Environment International 48 (2012) 56–64

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Review

Cooling off health security hot spots: Getting on top of it down under

Kris A. Murray a,b,⁎, Lee F. Skerratt b,⁎⁎, Rick Speare b, Scott Ritchie b, Felicity Smout b,Robert Hedlefs c, Jonathan Lee d

a EcoHealth Alliance, 460 W34th St, 17th Floor, New York, New York, 10001, USAb School of Public Health, Tropical Medicine and Rehabilitation Sciences, James Cook University, Townsville, Queensland, Australiac School of Veterinary and Biomedical Sciences, James Cook University, Townsville, Queensland, Australiad Animal Biosecurity and Welfare, Biosecurity Queensland, Department of Agriculture, Fisheries and Forestry, 203 Tor St, Toowoomba Qld 4350, Australia

⁎ Correspondence to: K. Murray, EcoHealth Alliance,York, New York, 10001, USA. Tel.: +1 212 380 4492.⁎⁎ Corresponding author. Tel.: +61 7 4781 6065.

E-mail addresses: murray@ecohealthalliance.org (Klee.skerratt@jcu.edu.au (L.F. Skerratt).

0160-4120/$ – see front matter © 2012 Elsevier Ltd. Alldoi:10.1016/j.envint.2012.06.015

a b s t r a c t

a r t i c l e i n f o

Article history:Received 28 November 2011Accepted 23 June 2012Available online xxxx

Keywords:BiosecurityEnvironmental healthOne HealthConservation medicineEmerging infectious diseasesInvasive species

Australia is free ofmany diseases, pests andweeds found elsewhere in theworld due to its geographical isolationand relatively good health security practices. However, its health security is under increasing pressure due to anumber of ecological, climatic, demographic and behavioural changes occurring globally. North Queensland isa high risk area (a health security hot spot) for Australia, due in part to its connection to neighbouring countriesvia the Torres Strait and the Indo‐Papuan conduit, its high diversity of wildlife reservoirs and its environmentalcharacteristics. Major outbreaks of exotic diseases, pests and weeds in Australia can cost in excess of $1 billion;however, most expenditure on health security is reactive apart from preventive measures undertaken for a fewhigh profile diseases, pests and weeds. Large gains in health security could therefore bemade by spending moreon pre-emptive approaches to reduce the risk of outbreaks, invasion/spread and establishment, despite thesegains being difficult to quantify. Although biosecurity threats may initially have regional impacts (e.g. Hendravirus), a break down in security in health security hot spots can have national and international consequences,as has been seen recently in other regions with the emergence of SARS and pandemic avian influenza. Novel ap-proaches should be driven by building research and management capacity, particularly in the regions wherethreats arise, a model that is applicable both in Australia and in other regions of the world that value and there-fore aim to improve their strategies for maintaining health security.

© 2012 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 562. Evidence for increasing risk and endemic emergence of diseases, pests and weeds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 573. Australia's unique health security status and risk pathways . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 574. Risk pathways and high risk regions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 585. Costs of health security . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 606. Estimating the cost of invasive diseases, weeds and pests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 617. The benefit of research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 618. Solutions to better mitigate current and future risks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 639. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63Appendix A. Supplementary data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63

460W34th St, 17th Floor, New

.A. Murray),

rights reserved.

1. Introduction

Australia remains free of many of the invasive diseases, pests andweeds that are detrimental to global health and that limit trade andfood security elsewhere. This suggests that Australia's biological border

57K.A. Murray et al. / Environment International 48 (2012) 56–64

security (biosecurity) has been relatively effective in the past. It alsosuggests that ongoing pre-emptive protection from diseases (human,agricultural, livestock and wildlife), and by extension invasive pestsand weeds, is an achievable and worthwhile target for Australia intothe future.

Likemany countries, however, Australia faces significant and ongoinghealth security risks. This has been repeatedly demonstrated by the re-cent incursion, emergence or re-emergence of multiple diseases, includ-ing those affecting humans (e.g., pandemic influenza, dengue, Hendra),livestock (equine influenza, abalone virus), agriculture (citrus canker,cane smut) and wildlife (chytridiomycosis, devil facial tumour dis-ease), in addition to numerous marine and terrestrial weeds andpests (e.g., black-striped mussel, northern pacific seastar, branchedbroomrape, Siam weed, red imported fire ants, papaya fruit fly)(e.g., Mackenzie et al., 2001; Prowse et al., 2009; Skerratt et al.,2007). All of these have incurred significant economic, social and/or en-vironmental costs for Australia (e.g., Prowse, 2006; Robertson, 2003;Taylor et al., 2008).

