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Echinococcus granulosus in Australia, widespread and doing well!
Parasitology International 55 (2006) S203 – S206 www.elsevier.com/locate/parint
Echinococcus granulosus in Australia, widespread and doing well! David J. Jenkins * Australian Hydatid Control & Epidemiology Program, 12 Mildura Street, Fyshwick, ACT 2609, Australia School of Botany of Botany and Zoology and Faculty of Medicine, Australian National University, Canberra, ACT 0200, Australia Available online 13 December 2005
Abstract Echinococcus granulosus is the only member of the Genus Echinococcus to occur in Australia. The major biomass of E. granulosus occurs in wildlife. The wildlife transmission cycle is predominantly perpetuated via a predator/prey interaction between wild dogs (dingoes and dingo/ domestic dog hybrids) and macropodid marsupials (wallabies and kangaroos). Other wildlife hosts include foxes, wombats and feral pigs. This wildlife reservoir for E. granulosus ‘‘spills over’’ to help maintain a domestic cycle through E. granulosus-infected wild dogs defecating on pasture, transmitting infection to livestock and some farmers and hunters feeding hydatid-infected offal of macropodids or feral pigs to domestic dogs. The potential transmission risk to humans using public picnic and camping areas in parks and forests, especially in the southeastern Australia, could be substantially reduced through regular distribution of baits containing praziquantel. Encroachment of wild dogs and foxes into urban centers presents a new potential path of transmission from wildlife to humans. D 2005 Elsevier Ireland Ltd. All rights reserved. Keywords: Echinococcus granulosus; Australia; Wildlife; Wild dogs; Dingoes; Kangaroos; Wallabies; Domestic dogs; Thylacines; Human; Infection; Control
1. Introduction Echinococcus granulosus can be found on all continents of the world, an impressive feat for a parasite with limited means of locomotion that originated in the northern hemisphere. The international migration of E. granulosus to the continents of the southern hemisphere was achieved in association with translocation of domestic animals (sheep and dogs) during various phases of European colonisation. Sheep first arrived in Australia in 1788 but the earliest introductions were unsuccessful. However, Spanish merinos adapted well and by 1860 Australia had a population of 20 million merinos [1]. Through complete ignorance of the transmission pattern and public health importance of E. granulosus plus the abundance of potential animal hosts, E. granulosus spread quickly in livestock and dogs in Australia and by the1860s, human hydatidosis was a major public health issue in the new colony [1]. Of great importance for the establishment and perpetuation of E. granulosus in Australia was the ability of the parasite to * Australian Hydatid Control & Epidemiology Program, 12 Mildura Street, Fyshwick, ACT 2609, Australia. Tel.: +61 2 6271 6331; fax: +61 2 6272 3124. E-mail address: [email protected]. 1383-5769/$ - see front matter D 2005 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.parint.2005.11.031
also incorporate Australian native wildlife into its transmission pattern. Non-marsupial dingoes (Canis lupus dingo), the toporder predator present in Australia at the time of European settlement, had arrived 4000– 5000 years previously from southeastern Asia and displaced the thylacine (Thylacinus cynocephalus), the original marsupial top-order predator [2]. The importance of the dingo, in respect of E. granulosus transmission, was that it was a canid, highly susceptible to infection with E. granulosus and large enough to predate on sheep. The dominant native herbivorous fauna in Australia at the time of European settlement were macropodid marsupials (kangaroos and wallabies) that had evolved in isolation in Australia and were highly susceptible to infection with E. granulosus. Transmission of E. granulosus into wildlife is likely to have occurred first through macropodids becoming infected by accidental ingestion of eggs of E. granulosus passed by domestic dogs, and dingoes predating on hydatidinfected sheep. It has been proposed that transmission of E. granulosus to Australian wildlife was greatly assisted by transhumant grazing of sheep, an agricultural practice that persisted in eastern Australia until 1972 [3]. A major recent achievement in the control of E. granulosus in Australia has been the provisional eradication of E. granulosus from Tasmania. This impressive achievement was
