ZOONOSES ASSOCIATED WITH AUSTRALIAN MAMMALS

Table 16.2 provides a summary of zoonoses documented in people from an Australian mammal source.

2.1 Viral diseases

2.1.1 Australian bat lyssavirus

ABLV is discussed in detail in Chapter 42.

2.1.2 Hendra virus disease

Hendra virus (HeV) is discussed in detail in Chapter 43. Flying-foxes are reservoir hosts for HeV (Halpin et al. 2011). People contract HeV disease through high-level con­tact with infected horses, including conducting veterinary procedures, necropsy of infected horses and extensive exposure to respiratory secretions without adequate PPE (Qld Health 2017). Four of the seven human cases that have occurred so far have been fatal.

2.1.3 Zoonotic arboviruses

Ross River virus is an alphavirus that causes Ross River virus disease, the most commonly reported mosquito- borne disease in Australia (NNDSS 2023). Ross River virus is endemic to Australia and is carried between animal reservoir hosts by a range of different mosquito vector species that also feed on humans, resulting in spillover events (Ng et al. 2014). On average, approxi­mately 5000 human cases are reported annually (NNDSS 2023) and although not fatal, severely debilitating effects can persist for many weeks and have significant social and economic effects. The ecology of this virus is compli­cated. Macropods and possums are thought to be the most significant reservoir hosts (Boyd et al. 2001; Potter et al. 2014; Claflin and Webb 2015; Koolhof and Carver 2017); however, the exact role they play in maintenance of the virus and transmission to people is unclear. Serologi­cal evidence of infection has been shown in a wide range of native mammals (WHA 2015). Much research investi­gates the role of reservoir host abundance and factors affecting mosquito numbers to try and predict disease outbreaks (Ng et al. 2014), while management focuses on mosquito control. Barmah Forest virus, Gan Gan and Trubanaman viruses are other arboviruses endemic to Australia that cause influenza-like illness with arthralgia in people. Marsupials are possible hosts of these viruses (Vale et al. 1991; Johansen et al. 2005).

2.2 Bacterial diseases

2.2.1 Tuberculosis

Two forms of zoonotic tuberculosis (TB) are associated with Australian mammals.

TB has been diagnosed in free-ranging and zoo-housed Australian sea-lions (Neophoca cinerea) and long-nosed fur-seals (Arctophoca forsteri) (Forshaw and Phelps 1991; Cousins et al. 1993) and in free-ranging Australian fur­seals (Arctocephalus pusillus) (Woods et al. 1995; Board­man et al. 2014). TB in seals is caused by M. pinnipedii (Forshaw and Phelps 1991; Cousins et al. 2003). Pinnipeds are the natural host, but M. pinnipedii can infect a range of other animals and humans (Cousins et al. 2003). The first reported human case involved transmission from seals to a

Table 16.2. Zoonoses associated with Australian native mammals

276 CurrentTherapyin MedicineofAustraIian Mammals

16-

.WWOd? csiroW⅛

Table 16.2. (continued)

278 CurrentTherapyin MedicineofAustraIian Mammals

*Human nationally notifiable disease.

¹Samaratunga etal. 1998; ²Hanna etal. 2000; ³Francis etal. 2014; ⁴ATAGI 2017; ⁵HaIpin etal. 2011; ⁶QId Health 2017; ⁷Chant etal. 1998; ⁸Barr etal. 2012; ⁹Boyd etal. 2001; ¹⁰Kay etal. 2007; ¹¹Potter etal. 2014; ¹²CIafIin and Webb 2015; ¹³Jackson etal. 1995; ¹⁴Cooke etal. 2002; ¹⁵Baker etal. 2006; ¹⁶Ladds 2009; ¹⁷Thompson etal. 1993; ¹⁸Boardman etal. 2014; ¹⁹Iveson and Bradshaw 1973; ²⁰Hart etal. 1987; ²¹Staffefa/. 2012; ²²Speare and Thomas 1988; ²³Cookefa/. 1967; ²⁴Stevenson efa∕. 2015; ²⁵FIint efa∕. 2016; ²⁶Currie etal. 1996; ²⁷Spratt 2005; ²⁸NSW Health 2016b; ²⁹Graves etal. 1993; ³⁰McBride etal. 2007; ³¹GIazebrookefa/. 1978; ³²Looke 1986; ³³MarshaII and Manktelow 2002; ³⁴QId Health 2016; ³⁵Jackson etal. 2012; ³⁶NSW DPI 2016; ³⁷Hui Chong etal. 2021; ³⁸WaIdron etal. 2010; ³⁹WHA 2009; ⁴⁰Skerratt and Beveridge 1999; ⁴¹BIanshard and Bodley 2008; ⁴²BouIton etal. 2013; ⁴³McPhee etal. 2016

