climate and weather; changing ecosystems; economic development and land use; human demographics and behaviour; technology and industry; international travel and commerce; breakdown of public health measures; poverty and social inequality; war and famine; lack of political will; and intent to harm (Lederberg and Morgan, 2003).
Biodiversity
A knowledge of the phylogeny of hosts and parasites, and of the history of the biodiversity of an ecosystem, can provide important clues to understanding the emergence and re-emergence of parasites and other pathogens (Brooks and Hoberg, 2000). Emerging and re-emerging infectious diseases are commonly viewed as threats to biodiversity because of their potentially erosive effects on host populations, with the risk of extirpation or extinction of host species (Daszak et al., 2000). This concern
Climate change
The scenarios proposed for global climate change, including extreme weather events, strongly suggest impacts on infectious disease, including those associated with zoonotic parasites, although the nature and magnitude of these effects will depend on the nature of the change, the parasites involved, and the region (Fayer, 2000, Patz et al., 2000, Dobson et al., 2003, Sutherst, 2001, Sutherst, 2004). Climate change may alter hosts—including vectors, as well as parasites, vegetation, abiotic
Some recent examples of emergence and re-emergence
This issue of the International Journal for Parasitology contains detailed updates for most of the major emerging zoonotic parasites transmissible from wildlife. What follows is an overview of recent reports of other such parasites that illustrate key features of emergence or re-emergence.
Disease ecology: an emerging or re-emerging science
The complexities of the relationships among infectious agents, including parasites, their human and animal hosts and the environment have renewed movement towards an all-encompassing approach to the study of infectious disease. Such an approach is sometimes referred to as disease ecology (Real, 1996), although a clear definition of this term remains elusive and it is sometimes used in a sense indistinguishable from disease epidemiology. Disease ecology is more, and implies consideration of all
Synergy for access and analysis
As already outlined, essential for success in an ecological approach to disease is synergy among key players, bringing together different perspectives and areas of expertise. This approach to the study of parasitic zoonoses in wildlife should include three special considerations. First, accessing wildlife for the collection of data and/or samples is often complex and expensive, particularly in remote areas. Other than in disease-crisis situations, biologists and others interested in the overall
Defining the parasite fauna of wildlife
Alongside the frequent difficulties in accessing wildlife, especially those that are remote or secretive, is the paucity of information regarding the host and geographic distributions of their zoonotic parasites, and the lack of validation of some of the diagnostic tests used for these infections in wildlife, particularly those based on serology. Fortunately, newer laboratory techniques show considerable promise in advancing monitoring and surveillance capabilities. For example: a coproantigen
Expect the unexpected, or the expected?
The discovery of E. multilocularis in Norway (Henttonen et al., 2001) is a good example of the surprises inherent in the study of zoonotic infectious disease in wildlife. In an analysis of the unexpected nature of emerging diseases in general, Stephen et al. (2004) applied descriptors for emerging phenomena in business: they are often unpredictable and counterintuitive; seemingly minor changes in the action of one component of the system can have profound effects on the whole system; and there
Monitoring and surveillance
Assessing the status of infectious agents, including parasites, in wildlife populations is a foundation of disease monitoring and, if subsequent intervention is planned, surveillance (Salman, 2003). Such assessments may be passive or active and retrospective or prospective. They require one or more points of assembly for wildlife disease data, on appropriate geographic scales, and ideally they should facilitate proactive detection and management of emerging and re-emerging infections and
Predictions of emergence and re-emergence
Among zoonoses transmitted from wildlife, the discovery rate of new parasites is currently low relative to new bacteria and viruses. Thus we have greater familiarity with the organisms. Despite this it is sometimes difficult to identify, in advance or with hindsight, the events leading to emergence or re-emergence of a wildlife-derived zoonotic parasite in a particular ecosystem. In some instances, an increase in the incidence of human infection or disease associated with a wildlife-derived
Public awareness
Public education can be very helpful for the prevention and control of human infections with many of the parasitic zoonoses acquired from wildlife. Usually efforts are focussed on making people aware of possible sources of the parasites and on measures to lessen or remove the risk of human infection. This type of awareness enhancement is more easily achieved in the developed world, but there are significant opportunities elsewhere. A pioneering example is the testing program for Trichinella in
Looking forward
While at present some emerging and re-emerging wildlife-derived zoonotic parasites and diseases are perhaps behind the forefront of societal concern, planning for the effective management of these diseases will result in benefits for global ecosystem integrity and for human health and well being. Identifying priorities for society's scientific resources at this complex intersection of people, domestic animals, wildlife and pathogens is difficult, but the following certainly merit attention: (i)
Acknowledgements
The development of this review benefited greatly from conversations with Dr Susan Kutz and Dr Emily Jenkins, Research Group for Arctic Parasitology, Dr Alvin Gajadhar, Head, Centre for Animal Parasitology, Canadian Food Inspection Agency, and especially with Dr Eric Hoberg, Chief Curator, US National Parasite Collection, United States Department of Agriculture.
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