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the result of more than 30 years of concerted, well-funded and organised hydatid control, backed up by state legislation [4].The most important factors contributing to the success of the Tasmanian campaign were that wildlife never became involved in transmission and, as an island, the control area was manageable and movements of animals into Tasmania could easily be controlled [1]. Domestic dogs and livestock still become infected with E. granulosus on mainland Australia but the prevalence is lower than 50 years ago [1]. However, the main source of infection for domestic animals today is via wildlife [3] rather than through a domestic animal transmission pattern. Therefore, the emphasis of this paper will be on transmission of E. granulosus within the wildlife reservoir, including circumstances where the wildlife reservoir may ‘‘overflow’’ into domestic animals. 2. E. granulosus transmission in wildlife The transmission pattern for E. granulosus in Australian wildlife is maintained through a predator/prey interaction between wild dogs (dingoes and dingo/domestic dog [Canis familiaris] hybrids), foxes (Vulpes vulpes) and macropodid marsupials [5], wombats (Wombatus ursinus) and feral pigs (Sus scrofa). Data indicate E. granulosus can utilise whatever hosts are available, transmitting between wildlife and domestic animals and also to humans [3]. 2.1. Wild dogs Dingo hybrids are similarly susceptibility to E. granulosus as pure-bred dingoes [5,6]. The prevalence of E. granulosus in wild dogs, particularly in eastern Australia, is high with prevalence levels ranging between 25% and 100% in Victoria and New South Wales [5] and between 76% and 100% in eastern Queensland [7– 9]. The worm burdens in wild dogs in southeastern Australia are commonly up to 10,000 worms but burdens greater than 50,000 to 100,000 worms occur regularly [5]. Heavier burdens, up to 300,000 worms, have been recorded [6]. Wild dogs represent the most important definitive host for transmission of E. granulosus in Australia today. 2.2. Wild dogs in urban areas A recent development in the behaviour of wild dogs in Queensland has been incursions of wild dogs, some E. granulosus infected, into urban habitats, Townsville [10], northwestern Brisbane (Jenkins and Shield, unpublished data) and the Sunshine Coast (Jenkins and Allen, unpublished data). These ‘‘urban’’ wild dogs scavenge rubbish bins, defecate in gardens and have been reported killing domestic pets. Apart from the public nuisance, the presence of E. granulosusinfected wild dogs in residential areas is a potentially important public health issue. Brown and Copeman [10] reported E. granulosus in 6 of 20 wild dogs examined from Townsville and Jenkins and Allen (unpublished data) have found 11 infected of 44 wild dogs examined from the Sunshine Coast. Worm burden data were unavailable from the Townsville wild dogs, but the