16-Zoonoses 279

seal trainer in Australia, resulting in pulmonary TB mani­festing 2 yr later (Thompson et al. 1993). Since then, TB has been identified in many seal facilities and presents a defined health risk to staff. TB in seals is a slowly progres­sive disease and clinical signs may not be apparent until late in the disease. Antemortem diagnosis is difficult and zoo-housed seals may be infectious for years before disease is suspected (see Chapter 45) (Jurczynski et al. 2012).

Pyogranulomatous pneumonia is the most common pathology in seals with TB, though other organs may be involved (Ladds 2009). Because the disease is primarily pulmonary in both pinnipeds and humans, transmission is presumed to be by inhalation of aerosolised organisms (Kiers et al. 2008; Jurczynski et al. 2012). People at most risk are those with prolonged or regular contact with pin­nipeds or who perform necropsies on tuberculous pinni­peds (Hunt et al. 2008; Waltzek et al. 2012).

2.2.2 Salmonellosis

Salmonellosis in people is a nationally notifiable disease and is mainly food-borne in origin. Salmonellosis is a well-recognised zoonosis and the potential role of wild­life in the zoonotic transmission of Salmonella serovars is of increasing interest (Hilbert et al. 2012). Isolated cases and outbreaks of salmonellosis in people have been caused by infection derived from Australian mammals (Iveson and Bradshaw 1973; Staff et al. 2012). People are at risk of infection through indirect transmission from contaminated environments, as well as through close contact with healthy carrier animals, animals with sal­monellosis and through consumption of improperly prepared contaminated meat from infected kangaroos. Salmonellosis is usually self-limiting in immunocompe­tent people and may go undiagnosed, so the incidence of transmission between Australian mammals and people may be higher than published reports suggest.

Many healthy free-ranging Australian mammals, including marine mammals, carry Salmonella in their intestines and shed the bacteria into the environment in faeces (Vogelnest and Woods 2008; Parsons et al. 2010). Macropods and possums in particular are capable of har­bouring multiple serovars, but disease in free-ranging animals is not reported (Johnson and Hemsley 2008; Vogelnest and Portas 2008; Ladds 2009). The prevalence of Salmonella carriers varies between different species and environments; for example, Salmonella enterica was isolated on non-selective media from 2% or less of dasyu- rids, rodents, macropods, koalas (Phascolarctos cinereus), wombats and possums and 0% of bats, monotremes and bandicoots sampled from different undeveloped geo­graphical areas of Australia (Parsons et al. 2010). At dif­ferent sites in the NT 50-100% of northern quolls (Dasyurus hallucatus) and northern brown bandicoots (Isoodon macrourus) carried Salmonella (Reiss et al. 2015). Almost 100% of free-ranging quokka (Setonix brachyurus) shed large numbers of Salmonella of differ­ent serovars in response to seasonal stressors (Hart et al. 1987) and transmission of S. javiana to a child through contact with quokka faeces on Rottnest Island has been documented (Iveson and Bradshaw 1973).

Quolls, Tasmanian devils (Sarcophilus harrisii), kan­garoos and birds are proposed as likely reservoir hosts for human S. mississippi infections in Tasmania by contami­nating land and water environments (Ashbolt and Kirk 2006). Long-nosed bandicoots (Perameles nasuta) were identified as the source of a localised outbreak of salmo­nellosis caused by S. enterica var. Java in children in NSW through contamination of sand in a playground, with organisms remaining infective in the sand for up to 9 mo (Staff et al. 2012).

Kangaroos harvested for human consumption may pose a food-borne salmonellosis risk through accidental carcass contamination with enteric Salmonella serovars during evisceration (Bensink et al. 1991).

The risk of Salmonella cross-infection is highest where there is close or direct contact between humans and ani­mals and when the animals are subject to stress. Zoo­housed wildlife or those that come into care orphaned, injured or suffering concurrent disease are more likely to harbour a high load of Salmonella organisms and to shed them in greater numbers while remaining asymptomatic (Thomas et al. 2001; Ladds 2009). Hand-reared macro­pods and possums, especially those with diarrhoea, pose a particularly high risk (Speare and Thomas 1988; John­son and Hemsley 2008).