There are changing ecological, climatic, demographic and behaviouralfactors that combine to continually expose the continent to globally sig-nificant emerging or invasive threats. In response, Australia must beginto contemplate and confront the effects of the vast global changes thathave occurred and will occur in response to habitat degradation, biodi-versity loss, population growth, climate change and increases in the vol-ume of international trade and traffic (Pongsiri et al., 2009; Tatem et al.,2006). In addition, Australia will inevitably have to move away from atraditional insurance-based approach to risk, whereby intervention is re-active and occurs at the level of the affected population, and move in-stead towards an approach of pre-emption and preparedness (Wraithand Stephenson, 2009). The key to effective preparedness is a better un-derstanding of the factors that are implicated in the incursion and emer-gence of invasive species and diseases (e.g., Jones et al., 2008). Anappreciation of the economic advantages of pre-emptive research, sur-veillance, data analysis and intervention over post-invasion reactive re-sponses is also important, particularly in sectors controlling fundingallocation, decision-making and policy development (Prowse, 2006).

This shift in strategy could be underpinned by a new paradigm inglobal preparedness research that has itself recently emerged; the ‘OneHealth’ concept that recognises that common factors govern or drivethe emergence of new and recurring biological threats across differentsectors (Daszak et al., 2000). There is now a strengthening recognitionthat a collective consideration of these factors is critical to future successin preparedness for wildlife, food, animal and human disease manage-ment (Enserink, 2007). Nowhere is this One Health concept better illus-trated than by the suite of trans-boundary diseases that involve wildlife,domestic animals and humans (e.g., Henipah viruses, filoviruses, SARS,swine flu). This concept logically extends to the treatment of otherthreats such as invasive pests and weeds. Management requirementsin these cases are necessarily multidisciplinary. A combined effort di-rected towards the common underlying drivers of invasion and emer-gence promises to be more efficient and cost-effective for successfulpre-emptive intervention and preparedness (Daszak et al., 2000).

When backed by adequate research, a OneHealth approachwill pro-vide insights to the mechanisms of emergence and incursion. The bene-fits of this approach are thus shared across traditionally isolated fields(e.g., human, domestic animal and wildlife health, invasive pests andweeds) and the inclusive management of the full spectrum of invasivespecies and pathogens should improve the protection of national healthsecurity. The approach specifically involves improved management andsharing of relevant biosecurity information, cross-sectoral developmentof laboratory infrastructure, new cross-jurisdictional policies and newmultidisciplinary approaches to invasive species and disease research(Prowse et al., 2009).

In this review, we address Australia's health security needs in thecontext of a OneHealth approach.We extend the concept fromone lim-ited to diseases (human, livestock, agriculture and wildlife) to include

the health security of the environment at large by also considering theimportance of invasive weeds and pests. We first review the evidencethat risks to health security are increasing globally and locally. Wethen scrutinise Australia's perceived uniqueness (in terms of its naturalresilience and capacity to defend its borders from new invasions andpathogens) as something worthy of increased and ongoing investment.We next characterise the high risk region (in terms of incursion andemergence risk) of northern Australia/Queensland to demonstratewith a case study the importance of managing risk pathways and thecritical need for targeted, local investment. We close by providingsome solutions and specific recommendations for ways forward in a re-source limited world when confronted with the challenge of improvingapproaches to health security. In doing this, we review how economicand social motivations may help to underpin a One Health modelfrom a governance and administrative perspective. We argue that pro-moting an agenda of increased investment in research (even in theface of uncertainly quantified benefits) is the key to preparedness andeffective response and could considerably improve efficiency in healthsecurity spending. This model is applicable both in Australia and inother regions of the world that value and therefore aim to improvetheir strategies for maintaining human and environmental health.

2. Evidence for increasing risk and endemic emergence of diseases,pests and weeds

In recent years, numerous examples implicate Australia's health se-curity. Our intention is not to provide a comprehensive review on recentinvasive or emergent pests and diseases (see e.g., Prowse et al., 2009),but to draw attention to some of the key issues. The reality of ongoingdisease threats has been demonstrated by several recent outbreaksthat have had a substantial impact on health security in Queensland.Dengue, Hendra virus, Australian Bat Lyssavirus and equine influenzahave caused human and domestic animal morbidity and mortality andresulted in substantial public and veterinary health expenditure. Dengue,Barmah Forest and Chikungunya cases are all on the rise nationally(Fig. 1). Other examples of some of the more significant diseases thathave affected Australia include Menangle virus, abalone herpesvirusand Japanese encephalitis (Prowse et al., 2009; Table 1).

There have also been significant disease impacts on biodiversity.Chytridiomycosis, a disease linked with movement of infected animalsthrough trade routes globally has caused the extinction of several am-phibian species in Queensland and is threatening the survival of manymore (Berger et al., 1998; Murray et al., 2011; Skerratt et al., 2007).Similarly, although causes for its emergence remain obscure, Tasmaniandevil facial tumour disease (DFTD) has had dramatic population level im-pacts resulting in elevated extinction risk for this iconic species (Lachishet al., 2007).

These emergence events coincide with evidence that human activi-tiesmaypromote the emergence or spread of infectious diseases throughthe large-scale modification of natural environments and by increasingglobal connectivity. Increasing rates of endemic disease emergencewith-in the south-east Asian/Pacific region aswell as within Australia could bedue to a range of factors, such as population growth, increasing urbanisa-tion and agricultural expansion causing changes in the ecology ofwildlifedisease reservoirs and enhanced opportunities for disease spillover(e.g., the emergence of Hendra virus from flying foxes in Queensland;Plowright et al., 2011). The initial impacts of these changes on risk areoften subtle and not recognised in periodic assessments until significantdisease is apparent. Therefore, we need to better understand the driversof emergence in order to successfully mitigate this risk.

