Patterns of Ecological Change and Emerging Infectious Disease in the Australasian Region

An unusually rapid and widespread increase in apparently new and changing infectious diseases has occurred globally over the past four decades. This has also been a time of accelerated global ecological change. Associations between the two phenomena are unclear: emerging infectious diseases (EIDs) are reported more frequently in wealthy countries, with greater capacity for resources for surveillance and detection than less affluent centres, even though the latter are often undergoing accelerated socioecological change. Here, a series of transdisciplinary studies is reviewed that test the hypothesis that specific ecological change accounts for a significant component of the rise in EIDs in the Australasian region. Amongst the range of mechanisms, factors such as wildlife adaptation to changing landscapes and selection for antimicrobial resistance appear to be of major significance. However, exploring multi-scale complex relationships is a challenge to epidemiology. The importance of framing the scale of relationships and limitations of available data are discussed. Despite obstacles, insight into approaches to mitigating disease risk at a landscape level is expanding. Introduction – Global Patterns, Global Questions The past four decades have seen an unusually rapid and widespread increase in apparently new and changing infectious diseases in humans, domesticated animals, wildlife and plants. Some 335 novel or re-emerging infectious diseases of humans have been described since the 1940s (Jones et al., 2008). The majority of these ‘emerging infectious diseases’ (EIDs) – defined as infectious diseases Health of People, Places and Planet 462 that are novel or expanding in pathogenicity and range (Morse, 1995) – have occurred since the 1970s. The increase in EIDs has coincided with an acceleration of anthropogenic ecological change, defined as a change in interactions among living organisms with each other and with their environments, driven by the increasing global human population. Links between the two phenomena have been postulated (McMichael, 2004). The rise in EIDs has been linked broadly to changing ecosystems; climate and weather; economic development and land use; human demographics and behaviour; international travel and commerce; poverty and social inequality; breakdown in public health measures; lack of political will; intent to harm (such as bioterrorism); and the impacts of new technologies and industries (Smolinski et al., 2003). This multitude of potential influences on pathogen, vector and host(s) has also been discussed in terms of complex social–ecological systems (Wilcox and Colwell, 2005). The socioecological system perspective on disease causation reinforces a broader discussion of anthropogenic ecological change as systemic health risk (e.g. McMichael and Wilcox, 2009). Understanding the role of ecological change poses many challenges for epidemiology. Many of the speculated relationships are not easily tested. Available ecological information may describe a dynamic of interest at a scale other than that at which disease is understood, and multiple influences may act and interact across multiple scales. This chapter describes our approach to assembling a robust evidence base to understand the role of ecological change in EIDs of the Australasian region. By framing issues at appropriate scales and exploring relationships where data are available, we hope to add complexity and insight progressively. Reviews of EIDs alert us to two major areas of ecological change resulting in new human–pathogen interactions. Approximately 20 per cent of global (human) EIDs are antimicrobial-resistant (AMR) pathogens and 75 per cent are zoonoses, most from wildlife, particularly wild mammals (Taylor et al., 2001; Jones et al., 2008). A modest overlap between these two groupings also exists. The small remainder includes environmental pathogens, opportunistic pathogens (such as those affecting immunocompromised individuals) and other less easily grouped diseases. These patterns potentially tell us much about our changing ecological impact. Human influence on the selection of AMR is complex, but a direct relationship is clear. Prescriptions of antibiotics began in the 1930s and AMR was recognised shortly thereafter, steadily increasing until now, where multidrug-resistant organisms are common and widespread, including in many intensive livestock production systems (Levy and Marshall, 2004). Belatedly, research has turned to understanding the role of antibiotics and AMR in the natural systems in which they evolved. We are also only beginning to understand the lability and significance of environmental contamination with human and animal 26 . Patterns of Ecological Change and Emerging Infectious Disease in the Australasian Region 463 drug-resistant organisms (Finley et al., 2013). Similarly, there are many issues surrounding the rise in anti-fungal, malarial, parasitic