2.2.3 Q fever

Q fever is caused by infection with the intracellular gram­negative bacterium Coxiella burnetii. The disease in humans can be mild and go unrecognised or take an acute or chronic course with potentially life-threatening consequences (NSW Health 2015; Stevenson et al. 2015) (Table 16.2). Approximately 500 cases are reported annu­ally, mostly in NSW and Qld (NNDSS 2023). Domestic ruminants are considered the primary reservoir of Q fever and before the commencement of vaccination programs, approximately half of all cases occurred in abattoir workers. More recently, there have been increas­ing reports from regional or urban areas among people not identified as at risk (NSW Health 2015; ATAGI 2017), with attention focussed on the role of native mammals as reservoir hosts for infection in livestock and humans (Banazis et al. 2010; Tozer et al. 2014). Infection in ani­mals is mostly asymptomatic with persistent environ­mental shedding of bacteria via urine and faeces. In pregnant females, there may be replication in the repro­ductive tract leading to abortion or low birthweight young and massive shedding of bacteria in birth products. C. burnetii is resistant to environmental conditions and to many disinfectants and can be carried over large dis­tances by wind and dust. Transmission to humans is pri­marily by inhalation (NSW Health 2015).

Macropods in many parts of Australia have antibodies to C. burnetii (Banazis et al. 2010; Potter et al. 2011), with an overall seroprevalence of ~20% (Cooper et al. 2012), and shed C. burnetii in their faeces (Banazis et al. 2010). C. burnetii DNA was found in ticks and blood from kan­garoos, wallabies, bettongs, bandicoots and common brush-tailed possums in north Qld, confirming they are capable of acting as reservoir hosts (Cooper et al. 2013). Dingoes (Canis lupus dingo), flying-foxes and koalas have also been implicated as potential hosts (Cooper 2011; Tozer et al. 2014). Many of these species either range on the outskirts of urban areas (e.g. macropods and dingoes) or are adapted to urbanisation (e.g. bandicoots and pos­sums), suggesting their possible role in transmitting Q fever to humans and domestic animals either through ticks (Pope et al. 1960) or through shedding the organism into the environment. Three recent cases of Q fever in Qld, one resulting in life-threatening organ failure, have arisen either through occupational handling of dead kan­garoos and joeys or, in two cases, also mowing grass con­taminated with kangaroo faeces (Stevenson et al. 2015; Flint et al. 2016).

2.2.4 Scrub typhus and Queensland tick typhus Arthropod-borne rickettsial zoonoses in Australia include scrub typhus and Queensland tick typhus. Scrub typhus is caused by Orientia tsutsugamushi (formerly Rickettsia tsutsugamushi) and is different to human epi­demic typhus. Scrub typhus occurs across south-east Asia and in Australia is confined primarily to coastal north Qld and some pockets of rainforest in the NT (Litchfield National Park) and the Kimberleys in WA (NSW Health 2016b). The northern brown bandicoot and several species of native rodents (see Table 16.2) carry the organisms without evidence of disease (Cook et al. 1967; Breed and Eden 2008). Transmission between hosts and people is via the bite of a larval mite vector, Leptotrombid- ium delicense (Bell and Whelan 1993). Scrub typhus is a severe influenza-like illness with lymphoid involvement, truncal macular rash and an easily missed localised scab or eschar at the site of mite attachment. Incubation period is 1-2 wk and without appropriate treatment (doxycy­cline) the disease can be fatal, as evidenced by the death of a man who was infected while constructing a tourist pathway in Litchfield National Park and delayed seeking medical attention for 1 wk (Currie et al. 1996). The illness resembles many other zoonoses in the north of Australia such as Q fever, Ross River virus, leptospirosis and bru­cellosis which can delay diagnosis.

2.2.5 Leptospirosis

Leptospirosis is caused by spirochaete bacteria in the genus Leptospira. It is an important zoonosis worldwide, with more than 250 pathogenic serovars. Most Leptospira have natural reservoirs in mammals, particularly rodents, which remain healthy but shed organisms intermittently into the environment in urine. Transmission to humans or other incidental host species occurs through contact of broken skin or mucous membranes with urine from infected animals, or more commonly through contact with contaminated water or soil. Warm, wet climates favour survival of the organisms in the environment (Qld Health 2016).