3. Australia's unique health security status and risk pathways

Australia's assemblage of human infectious diseases is demonstra-bly unique. From an assemblage similarity perspective (i.e., how dis-eases present in one country statistically relate to diseases in other

Fig. 1. Number of Australian cases of dengue, chikungunya and Barmah Forest virus infections 1991–2011 (Source: National Notifiable Diseases Surveillance System: http://www9.health.gov.au/cda/Source/CDA-index.cfm). The majority of dengue and all chikungunya are imported cases, indicating weaknesses in screening and border security and potentialincreases in disease incidence overseas. Barmah Forest virus is endemic, with increases potentially due to increasing suitability of conditions for disease emergence or better de-tection techniques.

58 K.A. Murray et al. / Environment International 48 (2012) 56–64

countries), Australia sits in distinct isolation from other countries inSouth-east Asia and the Pacific region (see Appendix S1 for analysisdetails). This suggests that unique natural or artificial barriers todisease flow are in place that limit the sharing of diseases evidentregionally and beyond.

This analysis also highlights some potential mechanisms relevant tobiosecurity by shedding light on potential risk pathways. For example,geographic clustering is most evident for the large number ofvector-borne and zoonotic diseases (the latter being the group fromwhich the majority of new emerging infectious diseases affectinghumans arise; Jones et al., 2008). This suggests that an informative pre-dictor of what vector-borne and zoonotic diseases a countrywill harbouris the disease assemblage of its neighbours. We might expect the same‘biogeographic’ principles to apply to other forms of invasive species

Table 1Examples of new and emerging diseases in Australia (reproduced from Prowse et al.,2009; references therein).

Disease/agent Date ofoutbreak(s)

Zoonosis Wildlife involved

Avianinfluenza

1976–1997 Yes Possibly wild waterfowl

Dengue 1981–2008 No NoHendra virus 1994–2008 Yes Bats (Pteropus spp.)Pilchardherpesvirus

1995 No Pilchards (Sardinops sagax neopilchardus),probably novector

Australian batlyssavirus

1995 Yes Bats

Japaneseencephalitis

1995 Yes Possibly domestic and feral pigs

Menanglevirus

1997 Yes Bats

Chytridfungus

1998 No Amphibians

Devil facialtumourdisease

2002 No Tasmanian devil (Sarcophilusharrisii), probably no vector

Porcinemyocarditis

2003 No No

Leishmania 2004 No MacropodsAbaloneherpesvirus

2005 No Wild abalone (Haliotis spp.)

Equineinfluenza

2007 No No

(Reperant, 2010), such as weeds and animal pests that may dispersesubject to similar underlying drivers (e.g., wind, ocean currents, animalmigration) (Lonsdale, 1999). Relevant biosecurity risks and theirunderlying mechanisms of dispersal may thus be identified ahead ofnew incursions, improving the ability to prevent and respond.

A significant part of Australia's health security riskmay thus be quan-titatively attributable to the diseases, pests and weeds that occur in itsneighbouring countries. Australia's vector-borne diseases of humans,for example, are most similar to those found in Papua New Guinea(PNG) (Appendix S1, Fig. S1b), so it follows that diseases emerging inor invading PNG pose a relatively higher risk for Australia's health secu-rity than diseases present or emerging in more distant countries andcontinents. Health security for Australia may therefore be justifiablymanaged not at a national border-oriented level, as has been traditional-ly the case (Beale et al., 2008), but rather more holistically and at the re-gional level where specific mechanisms and pathways of invasionrequire additional consideration. This regionally collaborative approachis likely to have significant cross-border appeal for its potential to allevi-ate the burden of border protection that is currently the sole responsibil-ity of individual countries that are immediately threatened (e.g., seeGeorganas, 2010). There is a growing realisation that threats to healthsecurity start well before reaching the border.

4. Risk pathways and high risk regions

The Australian landmass is not homogenous with respect to the riskof invasion by invasive pests, weeds and diseases. This is not surprisinggiven themultitude of risk factors for disease, weed andpest emergenceand invasion. These include humandemographics and behaviour, socio-economic status, population growth, land-use patterns and encroach-ment, biodiversity loss, frequency and volume of international traffic/trade (e.g., cargo ships and planes), climate and other environmentalfactors (temperature, rainfall, winds and ocean currents), geographicfactors (e.g., distance to neighbours), the presence or potential presenceof vectors, wildlife host richness and so on (Jones et al., 2008; Lonsdale,1999; Morens et al., 2004; Pongsiri et al., 2009; Tatem et al., 2006;Taylor et al., 2001; Westphal et al., 2008). Further, these risk factorsmay not only vary and interact temporally and spatially, but also acrossvarious taxa (e.g., the relative importance of key risk factorswill vary forinvasive marine species vs invasive terrestrial species). Despite thiscomplexity, some generalisations for Australia can be derived.