worm burdens in the 11 Gold Coast dogs ranged between 120 and 10,950 worms. 2.3. Macropodids Kangaroos and wallabies are the most widespread wildlife intermediate hosts for E. granulosus in eastern Australia, consisting of three main species, eastern grey kangaroos (Macropus giganteus), red-necked wallabies (Macropus rufogriseus) and swamp wallabies (Wallabia bicolor). Of all intermediate macropod hosts examined in southeastern Australia, the highest prevalence of infection (over 60%) and the highest cyst fertility has been found in swamp wallabies [5]. Swamp wallabies are of importance in the transmission pattern of E. granulosus because they are a favoured food item of wild dogs [5]. The site of predilection for E. granulosus metacestodes in macropodids is in the lungs, which may render infected animals more susceptible to predation, through compromised lung function [6]. Durie and Riek [7] reported catching a sick red-necked wallaby by hand, that was later found infected with a large lung hydatid cyst. The authors believed the cyst to be the cause of the incapacity of this animal. Johnson et al. [11] reported deaths of Queensland rock wallabies and nailtail wallabies due to pulmonary hydatidosis and most recently (2004), pulmonary hydatidosis has also been reported as the cause of death of brush-tailed rock wallabies in two different, closely monitored colonies in Queensland (Barnes, personal communication). Swamp wallabies are common throughout eastern Australia, particularly along The Great Dividing Range and they are pivotal in the successful transmission of E. granulosus in wildlife [3]. However, their importance as an intermediate host may vary in some local areas. South of Charters Towers, North Queensland, where swamp wallabies were rare, Banks [8] found a high prevalence of hydatid infection (22%) in black-striped wallabies (Macropus dorsalis). A range of other macropodid marsupial species are also susceptible to hydatidosis. These include the bridled nailtail wallabies (Onychogalea fraenata), rock wallabies (Petrogale persephone; Petrogale mareeba), red-necked wallabies (M. rufogriseus), whiptail wallabies (Macropus parryi) and pademelons (Thylogale stigmatica) [3]. 2.4. Wombats Hydatidosis has only been reported in wombats from Victoria [12]. The cysts recovered from the Victorian wombats, as with macropods, contained many protoscoleces and were all located in the lungs. Although wombats are also a favoured dietary item of dingoes, the apparent low prevalence or absence of hydatid infection in wombats from many areas suggests they may be considered as an intermediate host of only local importance. 3. Introduced wildlife The introduction of rabbits (Oryctolagus cunniculus) and foxes (V. vulpes) into Australia and the establishment of feral
D.J. Jenkins / Parasitology International 55 (2006) S203 – S206
pigs (S. scrofa) provided several potential new hosts into the wildlife transmission pattern. 3.1. Lagomorphs Rabbits occur in large numbers throughout much of Australia and occasional unconfirmed reports of hydatid infection in wild rabbits appear in the Australian historical scientific literature, but these reports are likely to have been descriptions of metacestodes of Taenia serialis. In a single experimental study Jenkins and Thompson [13] induced hydatid infection in only one of five wild-caught rabbits challenged with 500– 6000 eggs. The infected rabbit received 6000 eggs. The lack of confirmed reports of hydatid infection in wild rabbits suggests they are not naturally involved in transmission in Australia. 3.2. Feral pigs Feral pigs are numerous in much of Australia except the arid center. Hydatid infection in feral pigs is common in many areas of eastern and parts of Western Australia, but cyst fertility is usually low. Wild dogs have a preference for hunting young pigs whose cysts are likely to be immature, suggesting that the contribution of feral pigs to the transmission of E. granulosus in Australia is modest [3]. 3.3. Foxes Foxes infected with E. granulosus have been found widely in southeastern Australia [3]. Only a few individuals are infected in each population, but in one area, prevalence reached 46% [5]. Worm burdens of infected foxes are low (usually less than 50 worms); therefore, the contribution of foxes in contaminating the bush with eggs of E. granulosus, compared with wild dogs, is small. However, where E. granulosusinfected foxes infiltrate urban centers, the few eggs distributed by infected animals may be of more public health importance than is currently appreciated, particularly in the vicinity of popular public barbecue/picnic sites [14].