Leptospirosis is a human notifiable disease in Aus­tralia with ~100 cases reported annually, mostly in Qld (Qld Health 2016). The four main serovars involved are Arborea, Hardjo, Australis and Zanovi. Arborea and Hardjo account for most infections and have their reser­voir in introduced rodents and cattle, respectively, while Australis and Zanovi have their reservoir in native rodents and bandicoots and are causes of ‘cane cutters’ disease’ (Glazebrook et al. 1978; Slack et al. 2006; Qld Health 2016). Occupational risk is higher in agricultural workers, although recreational activities such as swim­ming and bushwalking also pose a risk (Slack et al. 2006). A zoologist contracted leptospirosis while handling wild native rats in Qld (Looke 1986). An incubation period of ~10 d is followed by a febrile flu-like illness with GI signs lasting up to 3 wk. A proportion of patients will develop more serious signs with multi-organ involvement which may progress to organ failure and death if untreated. In up to 50% of cases patients require hospitalisation (Qld Health 2016).

A wide range of other Australian native mammals have been shown to have antibodies to Leptospira, includ­ing flying-foxes, common brush-tailed possums, macro­pods, platypus (Ornithorhynchus anatinus), Tasmanian devils, wombats and koalas (Munday 1972; Milner et al. 1981; Smythe et al. 2002; Eymann et al. 2007; Loewenstein et al. 2008; Roberts et al. 2010; Wynwood et al. 2016). In most cases, urinary excretion of organisms has not been proven and it is unknown whether these animals are inci­dental hosts or true carriers and the role they play in spread of pathogenic serovars to humans is unclear. Organisms have been identified by PCR in kidney (11% of samples) and urine (39% of samples) from all four species of flying-foxes, suggesting they are carriers of Leptospira spp., although the serovars involved are unknown (Cox et al. 2005). There has been no evidence to date of Leptospira infection in Australian marine mammals, but outbreaks are seen regularly in pinnipeds along the North Ameri­can Pacific Coast (Norman et al. 2008).

2.2.6 Tularaemia

Tularaemia is caused by the intracellular gram-negative bacterial rod Francisella tularensis. Two subspecies cause illness in both animals and people: the highly virulent F. tularensis tularensis (type A) is found only in North America and the less virulent F. tularensis holarctica (type B) is found throughout the northern hemisphere but was previously unknown in the southern hemisphere. The bacteria are highly infectious with a broad host range, but tularaemia is primarily a disease of rodents and lagomorphs, in which it can result in acute septicae­mia and sometimes mass deaths (NSW DPI 2016).

In 2011 in western Tasmania, two separate human infections caused by F. tularensis holarctica biovar japon- ica were diagnosed serologically and by 16sRNA sequenc­ing after a bite or scratch from an eastern ring-tailed possum (Jackson et al. 2012; NSW DPI 2016). No evidence of infection has been found in any wildlife sampled from Tasmania; however, in 2016, F. tularensis holarctica biovar japonica was isolated by direct fluorescent antigen testing and real-time PCR on archived tissues from eastern ring­tailed possums that died in NSW in 2002 and 2003 (Eden et al. 2017). Little else is currently known about the distri­bution, prevalence or epidemiology of F. tularensis in Australian wildlife.

2.3 Protozoal diseases

2.3.1 Cryptosporidiosis

Cryptosporidia are protozoan parasites with a broad ver­tebrate host range and variable host specificity. Applica­tion of molecular tools revealed that the majority of cryptosporidia found in naturally infected wildlife is dif­ferent from those in humans, who are primarily infected with Cryptosporidium hominis and C. parvum (Chhabra and Muraleedharan 2016). Host-adapted Cryptosporidium spp. have been identified in kangaroos, wallabies, bandi­coots, koalas and common brush-tailed possums (Ryan and Power 2012) and C. hominis or C. parvum has also been identified in faeces from bandicoots, possums, kan­garoos and dingoes, suggestive of human spillover (refer­ences cited in Zahedi et al. 2016). Faecal passage of both host-adapted and recognised human pathogenic species from infected wildlife contributes to the overall pool of cryptosporidia oocysts identified in environmental sam­ples (Chhabra and Muraleedharan 2016), and contamina­tion of water catchment areas is considered a major mode of transmission to people (Zahedi et al. 2016). A novel subtype of C. viatorum, with as yet unproven zoonotic potential, was discovered in faeces from swamp rats (Rattus lutreolus) inhabiting a protected water catchment area in Melbourne, Vic. C. viatorum is a globally distrib­uted pathogenic species that has previously only been identified in humans (Koehler et al. 2018). C. fayeri, a marsupial-specific species not previously recognised as zoonotic, caused self-limiting GI disease in a person in frequent contact with habituated macropods (Waldron et al. 2010). Both C. fayeri and C. parvum have been identi­fied in eastern grey kangaroos (Macropus giganteus) graz­ing in the Sydney water catchment area (Ryan and Power 2012; Zahedi et al. 2016).