Northern Australia is considered particularly vulnerable to pests anddiseases that could enter from neighbouring countries to the north.

59K.A. Murray et al. / Environment International 48 (2012) 56–64

Migrating wildlife, human activities and wind currents can carry pestsand vectors to Australian shores from these countries, potentiallyusing islands as stepping-stones. Australia's northern coastline is vastand sparsely populated,making it vulnerable to undetected foreign ves-sels that by-pass the usual quarantine checks at Australian borders(http://www.daff.gov.au/aqis/quarantine/naqs).

Northern Australia Quarantine Service (NAQS) risk assessments sug-gest that risk of invasion of human and animal diseases, pests andweedsis not homogenous evenwithin the high risk zone of northern Australia.The area of northern Australia subject to NAQS activities is broken into anumber of surveillance zones, with risk ratings that correspond to fac-tors of invasion, such as pathways, geography, human population densi-ty and host populations. The overall level of risk is evaluated for eachzone and depends upon the above mentioned factors. However, thelevel of risk may be modified by the level of investment in prophylacticsurveillance (i.e., the frequency of surveys). In this context, the regionconsidered to be at the greatest risk from exotic animal disease incur-sions is the west coast of Cape York Peninsula in Queensland (Fig. 2)(NAQS, 2004). Following this are a number of high risk zones in coastalregions of the Northern Territory and other parts of the Queenslandcoast.

In light of the analysis presented inAppendix S1 andNAQS risk assess-ments (Fig. 2), the Indo‐Papuan conduit clearly presents a major riskpathway for entry of many exotic diseases and pests to the Australiancommunity. Indeed, a number of exotic pathogens are already onAustralia's doorstep, including multi drug resistant tuberculosis(MDRTB), rabies, chikungunya, avian influenza H5N1, classical swinefever, screwworm fly and surra. An outbreak of rabies killing 16 peoplehas been recently reported in Pulau Larat in the Tanimbar Islands,Maluku Province, Indonesia. After earlier outbreaks in Bali and Flores(Susetya et al., 2008), rabies appears to be expanding eastwardsthrough Indonesia at an unpredictable rate and must now be consid-ered a genuine threat to West Papua, Papua New Guinea and Australiawhere native and domestic dog varieties are very widespread. The out-break in Bali provides a sobering example of how this disease canspread rapidly from the introduction of a single infected but subclinicalanimal.

Fig. 2. Northern Australia Quarantine Strategy (NAQS) animal health area risk ratings. Areas(red shade).

Themain risk pathways relevant to this area include human and an-imal movements, environmental drivers including wind and ocean cur-rents, and proximity of land masses for island hopping. Fruit bats ofmultiple species, for example, are known to be hosts for Nipah andHendra viruses (two recent emerging infectious diseases in South-eastAsia and Australasia with serious public health implications) and havebeen observed making long distance movements across internationalboundaries between Indonesia, Papua New Guinea and Australia(Breed et al., 2010). Bats have also been implicated as potential reservoirhosts for other zoonotic diseases suchas SARS, Japanese encephalitis andEbola. Nomadic waterfowl could act as effective hosts and vectors fordiseases such as highly pathogenic avian influenza (East et al., 2008).Wind patterns could play a role in the dispersal of a number ofhaemotaphagous insects, such as midges and mosquitoes, to Australiafrom PNG (Johansen et al., 2003). These insects may be efficient vectorsfor a variety of significant human and animal diseases, such as malaria,Japanese encephalitis, dengue and bluetongue.Windmay also be impli-cated in the spread of some plant diseases (Davis et al., 2002), pests suchas spiralling whitefly (Lambkin, 1998), papaya fruit fly (Pike andCorcoran, 1998) and multiple sugar cane pests (Anderson et al., 2009).Ocean currents are important for some marine pest species (Dennis etal., 2001).

Mechanisms aside, several highly significant viruses and mosquitovectors have been carried recently on the ‘conduit’ and subsequentlyrecorded from within Australia (Table 2). Similarly, the movement ofpeople across international borders along the Indo-Papuan conduit insome cases is likely to have already lead directly to the incursion of dis-eases into Australia. Examples include MDRTB (Gilpin et al., 2008) andmalaria (Merritt et al., 1998). Under the Torres Strait Treaty residentsof designated villages in PNG and Torres Strait canmove relatively free-ly across the international border (DFAT, 2009) (animal movement isrestricted by Australian quarantine legislation (DEWHA, 2009)). The in-adequate health infrastructure and non-existent veterinary infrastruc-ture in the south of the Western Province in PNG contribute to thelack of control of communicable disease in this critical area. As fore-shadowed above, a suite of significant emerging infectious diseases isknown to be present in PNG, Papua and other parts of Indonesia.

of highest risk are concentrated on the west coast of Cape York Peninsula in Queensland

Table 2Incursions of mosquito vectors and vector-borne diseases of significance into Australia via the Indo-Papuan conduit (see text for description).