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like dingoes, predated on sheep. However, despite thylacines predating on sheep, and there being abundant macropodids of several species living in Tasmania, E. granulosus never established in Tasmanian wildlife. It is tempting to suggest that thylacines, like the species of dasyurids mentioned above, may have also been refractory to infection with E. granulosus and unable to act as the transmission conduit between sheep and macropodids. 5. Transmission of E. granulosus to domestic animals and humans via wildlife In a recently reported coproantigen study in rural dogs [16, in press], 29% of 344 dogs in New South Wales and 18% of 218 Victorian dogs tested positive. Most of the E. granulosus coproantigen-positive dogs occurred on farms possessing more than 5 dogs, where farmers commonly supplemented feeding commercial dry dog food with wildlife carcasses. Wild dogs have been implicated in the transmission of E. granulosus to sheep [12] and cattle [8] and anecdotally once in feral goats (Thompson, personal communication). However, an experimental infection study with feral and angora goats, using eggs from E. granulosus grown in dingoes experimentally infected with protoscoleces obtained from a kangaroo, resulted only with infection in the angora goats (Jenkins, unpublished data). These data suggest feral goats may not be acting as intermediate hosts for E. granulosus in Australia. In view of the high prevalence of E. granulosus in Australian wild dogs, it is not unreasonable to speculate that a proportion of human cases occurring in rural Australia are wildlife derived [17]. However, the long latent period from infection to diagnosis makes it difficult to conclusively link cases of human hydatidosis to contact with wildlife. In two cases investigated in Queensland, cyst material was shown to be genetically indistinguishable from E. granulosus cyst and adult worm tissue from wildlife [18]. One patient had admitted to contact, for 9 years, with domestic dogs fed offal from macropodids, whilst the other had had contact with a wildcaught dingo pup 5 years previously. Other reports of hydatid transmission from wildlife to humans have been reviewed by Jenkins and Macpherson [3].
4. Native Carnivores 4.1. Dasyurids
6. Use of praziquantel baits to treat wild canids around camping grounds
A recent survey of E. granulosus coproantigens in the faeces of wild, spotted-tailed quolls (Dasyrurus maculatus) failed to detect a positive sample, despite finding the remains of swamp wallaby (W. bicolor), in the faeces of some of the quolls [15]. Previous attempts to experimentally infect other dasyrurid species, namely, the Tasmanian devil (Sarcophilus harrisii) and the crest-tailed marsupial rat (Dasyuroides burnei), were unsuccessful [15], suggesting dasyruids, as a group, may be refractory to infection with E. granulosus. Thylacines were dasyurids and still common in Tasmania when Europeans arrived. Hydatid disease was present in Tasmanian sheep during settlement (as it was in mainland sheep) and thylacines,
In many parts of eastern Australia, the use of parks and forests by the general public and tourists for activities such as camping and barbecues (in designated areas) is becoming more popular. Dingoes and foxes are attracted to these places to scavenge food scraps once campers have departed. If a campsite or picnic area occurs in the home range of a pack of wild dogs and/or a fox, the highly territorial nature of these species ensures the same animals visit the area repeatedly. This presents a realistic opportunity to control E. granulosus infection in these animals through the use of baits containing praziquantel being distributed at 4 –6 weekly intervals in and around these bush recreational areas. Praziquantel baits have
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been used for treating wild red foxes (V. vulpes) in a trial in Germany. The study clearly demonstrated the possibility of substantially reducing the prevalence of E. multilocularis in wild foxes [19] through the use of medicated baits. However, this effect could only be sustained with continued regular use of praziquantel baits, once baiting ceased foxes became reinfected within a few months. 7. Prospects Since E. granulosus occurs commonly in wildlife over a large part of Australia (often in inaccessible country), it is unlikely the parasite could ever be eradicated. The best that could be expected is to undertake practical control measures as required and rely on good public education. Control measures could include the use of the EG95 vaccine [20] in sheep on farms adjacent to parks and forests containing wild dogs, the use of praziquantel baits around camping grounds in parks and forests and the removal of foxes and wild dogs from urban areas. Acknowledgment This paper is dedicated to the memory of Dr. D.D. Banks. References [1] Jenkins DJ. Hydatid control in Australia: where it began, what we have achieved and where to from here. Int J Parasitol 2005;35:733 – 40. [2] Corbett L. The dingo in Australia and Asia. Sydney’ University of New South Wales Press; 1995. [3] Jenkins DJ, Macpherson CNL. Transmission ecology of Echinococcus in Australia and Africa. Parasitology 2003;127:S63 – 72. [4] Beard T, Bramble AJ, Middleton MJ. Eradication in our time: a log book of the Tasmanian hydatid control programs, 1962 – 1996. Hobart’ Department of Primary Industry, Water and Environment; 2001. [5] Jenkins DJ, Morris B. Echinococcus granulosus in wildlife in and around the Kosciuszko National Park. Aust Vet J 2003;81:81 – 5. [6] Jenkins DJ, Morris B. Unusually heavy infection of Echinococcus granulosus in wild dogs in south eastern Australia. Aust Vet J 1991; 68:36 – 7.