2.4 Parasitic diseases

2.4.1 Hydatid disease

The hydatid tapeworm Echinococcus granulosus is estab­lished throughout eastern Australia and part of the south-west. Dingoes and wild dogs are currently the most important definitive host for the transmission of E. gran­ulosus in Australia, with macropods serving as interme­diate hosts in a sylvatic cycle (Jenkins et al. 2008). Recreational visitation to national parks frequented by dingoes and infiltration of dingoes into the fringes of urban areas pose an important potential public health risk. Along the Sunshine Coast in Qld the prevalence of hydatid infection in dingoes and their hybrids is as high

Table 16.3. Selected potential zoonotic agents identified in Australian mammals where zoonotic transmission has not been demonstrated

16-Zoonoses 283

Table 16.3. (continued)

¹Fyfeefa/. 2010; ²Steffen etal. 2010; ³Lavender etal. 201 Ij⁴Boyd etal. 2012; ⁵Carson etal. 2014; ⁶O'Brien etal. 2017; ⁷RoItgen etal. 2017; ⁸Xu etal. 2022; ⁹Bakerefa/. 1998; ¹⁰Cawthorn 1994; ¹¹Huntefa/. 2008; ¹²Lynch efa∕. 2011a; ¹³Cookefa/. 1967; ¹⁴Hopkinson and Lloyd 1981; ¹⁵EIIiott 2007; ¹⁶PapanicoIas efα∕. 2012; ¹⁷VogeInest and Portas 2008; ¹⁸Ladds 2009; ¹⁹Wang efα∕. 2010; ²⁰Vaughan-Higgins efα∕. 2013; ²¹Dawson 2005; ²²Lynch efα∕. 2011b; ²³Hernandez-Mora efα∕. 2013; ²⁴PaImer and Peterson 2014; ²⁵GriIIo efα∕. 2014; ²⁶Robson efa∕. 1995; ²⁷Rose efa∕. 2004; ²⁸DougaII efa∕. 2009; ²⁹DougaII efa∕. 2011; ³⁰Smoutefa/. 2013; ³¹Spratt 2005; ³²Vos efa∕. 2016

284 CurrentTherapyin MedicineofAustraIian Mammals

as 46.3% (Jenkins et al. 2008) and a local council employee was infected while working on a dingo control program (Michael 2011). Individual dingoes may harbour many thousands of worms, shedding large numbers of eggs in their faeces while remaining healthy. Eggs are immedi­ately infective to humans and may remain viable in the environment for up to 1 yr. Flies may play a part in spreading eggs from faeces to human food in national parks and other recreational areas frequented by dingoes (Jenkins et al. 2008), and eggs may adhere to the coat and perianal area of infected dingoes, increasing the risk of transmission to workers that handle them.

2.4.2 Scabies

Sarcoptic mange caused by the burrowing mite Sarcoptes scabiei is a well-recognised skin disease in the common wombat (Vombatus ursinus), southern hairy-nosed wombat (Lasiorhinus Iatifrons) and occasionally in koalas and wallabies (Vogelnest and Woods 2008), characterised by crusting, alopecia and hyperkeratosis (see Chapter 12). S. scabiei from wombats and koalas have infected humans (Barker 1974; Skerratt and Beveridge 1999) causing a pru­ritic rash with erythematous papules. The mites are spread by direct contact with infected animals. Dead wombats may pose a greater risk of transmission because the mites may be seeking a new host, stimulated by the temperature differential between a carcass and a living host (Skerratt and Beveridge 1999).

2.5 Fungal diseases

2.5.1 Dermatophytosis

Dermatophytosis can occur in any Australian mammal and if zoophilic fungi are involved, can pose a zoonotic risk to people in close contact. Zoo-housed macropods, especially young red kangaroos (Osfranter rufus), appear to be more commonly affected (Boulton et al. 2013) and sporadic outbreaks can occur. Free-ranging macropods rarely show lesions, but subclinical infection can occur (Vogelnest and Portas 2008). Most reports of zoonotic transmission are from kangaroos and involve Trichophy­ton mentagrophytes (Kaminski 1983; McPhee et al. 2016).

3.