Vector/virus Pathogens vectored Date of incursions Reference

Culex gelidus Japanese encephalitis virus, RossRiver virus

Before 1995 Muller et al. (2001), van den Hurk et al. (2001), Ritchie (unpublisheddata).

Aedes albopictus Dengue, chikungunya, possiblyRoss River

2004 ongoing invasions in Torres Moore et al. (2007), Ritchie et al., (2006), Russell et al. (2005), N Beebe(unpublished data)

Japaneseencephalitis virus

1995, ongoing invasions in Torres1998, 2004 Cape York

Hanna et al. (1996, 1999), van den Hurk et al. (2006), van den Hurk etal. (2009)

Dengue viruses 1997, 2004 Torres St to Cairns, Townsville2005 Torres St.

Hanna et al., (1998, 2006)

Malaria 1989, 2003, Harley et al. (2001), Qld. Health, unpublished data

60 K.A. Murray et al. / Environment International 48 (2012) 56–64

These include HIV, MDRTB, HPAI H5N1 (East et al., 2008), chikungunya(Laras et al., 2005), rabies (Susetya et al., 2008), Japanese encephalitis(Mackenzie et al., 1997; Ritchie et al., 2007) and Nipah virus (Field etal., 2001). In addition, PNG and Papuan wildlife have an immense po-tential to yield novel infectious agents, potentially capable of becomingemerging infectious diseases of humans and other animals (Mackenzieet al., 2001).

The area of highest risk as assessed by NAQS is the west coast of CapeYork Peninsula and in general Queensland is at higher risk than otherstates (Fig. 2). Queensland records the majority of cases nationally formany key diseases including dengue and malaria (Table 3), and it alsoappears to host the highest number of invasive species for any Australianstate (Table 4). However, much of North Queensland is rural and remote,with attendant challenges for the timeliness of detection of diseaseand pest incursions. Receptivity for dengue, an important globalre-emerging infectious disease, is unique in the Australian context. Twomosquito vectors for dengue are now found in north Queensland. Aedesaegypti is well established and will spread as local governments legislatefor household water tanks (Kearney et al., 2009; Russell, 1998). Aedesalbopictus is a newly arrived dengue vector, now established in TorresStrait and moving south (Ritchie et al., 2006).

On the Australian side communicable disease surveillance systemsexist for humans and livestock, but timeliness is a challenge. Other ani-mals, including pets and wildlife, are arguably very poorly monitoredfor disease. In addition, communication between the health and animalindustry surveillance systems is poor and largely dependent on individ-uals, not on systemic structures. High level laboratory support for clini-cians to investigate unknown human or animal syndromes is available,but up to 2200 km south of where clinical cases may occur.

Due to enhanced trade and tourism, the Indo-Papuan conduit mayplay an even bigger role for Australia's health security in the future. Assuch, the health security of Australia is fundamentally dependentupon the level of knowledge, interaction and capacity of the healthinstitutions and biosecurity bodies resident or working at thePNG-Australia interface (and beyond regionally). A local focus is thusextremely important but currently lacking.

Table 3Overseas-acquired malaria cases, Australia 1 July 2008 to 30 June 2009, Plasmodiumspecies and state or territory.

Plasmodium species State or territory Aust Type%

ACT NSW NT QLD SA TAS VIC WA

Plasmodiumfalciparum

2 41 10 80 11 6 32 49 231 41%

Plasmodium vivax 6 63 8 94 11 2 73 21 278 49%Other Plasmodiumspecies

1 7 1 6 0 1 2 4 22 4%

Mixed Plasmodiumspecies

0 0 1 0 2 0 5 5 13 2%

Plasmodium species 0 0 0 20 0 0 1 2 23 4%Total 9 111 20 200 24 9 113 81 567

5. Costs of health security

Maintaining health security (whichwe define as including the healthof humans, domestic animals, agricultural plants and crops, wildlife andthe environment) is extremely expensive. Considering only humanhealth as an example, Australia spent $44.6 billion on health care in2000–01 (comprising hospital and out-of-hospital costs, aged carehomes, pharmaceuticals and research, but excluding costs attributed tosigns, symptoms. ill-defined conditions and other contact with thehealth system) (AIHW, 2005). In 2002, the total annual burden of diseaseand injury from all sources was estimated to be 9216 age-standardizeddisability adjusted lost years (ag-st-DALYs) per 100,000 population(WHO, 2004), representing roughly 206 DALYs per $1 billion across alldisease categories. Expenditure in this sense can be seen as a directmea-sure to combat the overall DALY burden. Equality in combating diseaseburden for each subcategory of disease may thus be evaluated relativeto the overall community burden. Ideally, expenditure would be propor-tional to burden. Although cost-efficiency of interventions may differamong categories for a number of reasons (e.g., social values that encour-age spending in sectors that haveminimal burden in terms of deaths anddisability such as skin diseases, or investment in the use of expensiveand/or experimental technologies), where expenditure is high relativeto the overall burden, suboptimal investment may currently be present(these were the most recent congruent data we could identify).