[7] Durie PH, Riek RF. The role of the dingo and wallaby in the infestation of cattle with hydatids (Echinococcus granulosus (Batsch1786) Rudolphi 1805) in Queensland. Aust Vet J 1995;28:249 – 54. [8] Banks DD. Epidemiology of Echinococcus granulosus in Tropical Queensland. PhD Thesis, James Cook University of North Queensland 1984. [9] Baldock FC, Thompson RCA, Kumaratilake LM, Shield J. Echinococcus granulosus in farm dogs and dingoes in south eastern Queensland. Aust Vet J 1985;62:335 – 7. [10] Brown B, Copeman DB. Zoonotic importance of parasites in wild dogs caught in the vicinity of Townsville. Aust Vet J 2003;81:700 – 2. [11] Johnson PM, Spear R, Beveridge I. Mortality in wild and captive rockwallabies and nailtail wallabies due to hydatid disease caused by Echinococcus granulosus. Aust Mammal 1998;20:419 – 23. [12] Grainger J, Jenkins DJ. Transmission of hydatid disease to sheep from wild dogs in Victoria. Int J Parasitol 1996;26:1263 – 70. [13] Jenkins DJ, Thompson RCA. Hydatid cyst development in an experimentally infected wild rabbit. Vet Rec 1995;137:148 – 9. [14] Jenkins DJ, Craig N. The role of foxes (Vulpes vulpes) in the epidemiology of Echinococcus granulosus in urban environments. Med J Aust 1992;157:754 – 6. [15] Jenkins DJ, Murray AJ, Claridge AW, Story GA, Bradshaw H, Craig PS. The contribution of spotted-tailed quolls (Dasyurus maculatus) to the transmission of Echinococcus granulosus in the Byadbo Wilderness Area, Koscuiszko National Park, Australia. Wldf Res 2005;32:37 – 41. [16] Jenkins DJ, He D, McKinlay A, Bradshaw H, Craig PS. Detection of Echinococcus granulosus coproantigens in faeces from naturally infected rural domestic dogs in south eastern New South Wales and eastern Victoria, Australia. Aust Vet J in press. [17] Jenkins DJ, Power K. Human hydatidosis in New South Wales and the Australian capital territory, 1987 – 1992. Med J Aust 1996;164:18 – 21. [18] Hope M, Bowles J, Prociv P, McManus DP. A genetic comparison of human and wildlife isolates of Echinococcus granulosus in Queensland: public health implications. Med J Aust 1992;156:27 – 30. [19] Schelling U, Frank W, Will R, Romig T, Lucius R. Chemotherapy with praziquantel has the potential to reduce the prevalence of Echinococcus multilocularis in wild foxes (Vulpes vulpes). Ann Trop Med Parasitol 1997;91:179 – 86. [20] Lightowlers MW, Jensen O, Fernandez E, Iriate JA, Woolard DJ, Gaucci CG, et al. Vaccination trials in Australia and Argentina confirm the effectiveness of the EG95 vaccine in sheep. Int J Parasitol 1999; 29:531 – 4.