and viral resistance, and in vectorcidal resistance following their widespread use. The relationship between the rise in (wildlife) zoonoses and anthropogenic ecological change is less obvious. The traditional view of zoonotic and crowd diseases arising from ancient humanity’s shift to densely populated agrarian settlements with domesticated animals (e.g. McNeill, 1976) sheds little light on the rise, now, of zoonotic pathogens of wild animals. There is a reported positive association between high mammal diversity, human density and zoonotic infectious diseases of wildlife origin (Jones et al., 2008; Morand et al., 2014), but it is difficult to undertake detailed global assessments. Data on EID emergence are usually more comprehensive in developed temperate regions, as are data on many other potential explanatory variables (such as the role of ecological and sociodemographic parameters). Exploring the importance of ecological change as a driver of EIDs is complicated by many factors. Advances in diagnostic technology, surveillance, fundability of research and even digital search engines have had (incompletely quantified) influence on the number of EIDs reported. According to one study, reporting of EIDs peaked in the 1980s (once the underlying reporting bias for papers from less-developed countries (LDCs) was addressed). This was a decade associated with taxonomical reclassification and diagnosis of novel co-infections with HIV/ AIDS (Jones et al., 2008). The rise in numbers of EIDs is not necessarily accompanied by an increase in the burden of disease. HIV/AIDS is unique in its combined novelty, significance and the proliferation of novel co-infections recognised during and since the 1980s. Many other EIDs are of minor or only potential population health importance, or of importance primarily for their scientific novelty, a fact that undermines research on novel EIDs in countries struggling to address other major health impacts (Butler, 2012). Many of the most important human EIDs (e.g. multidrug-resistant tuberculosis and malaria) are old scourges with new twists. HIV/ AIDS also illustrates the lag period that may follow ecological changes, and the spatially and temporally dispersed social changes that may result in infectious disease emergence. For this disease, the events that led to ancestral virus spilling from non-human primates to humans appear to have occurred in the early 20th century (or perhaps even prior to this) (Sharp et al., 2001). Social and demographic changes in the late 20th century gave rise to a global pandemic. Even as a signal of ecological change, human EIDs only tell part of the story. EIDs of plants and animals not involved in human disease transmission receive much less research and reporting effort, but are also a feature of recent decades. Wheat rust Ug99, white spot baculovirus syndrome of shrimp and Health of People, Places and Planet 464 porcine respiratory and reproductive syndrome are examples of EIDs that have arisen from, and caused collapse in, intensively produced human food production (Singh et al., 2011; Wang et al., 2006; Zhou et al., 2008). Intensive livestock production has proven to be a highly effective amplifier of zoonotic disease (Liverani et al., 2013). Infectious diseases of wildlife are also emerging in vulnerable species, degraded ecosystems and where least expected. The pandemic amphibian chytridiomycosis is responsible for multiple species extinctions even in pristine habitats; Tasmanian Devil Facial Tumour has decimated its marsupial carnivore host, a species not long ago regarded as a pest. Although there has been a vigorous literature on EIDs as a global phenomenon in a changing world, our understanding is biased to one host (humans) and to well-resourced developed countries. Patterns of EIDs in the Australasian Region To examine the hypothesis that ecological change accounts for a substantial component of the rise in zoonotic EIDs, a series of transdisciplinary studies based on the Australasian region were designed by the author under the doctoral supervision of Professors Tony McMichael and Adrian Sleigh and Dr Peter Black (McFarlane et al., 2011, 2012, 2013, 2014). These studies reflected Tony’s support for research that explored the awkward, important issues, and for epidemiology that – in an inventive and insightful way – sought to address these challenges. The postulated drivers of EIDs examined in these studies have a history and forward trajectory, and cannot be considered in isolation from other processes. In this way, each study contributed detail to the complex systems perspective of socioecological change as a health risk that Tony’s work brought to global research. The EID literature for Australasia is dominated by reports published by the sparsely populated, developed country, Australia. The region also includes smaller, developed New Zealand and the developing Melanesian nations. This region adjoins that of the adjacent, densely populated, rapidly developing Southeast Asia and