For infectious and parasitic diseases, expenditure was $1.2 billion inAustralia in 2000/01, whereas burden was estimated to be 184 DALYs(153 DALYs/$billion). Hence, expenditure on infectious and parasiticdiseases in that period in Australia represented a relatively unbalancedinvestment in terms of money spent combating the overall burden ofdisease when all sources of mortality and disability are considered. Ar-guably, over-expenditure in this disease categorymay be better spent inone or several other categories (e.g., neuropsychiatric illness, malignantneoplasms, injuries, respiratory diseases, perinatal conditions and con-genital anomalies) that incur relatively higher burden of disease butwhich may currently suffer from relative under-expenditure.

What then can be made of investment into infectious and parasiticdiseases and how does this relate to health security in Australia? TheWorld Economic Forum considers pandemics and infectious diseases

Table 4The number of invasive species per Australian state recorded in the Global InvasiveSpecies Database (GISD) (http://www.issg.org/database/welcome/). This is not acomprehensive list of all invasive species but should be indicative of general trends.The total number of invasive species recorded for Australia in the GISD is 223. Asmall number of species may be represented in two or more ‘Invasive type’ categories.

Invasive type State or territory

ACT NSW NT QLD SA TAS VIC WA

Alien 16 87 39 99 37 60 77 67Biostatus uncertain 0 1 0 2 0 0 0 0Native 1 17 8 22 6 8 8 11Native‐non-endemic 0 0 2 4 1 0 1 2Not specified 0 2 3 6 1 0 1 4Total 17 107 52 133 45 68 87 84

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as major risks in terms of the magnitude of potential economic loss totheglobal community over thenext 10 years. They estimate that togeth-er pandemics and infectious diseases could (5–10% likelihood) cost$500 billion–$2 trillion US (WEF, 2010). Similarly, concordant with theeconomic consequences, such events could incur dramatic health andsocial costs, which has of course already played amajor role in the shap-ing of human history (Morens et al., 2004). Likemany uncertain risks, inthe case of an emergency the costs of combating pandemics and infec-tious and parasitic diseases could clearly skyrocket over an extremelyshort period of time.

In the event of a serious disease outbreak of public health concern, forexample, Australia can be expected to suffer substantial economic costs,even where the event occurs well beyond its own borders. This wasdemonstrated recently with the outbreak of SARS. Although minimalcompared to China, Hong Kong and Taiwan, SARS caused economiclosses to Australia via a number of indirect routes, such as its effect onservices-related business including cancelled and postponed businessand leisure tourism, impacts on education revenue (including reductionof international student numbers), and losses from softeneddomestic de-mand for key markets such as live crustaceans, fish, dairy, meat produceand fresh fruit (Robertson, 2003; Treasury, 2003).Where diseases breachAustralia's borders, eradicable diseases continue to incur high short termcosts while non-eradicable diseases also incur ongoing costs. The directand indirect costs of any major disease incursion into Australia have his-torically exceeded $1 billion regardless of the disease (see below). This isequivalent to the total expenditure on infectious and parasitic diseases inAustralia in 2000–01. Costs associatedwith anoutbreakwill thus increasevery rapidly with little return in terms of reducing the overall existingburden of disease in the community, a poor outlook for a sector thatmay already be attracting disproportional expenditure.

6. Estimating the cost of invasive diseases, weeds and pests

Putting a price on outbreaks of diseases, pests and weeds is difficultbut necessary for sectors controlling funding allocations, decision-making and policy development. The cost of an incursion of an undesir-able invasive species or pathogen into Australia varies widely and affectsdifferent sectors (Prowse, 2006) and has been achieved for only a few se-lect events. Foot and Mouth Disease (FMD), for example, has had ex-tremely serious impacts in other countries. The spectacular UKoutbreak in 2001 resulted in 2030 cases, the culling of 6 million animals,and economic losses of around $19 billion (AUD) to agriculture, the foodchain and costs associatedwith compensation and clean-up of destroyedanimals. Australia is currently considered FMD-free, but the expectedcost of a single FMDoutbreak inAustralia has been estimated at $2–3 bil-lion, while a worst case scenario full incursion would cost $8–13 billion,with consequences lasting for up to 10 years (DAFF, 2009; Doran andLaffan, 2005).

Another reasonably well characterised example is the expected costof an influenza epidemic in humans arising from the current avian influ-enza pandemic. Avian influenza could have dramatic implications forpublic health if it were to become pandemic in humans and exhibit thecharacteristics of some of the past influenza pandemics (e.g., the1918–19 ‘Spanish flu’ outbreak) (Longini et al., 2005). Estimates of im-pact range according to severity of the outbreak scenario— for amild out-break, global losses are expected to be around 1.4 million lives and 0.8%of GDP ($330 billion US). The predicted impact on the Australian econo-my ranges from0.8% to 10.6% of GDPwith human losses of 2100–214,200lives for amild and ultra outbreak, respectively (McKibbin and Sidorenko,2006).