Echinococcus granulosus in Australia, widespread and doing well! David J. Jenkins * Australian Hydatid Control & Epidemiology Program, 12 Mildura Street, Fyshwick, ACT 2609, Australia School of Botany of Botany and Zoology and Faculty of Medicine, Australian National University, Canberra, ACT 0200, Australia Available online 13 December 2005
Abstract Echinococcus granulosus is the only member of the Genus Echinococcus to occur in Australia. The major biomass of E. granulosus occurs in wildlife. The wildlife transmission cycle is predominantly perpetuated via a predator/prey interaction between wild dogs (dingoes and dingo/ domestic dog hybrids) and macropodid marsupials (wallabies and kangaroos). Other wildlife hosts include foxes, wombats and feral pigs. This wildlife reservoir for E. granulosus ‘‘spills over’’ to help maintain a domestic cycle through E. granulosus-infected wild dogs defecating on pasture, transmitting infection to livestock and some farmers and hunters feeding hydatid-infected offal of macropodids or feral pigs to domestic dogs. The potential transmission risk to humans using public picnic and camping areas in parks and forests, especially in the southeastern Australia, could be substantially reduced through regular distribution of baits containing praziquantel. Encroachment of wild dogs and foxes into urban centers presents a new potential path of transmission from wildlife to humans. D 2005 Elsevier Ireland Ltd. All rights reserved. Keywords: Echinococcus granulosus; Australia; Wildlife; Wild dogs; Dingoes; Kangaroos; Wallabies; Domestic dogs; Thylacines; Human; Infection; Control
1. Introduction Echinococcus granulosus can be found on all continents of the world, an impressive feat for a parasite with limited means of locomotion that originated in the northern hemisphere. The international migration of E. granulosus to the continents of the southern hemisphere was achieved in association with translocation of domestic animals (sheep and dogs) during various phases of European colonisation. Sheep first arrived in Australia in 1788 but the earliest introductions were unsuccessful. However, Spanish merinos adapted well and by 1860 Australia had a population of 20 million merinos [1]. Through complete ignorance of the transmission pattern and public health importance of E. granulosus plus the abundance of potential animal hosts, E. granulosus spread quickly in livestock and dogs in Australia and by the1860s, human hydatidosis was a major public health issue in the new colony [1]. Of great importance for the establishment and perpetuation of E. granulosus in Australia was the ability of the parasite to * Australian Hydatid Control & Epidemiology Program, 12 Mildura Street, Fyshwick, ACT 2609, Australia. Tel.: +61 2 6271 6331; fax: +61 2 6272 3124. E-mail address: [email protected]. 1383-5769/$ - see front matter D 2005 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.parint.2005.11.031
also incorporate Australian native wildlife into its transmission pattern. Non-marsupial dingoes (Canis lupus dingo), the toporder predator present in Australia at the time of European settlement, had arrived 4000– 5000 years previously from southeastern Asia and displaced the thylacine (Thylacinus cynocephalus), the original marsupial top-order predator [2]. The importance of the dingo, in respect of E. granulosus transmission, was that it was a canid, highly susceptible to infection with E. granulosus and large enough to predate on sheep. The dominant native herbivorous fauna in Australia at the time of European settlement were macropodid marsupials (kangaroos and wallabies) that had evolved in isolation in Australia and were highly susceptible to infection with E. granulosus. Transmission of E. granulosus into wildlife is likely to have occurred first through macropodids becoming infected by accidental ingestion of eggs of E. granulosus passed by domestic dogs, and dingoes predating on hydatidinfected sheep. It has been proposed that transmission of E. granulosus to Australian wildlife was greatly assisted by transhumant grazing of sheep, an agricultural practice that persisted in eastern Australia until 1972 [3]. A major recent achievement in the control of E. granulosus in Australia has been the provisional eradication of E. granulosus from Tasmania. This impressive achievement was
