Methodology

The four major feral animal types that are commonly consumed in Australia are pigs (Sus scrofa), deer (Cervus elaphus, Cervus timorensis, Cervus unicolor, Dama dama, Axis axis and Axis porcinus), rabbits (Oryctolagus cuniculus) and hares (Lepus capensis), and goats (Capra hircus). Although the meat of other feral animals, such as camels (Camelus dromedarius) [24] and water buffalo (Bubalus bubalis) [25], are also consumed in Australia, this is generally within limited community groups and were not considered within this review. For the purpose of this review, only protozoal and helminth parasites that infest the muscle and organ (e.g. heart, liver and kidney) systems and are infective to humans upon ingestion were considered as potential zoonotic parasites.

A review of publications on feral animals and their parasites was conducted using online databases (CAB, PubMed and Web of Science); a search of the disease reporting database, ProMed, did not return any results. The Boolean search phrase used included the host information (“pig OR Sus OR Suidae”; “deer OR Cervus OR Dama OR Axis OR Cervidae”; “rabbit OR hare OR Oryctolagus OR Lepus OR Leporidae”; “goat OR Capra OR Bovidae”) in combination with “AND zoono* (to cover zoonosis, zoonoses and zoonotic) AND parasit* (to cover parasite, parasitism and parasitic) AND Australia AND food”. The PRISMA guidelines were followed to remove duplicate records and records that could not be retrieved (Online Resource 1A-D). Of the remaining records eligible for assessment, records that did not report Australian feral animals were then excluded. Finally, the remaining records were read to assess their content for inclusion. This was conducted individually by host species group.

A subsequent review of publications on zoonotic parasites in Australia was conducted using the same three online databases. The five most important meat-borne zoonotic parasites around the world are Toxoplasma gondii, Sarcocystis spp., Trichinella spp., Spirometra spp. and Taenia spp. [18, 26]; recent research conducted by our laboratory has also reported infections of the zoonotic pentastome, Linguatula serrata, in Australia [27]. The Boolean search phrase used included the parasite or disease name (“Sarcocyst*” (to cover Sarcocystis and sarcocystiosis); “Toxoplasm*” (to cover Toxoplasma and toxoplasmosis); “Spirometra OR Spargan*” (to cover spargana, sparganid and sparganosis); “Trichin*” (to cover Trichinella and trichinosis); “Taenia OR cysticer*” (to cover cyticercus and cyticercosis); “Linguatula OR pentastom*” (to cover pentastome, pentasomid and pentastomiasis)) in combination with “AND Australia AND feral”. The PRISMA guidelines were followed as outlined above individually by parasite type (Online Resource 1E-I).

The hostsPigs

A total of 39 records were found across the three databases; following assessment, 8 records remained. Of these eight records, only one specifically dealt with zoonotic parasites of Australian wildlife [28]. Spratt [28] listed sparganosis (caused by Spirometra erinaceieuropaei), pentastomiasis (caused by pentastomes of the genera Armillifer and Linguatula) and toxoplasmosis (caused by T. gondii) as potential zoonotic parasites but did not list any known cases of infection. Kelly [29] reviewed potential zoonotic parasites in Australia, referring to sparganosis being of importance where feral pigs were fattened for human consumption with a high prevalence of infection in many areas. Taenia solium and Trichinella spiralis were also listed as potential problems but both, despite widespread global distributions, were not endemic in Australia [29]. Sporadic reports of T. solium in pigs (as Cysticercus cellulosae) at slaughter had been made, while human infections in Australia with T. spiralis were usually acquired from imported pork products [29]. The remaining records primarily dealt with reviews of trichinellosis and listed the few reports of Trichinella spp. previously reported in wildlife in Australia, with no human infections [30,31,32]. VanderWaal and Deen [33] provided information on the changing epidemiology of a variety of infectious diseases of swine worldwide, concentrating on farmed animals. Of the 40 pathogens identified, only 3 were zoonotic parasites transmitted via consumption of infected meat or organs: Trichinella spp., T. solium and T. gondii [33].