As a result, the Australian government has recognised that, for a fewselect diseases, the expenditure of funds beyond its borders representsa potentially high return on investment, with significant resources nowcommitted to building capacity in neighbouring countries in the regionand in international disease bodies such as the World Organisationfor Animal Health (OIE). It is surprising that similar rationale is not

commonplace for other diseases, invasive pests and weeds whose com-bined economic burden vastly exceeds that of any one disease (furtherexamples of invasive invertebrate pests (red fire ants, papaya fruit fly)and weeds can be found in Appendix S2).

7. The benefit of research

The cost of disease, pest and weed outbreaks and incursions can bereduced through planning for a response, improving response capacityand risk mitigation (Prowse, 2006). Research plays a key role in thesetasks but in reality the benefits of improved disease detection, controland response are hard to pinpoint and quantify. It is clear that researchin the laboratory and the field can result in improved tools andmethodsto detect disease and invasive species, reduce public health costs andthe preservation and growth of market access in the agricultural sector(Prowse, 2006). Coordinated collection of surveillance information willenhance surveillance strategies and aid in the demonstration of free-dom from disease and invasive species and promote early detection ofoutbreaks. Research also improves disease control in neighbouringcountries, which further adds to Australia's health security throughriskmitigation. In addition, the social effect of a disease incursion is psy-chological stress and a concomitant loss of confidence in governmentpolicy on quarantine. This is closely followed by calls for an increasedscientific effort to prevent future incidents (Beale et al., 2008; Tayloret al., 2008). Recent pandemics such as avian, equine and swine influen-za have brought this issue to the forefront of the national conscience(Wraith and Stephenson, 2009), which should have ramifications fornational policy/legal infrastructure and funding allocations.

In general, however, Australia invests poorly inmaximising the ben-efits of research in preparedness and response (Russell, 1998). To returnto a previous example, of the $1.2 billion spent by Australia on infec-tious and parasitic diseases in 2000–01, around 89% was spent on reac-tive measures (hospitalisation, pharmaceuticals etc.,) while only 11%was spent on research (AIHW, 2005), very little of which is likely tohave been invested in effective prevention strategies.

One key problem that may be limiting investment is that realisticallyascribing economic value to improved preparedness and the subsequentreduction in risk remains a challenge. Market drivers for investing in re-search outcomes are lacking, particularly in the public health arena(Prowse, 2006). Estimating the benefits of research that reduce the riskof outbreaks of diseases, weeds or pests depends on the likelihood ofan incursion or outbreak, its expected impact and costs, the relative con-tribution of research in reducing that risk, the clear identification of theresearch and its progenitors, the uptake of the research, and its contribu-tion to consequent reductions in risk and expenditure. In some cases, thebenefit ascribed to reduced risk as a result of the research could be recur-rent. Risk profiles may also be influenced by the international environ-ment. For example, the continued pandemic of avian influenza in birdsand spill over into humans increases the risk that it will start spreadingamong humans (Prowse, 2006).

However, if generic pre-emptive research and preparedness canclearly provide long term savings in terms of reducing the overall bur-den of diseases and invasive species, then deconstructing the benefitsof research into any one significant disease or pest in order to providea base-level motivation for sequestering further funding may becomeredundant. Taking amore holistic approach to health security, wherebythe common drivers of incursion and emergence can be efficientlytargeted across traditionally isolated sectors, could confer real economicand practical advantages when adopting a One Health approach to na-tional health security.

Evidence to support the uptake of these newapproaches is neverthe-less required. Longini et al. (2005) show that sufficient preparednesscould, under certain epidemiological conditions, contain an outbreakof pandemic HPAI in humans at its source. The benefit of preventingeven a mild pandemic could exceed $300 billion (US) (McKibbin andSidorenko, 2006). An Australian example where the benefits of research

62 K.A. Murray et al. / Environment International 48 (2012) 56–64

might be directly quantifiable is the detection of the Philippines fruit fly(Bactrocera philippinensis) in Darwin in November 1997. Lessons learntfrom an earlier incursion of the papaya fruit fly lead to the developmentof an exotic fruit fly preparedness plan, which includes pre-event

Fig. 3. Biosecurity structures in place in Australia. Currently, the system is hierarchical andthrough better communication and sharing of resources where it is most relevant.

preparedness for fruit fly incursions (compilation of fruit fly targetlists), a national fruit fly trapping programme, surveys in NorthernAustralia, monitoring, eradication and containment programme inTorres Strait anddiagnostics (including national exotic fruitfly diagnostic

inefficient. A shift towards a network structure would confer significant advantages

63K.A. Murray et al. / Environment International 48 (2012) 56–64

training and development of improved taxonomy and molecular tech-niques). As a direct result of this improved research driven capacity,therewas a swift and efficient system in place to dealwith the later incur-sion of the Philippines fruitfly,whichwas officially declared eradicated inMay 1999. Attributable directly to early detection and effective response,preparedness and planning, eradication cost $5 million (AUD) comparedwith the $35 million (AUD) cost for the eradication of papaya fruit fly(see also Appendix S2).