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the result of more than 30 years of concerted, well-funded and organised hydatid control, backed up by state legislation [4].The most important factors contributing to the success of the Tasmanian campaign were that wildlife never became involved in transmission and, as an island, the control area was manageable and movements of animals into Tasmania could easily be controlled [1]. Domestic dogs and livestock still become infected with E. granulosus on mainland Australia but the prevalence is lower than 50 years ago [1]. However, the main source of infection for domestic animals today is via wildlife [3] rather than through a domestic animal transmission pattern. Therefore, the emphasis of this paper will be on transmission of E. granulosus within the wildlife reservoir, including circumstances where the wildlife reservoir may ‘‘overflow’’ into domestic animals. 2. E. granulosus transmission in wildlife The transmission pattern for E. granulosus in Australian wildlife is maintained through a predator/prey interaction between wild dogs (dingoes and dingo/domestic dog [Canis familiaris] hybrids), foxes (Vulpes vulpes) and macropodid marsupials [5], wombats (Wombatus ursinus) and feral pigs (Sus scrofa). Data indicate E. granulosus can utilise whatever hosts are available, transmitting between wildlife and domestic animals and also to humans [3]. 2.1. Wild dogs Dingo hybrids are similarly susceptibility to E. granulosus as pure-bred dingoes [5,6]. The prevalence of E. granulosus in wild dogs, particularly in eastern Australia, is high with prevalence levels ranging between 25% and 100% in Victoria and New South Wales [5] and between 76% and 100% in eastern Queensland [7– 9]. The worm burdens in wild dogs in southeastern Australia are commonly up to 10,000 worms but burdens greater than 50,000 to 100,000 worms occur regularly [5]. Heavier burdens, up to 300,000 worms, have been recorded [6]. Wild dogs represent the most important definitive host for transmission of E. granulosus in Australia today. 2.2. Wild dogs in urban areas A recent development in the behaviour of wild dogs in Queensland has been incursions of wild dogs, some E. granulosus infected, into urban habitats, Townsville [10], northwestern Brisbane (Jenkins and Shield, unpublished data) and the Sunshine Coast (Jenkins and Allen, unpublished data). These ‘‘urban’’ wild dogs scavenge rubbish bins, defecate in gardens and have been reported killing domestic pets. Apart from the public nuisance, the presence of E. granulosusinfected wild dogs in residential areas is a potentially important public health issue. Brown and Copeman [10] reported E. granulosus in 6 of 20 wild dogs examined from Townsville and Jenkins and Allen (unpublished data) have found 11 infected of 44 wild dogs examined from the Sunshine Coast. Worm burden data were unavailable from the Townsville wild dogs, but the
worm burdens in the 11 Gold Coast dogs ranged between 120 and 10,950 worms. 2.3. Macropodids Kangaroos and wallabies are the most widespread wildlife intermediate hosts for E. granulosus in eastern Australia, consisting of three main species, eastern grey kangaroos (Macropus giganteus), red-necked wallabies (Macropus rufogriseus) and swamp wallabies (Wallabia bicolor). Of all intermediate macropod hosts examined in southeastern Australia, the highest prevalence of infection (over 60%) and the highest cyst fertility has been found in swamp wallabies [5]. Swamp wallabies are of importance in the transmission pattern of E. granulosus because they are a favoured food item of wild dogs [5]. The site of predilection for E. granulosus metacestodes in macropodids is in the lungs, which may render infected animals more susceptible to predation, through compromised lung function [6]. Durie and Riek [7] reported catching a sick red-necked wallaby by hand, that was later found infected with a large lung hydatid cyst. The authors believed the cyst to be the cause of the incapacity of this animal. Johnson et al. [11] reported deaths of Queensland rock wallabies and nailtail wallabies due to pulmonary hydatidosis and most recently (2004), pulmonary hydatidosis has also been reported as the cause of death of brush-tailed rock wallabies in two different, closely monitored colonies in Queensland (Barnes, personal communication). Swamp wallabies are common throughout eastern Australia, particularly along The Great Dividing Range and they are pivotal in the successful transmission of E. granulosus in wildlife [3]. However, their importance as an intermediate host may vary in some local areas. South of Charters Towers, North Queensland, where swamp wallabies were rare, Banks [8] found a high prevalence of hydatid infection (22%) in black-striped wallabies (Macropus dorsalis). A range of other macropodid marsupial species are also susceptible to hydatidosis. These include the bridled nailtail wallabies (Onychogalea fraenata), rock wallabies (Petrogale persephone; Petrogale mareeba), red-necked wallabies (M. rufogriseus), whiptail wallabies (Macropus parryi) and pademelons (Thylogale stigmatica) [3]. 