Deer

As only two records were obtained using the full search phrase, and both were deemed unsuitable, “food” was removed and the search re-run. A total of 23 records were obtained using this shortened search phrase; however, following assessment, no records were deemed suitable for inclusion.

Goats

A total of 26 records were found across the three databases; following assessment, 2 records remained. Both dealt with infections within production animals [34, 35], rather than feral goats, but given that large numbers of feral goats are “domesticated” to become rangeland goats for future meat production, they were considered relevant to this review. A 34% antibody level in the population (in the State of South Australia) for Sarcocystis spp., which is a potential zoonotic parasite transmitted by ingestion of infected meat, was found in one study [34]. Echinoccocus and Fasciola were listed as potential zoonotic risks [35], but infection with both does not involve the consumption of infected goat meat. The only other zoonotic parasite mentioned was Trichinella and its absence from Australia [35].

Rabbits and Hares

As only three records were obtained using the full search phrase, of which two were deemed unsuitable and the third was unobtainable, “food” was removed and the search re-run. A total of 48 records were obtained using this shortened search phrase; following assessment, 2 records remained. Eight rabbits and a single European hare (as well as a feral pig and goat, but this reference did not appear in those searches) were examined for larval stages of the zoonotic pentastomid Linguatula serrata; none was infected [27]. The health impacts of feral mammals on humans were reviewed, including potential zoonotic parasites where hares were infected with Toxoplasma, but no specific details of the geographical location were provided [1].

The Parasites Trichinella

A total of 8 records were obtained for infection with Trichinella in Australian feral animals; following assessment, three records remained, all of which were general reviews of Trichinella [32] or pig-borne diseases in general [4, 36]. Although the known zoonotic species, Trichinella spiralis, has yet to be reported from Australia, both T. pseudospiralis and T. papuae have been reported from various mammals, although only T. papuae was reported from pigs, but not from mainland Australia [32].

Previous reports of human infections within Australia by nematodes within muscle tissues were initially diagnosed as T. pseudospiralis [30]. However, this has been shown to be a misidentification, with Haycocknema perplexum the actual parasite [37]. This parasite has only been reported from Australia (either in northern Queensland or Tasmania) with 13 known cases, all with an unknown source of infection [37]. Each case had some association with wildlife, but not all consumed wild game meat, although this has not been ruled out as a potential risk factor [37].

Linguatula

Only three reports were obtained discussing infection with Linguatula serrata in feral animals [27, 38, 39]. After documenting the widespread occurrence of L. serrata in wild dogs and foxes in the highlands of southern Australia, but not being able to find infection within a range of potential intermediate hosts, including rabbits, hares and pigs [27], intermediate stages were subsequently found in the liver and lung tissues of rabbits [39] and the mesenteric lymph node of a feral goat (identified as Linguatula sp.; 38).

Spirometra (Sparganosis)

A total of 34 records were obtained for infection with Spirometra erinacei/erinaceieuropaei or sparganosis in feral animals in Australia; following assessment, 8 remained for inclusion. The majority of the references excluded were detailing the infection of Spirometra in definitive hosts (cats, foxes and wild dogs) without mention of hunted feral animals as prey items [40,41,42,43,44]. The remaining records all detailed sparganosis infection in feral pigs, with specific mention of potential human health risks from consumption.

Sparganosis in feral pigs occurs along the eastern edge of Australia (from tropical north Queensland to Victoria) [45,46,47]. Given that the distributions of foxes, wild dogs and feral cats overlap with pigs across most of their distribution, it is likely that spargana could occur in feral pigs wherever they are found in Australia. Indeed, carcasses of feral pigs were commonly condemned at abattoirs due to infection with spargana [10, 48]. Rates of condemnation were usually over 50%, but this differed between geographical location and year, with infection levels of spargana in adult feral sows corresponding with good seasonal conditions [49]. Standard meat inspection procedures, however, often failed to find spargana in deep muscles which would lead to an underreporting of infection levels [49].