8. Solutions to better mitigate current and future risks

It is clear that an economic benefit to Australia can be delivered byan improved capability and capacity to prevent and respond to out-breaks of diseases, pests and weeds (e.g., Philippine fruit fly) but directexamples are limited. The processes to determine these benefits remainchallenging but estimates that have a level of rigour can be made usingavailable information.

In terms of improving capability and capacity in health security, theOne Health approach is showing promise in numerous regions globally(Dedmon et al., 2010; Greene, 2010; Kahn et al., 2009; Mazet et al.,2009; Mullins et al., 2010). This involves multidisciplinary coordinationthrough the sharing of resources and expertise across sectors such aspublic and animal health, agriculture and environment in order to solvecomplex health problems. A recent example of the advantage of this ap-proach was the discovery of the spread of chytridiomycosis as the majorcause of enigmatic amphibian declines and extinctions (Skerratt et al.,2007). The problem of amphibian declines had puzzled the environmen-tal sector for over 20 years andwas not solved until veterinary andmed-ical expertise and resources became involved (Berger et al., 1998).

There are several targets that can be addressed to facilitate a OneHealth approach. One is to form a network for integrating expertise andresources across disciplines and sectors. There should also be a formal in-tegration of health, animal health and environmental health surveillancedata and analysis (Greene, 2010). Thiswill lead to a better understandingof the risk factors driving disease emergence (e.g., Jones et al., 2008).There is currently a framework for understanding and managing healthsecurity in northern Australia but it operates at the senior managementlevel and has a hierarchical structure (Fig. 3). In contrast, a networkoperates at all levels and enables ready communication among those onthe ground. It understands and facilitates social networks, which are thedrivers of solutions to major issues. A focal hub of cross-disciplinary ex-pertise and resources in the form of an institute can help to maintainand drive a network and foster cross-border interrelations (Georganas,2010; see also http://www.onehealthinitiative.com/index.php).

One of the major issues for health security in northern Australia isthat most expertise and resources are located in southern Australia.This is probably because the vast majority of the Australian populationlive below the tropic of Capricorn. Simply relocating resources to thenorth will result in better surveillance at the border and pre-border forall sectors but especially wildlife and domestic animals. For example,health clinics, hospitals and laboratories that collect and report data inreal time could be located in areas such as the Torres Strait rather thanhaving to transport people and samples thousands of kilometres south.On the PNG side, a wholly integrated surveillance system for bothhuman and animal communicable diseases is needed. Initial laboratorysupport could be provided from Australia but ultimately it could besupported by public health laboratories at Balimo and Port Moresby.This will also lead to an improved emergency response capability. Amajor outbreak in northern Australia or PNG, especially involving wild-life, would be of great concern given Australia's current capacity in thatsector in the north. Joint investigation of suspect outbreaks by multi-disciplinary teams and implementation of control strategies that consid-er all sectors such as wildlife, domestic animals and humans should beroutine and is likely to be very strongly supported by PNG (Georganas,2010).

9. Conclusion

Australia enjoys a certain level of protection frommany of theworld'sdiseases, pests and weeds due in part to its geographic isolation and his-tory of strong border security. However, consistentwith a global trend ofincreasing disease emergence and pest and weed spread and establish-ment, Australia remains (like many countries) vulnerable to ongoingrisks. This is demonstrated by the suite of diseases, pests and weedsthat have emerged in recent decades andwhich have incurred significantenvironmental, economic and social costs. Many of these incursions ex-pose north Queensland as a particularly high risk area (a health securityhotspot) due to its connection with neighbouring countries via theIndo-Papuan conduit. Many more diseases, pests and weeds loom onthe horizon because of their almost inevitable transport along the con-duit. Major outbreaks of diseases, pests and weeds have historicallybeen extremely expensive in Australia. Despite this and with the excep-tion of some high profile cases, most expenditure combating diseases,pests and weeds is reactive and invested well after a problem emergesand balloons into a more serious event that potentially could havebeen prevented or contained at a lower cost. In order to improve healthsecurity in Australia in an era of increasing risk, there will need to be ashift in strategy from this reactivity to pro-activity, where pre-emptionand preparedness are more highly valued. Large gains in the qualityand efficiency of health security could therefore bemade bymore strate-gic investment in these areas to reduce the risk of outbreaks, invasion/spread and establishment. Such approaches could be driven by increasedresearch andmanagement capacity consistent with the One Health con-cept that fosters multidisciplinarity among traditionally isolated fieldsand operates at a transboundary scale (e.g., regionally and international-ly). Of particular need is a shift towards local capacity in regions alongdocumented risk pathways in the regions of greatest risk. The benefitsof a more efficient health security system are not just regional but alsonational and international given regional threats can quickly becomepandemics. This model is applicable both in Australia and in other re-gions of the world that value and therefore aim to improve their strate-gies for maintaining health security.

Appendix A. Supplementary data

Supplementary data to this article can be found online at http://dx.doi.org/10.1016/j.envint.2012.06.015.

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