The initial report of spargana in the muscle of feral pigs that had been caught and kept to be fattened for later slaughter was documented in further detail by Bearup [48] in a description of the life cycle. Spargana were most commonly found under the perinoneum of the abdominal wall and diaphragm but were also found in the connective tissue between muscles in almost every region of the body [45, 48].

Despite these high levels of infection in feral pigs, only 8 cases of human sparganosis have so far been reported in Australia, which is most likely due to misdiagnosis of infection [50]. Most cases reported in Australia are subcutaneous sparganosis in Australian-born people who have never travelled overseas [48, 50]. These cases were most likely acquired through the consumption of infected copepods (first intermediate hosts) in unfiltered water; however, one case reported consumption of wild pigs and rabbits [50]. Subcutaneous infections generally present as a small tumour or lump, which are often misdiagnosed [45, 48, 50] until excised and identified [50]. An experimental infection produced oedema and erythema accompanied by chills and fever caused by the migration of spargana [48]. Worldwide, cerebrospinal sparganosis is the most common infection, accounting for approximately 25% of all cases; the only report of cerebral sparganosis in Australia was from an East Timor refugee [50].

Spargana left in situ in a pig carcass for 24 h at room temperature were viable and infective to dogs and cats and could remain viable for up to 14 days in a domestic refrigerator [45]. Freezing at − 8 °C for 24 h [45] or cooking at a temperature of at least 80 °C for a few minutes [49] was considered sufficient to kill sparagana in tissues. Infection in people in Australia is likely to be low risk due to most Australians cooking pig meat thoroughly, although “immigrants from some European countries are accustomed to eating raw pork in various dishes” and would be more susceptible to infection [45].

Sparganosis is likely an under-recognised zoonotic disease in the Australian population and, as all the native Australian cases occurred in rural settings, this highlighted the need for rural and remote health practitioners to be aware of this disease [50].

Taenia solium

A total of 32 records were obtained for Taenia infection; following assessment, 1 remained for inclusion which did not include T. solium as a parasite of feral pigs in Australia [49]. Most of the references that were obtained dealt with other species of Taenia that utilise dogs and cats as definitive hosts.

Toxoplasma gondii

A total of 73 records were obtained for T. gondii infection; following assessment, 3 remained for inclusion. The majority of records that were excluded were only reporting prevalence of infection in feral cats in different regions of Australia, mostly showing high prevalence of infection in areas where cat populations are high [51, 52]. The records that did mention feral animals that are consumed by humans all had negative results for the presence of T. gondii and/or its antibodies, although for most studies, numbers of examined animals were usually low, and the study took place in a single geographical location. Rabbits were found to be uninfected in Western Australia (n = 57) [53] and Queensland (n = 4) [54], while fallow deer (n = 2) and feral goats (n = 5) were also uninfected in Tasmania and Queensland, respectively [55].

Sarcocystis

A total of 17 records were obtained for Sarcocystis in feral animals in Australia; following assessment, 9 remained for inclusion. The majority of these references did not refer to feral game for consumption but were detailing prevalence of infection in definitive hosts (primarily cats) which presents information on risk of infection in local animals exposed to infective stages [44, 56,57,58,59,60]. A survey of feral goats slaughtered at abattoirs in South Australia found that there were a significant proportion of the goats, from all regions in South Australia, infected with the microscopic sarcocysts in a variety of tissues, including skeletal muscles [61]. Although the cost of Sarcocystis infection to the production animal industry is large (almost AU$2 million annually from carcass condemnation and meat trimming), no human infections have yet been reported [60]. As there are a number of species of Sarcocystis that infect animals in Australia, it is possible that none is pathogenic to people; however, only one study appears to have tested this hypothesis [62]. Human volunteers were fed either microscopic or macroscopic Sarcocystis cysts collected from sheep muscle, but all tested negative for infection after 60 days [62]. In comparison, macroscopic cysts were found to infect cats, and microscopic cysts were found to infect dogs and foxes after the same time period [62]. Areas with high cat densities correlate to areas with high levels of infection in production animals [59, 60]; however, there has been no corresponding survey of wildlife in these areas to determine impacts of cat density on levels of infection.