2.4. Wombats Hydatidosis has only been reported in wombats from Victoria [12]. The cysts recovered from the Victorian wombats, as with macropods, contained many protoscoleces and were all located in the lungs. Although wombats are also a favoured dietary item of dingoes, the apparent low prevalence or absence of hydatid infection in wombats from many areas suggests they may be considered as an intermediate host of only local importance. 3. Introduced wildlife The introduction of rabbits (Oryctolagus cunniculus) and foxes (V. vulpes) into Australia and the establishment of feral
D.J. Jenkins / Parasitology International 55 (2006) S203 – S206
pigs (S. scrofa) provided several potential new hosts into the wildlife transmission pattern. 3.1. Lagomorphs Rabbits occur in large numbers throughout much of Australia and occasional unconfirmed reports of hydatid infection in wild rabbits appear in the Australian historical scientific literature, but these reports are likely to have been descriptions of metacestodes of Taenia serialis. In a single experimental study Jenkins and Thompson [13] induced hydatid infection in only one of five wild-caught rabbits challenged with 500– 6000 eggs. The infected rabbit received 6000 eggs. The lack of confirmed reports of hydatid infection in wild rabbits suggests they are not naturally involved in transmission in Australia. 3.2. Feral pigs Feral pigs are numerous in much of Australia except the arid center. Hydatid infection in feral pigs is common in many areas of eastern and parts of Western Australia, but cyst fertility is usually low. Wild dogs have a preference for hunting young pigs whose cysts are likely to be immature, suggesting that the contribution of feral pigs to the transmission of E. granulosus in Australia is modest [3]. 3.3. Foxes Foxes infected with E. granulosus have been found widely in southeastern Australia [3]. Only a few individuals are infected in each population, but in one area, prevalence reached 46% [5]. Worm burdens of infected foxes are low (usually less than 50 worms); therefore, the contribution of foxes in contaminating the bush with eggs of E. granulosus, compared with wild dogs, is small. However, where E. granulosusinfected foxes infiltrate urban centers, the few eggs distributed by infected animals may be of more public health importance than is currently appreciated, particularly in the vicinity of popular public barbecue/picnic sites [14].
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like dingoes, predated on sheep. However, despite thylacines predating on sheep, and there being abundant macropodids of several species living in Tasmania, E. granulosus never established in Tasmanian wildlife. It is tempting to suggest that thylacines, like the species of dasyurids mentioned above, may have also been refractory to infection with E. granulosus and unable to act as the transmission conduit between sheep and macropodids. 5. Transmission of E. granulosus to domestic animals and humans via wildlife In a recently reported coproantigen study in rural dogs [16, in press], 29% of 344 dogs in New South Wales and 18% of 218 Victorian dogs tested positive. Most of the E. granulosus coproantigen-positive dogs occurred on farms possessing more than 5 dogs, where farmers commonly supplemented feeding commercial dry dog food with wildlife carcasses. Wild dogs have been implicated in the transmission of E. granulosus to sheep [12] and cattle [8] and anecdotally once in feral goats (Thompson, personal communication). However, an experimental infection study with feral and angora goats, using eggs from E. granulosus grown in dingoes experimentally infected with protoscoleces obtained from a kangaroo, resulted only with infection in the angora goats (Jenkins, unpublished data). These data suggest feral goats may not be acting as intermediate hosts for E. granulosus in Australia. In view of the high prevalence of E. granulosus in Australian wild dogs, it is not unreasonable to speculate that a proportion of human cases occurring in rural Australia are wildlife derived [17]. However, the long latent period from infection to diagnosis makes it difficult to conclusively link cases of human hydatidosis to contact with wildlife. In two cases investigated in Queensland, cyst material was shown to be genetically indistinguishable from E. granulosus cyst and adult worm tissue from wildlife [18]. One patient had admitted to contact, for 9 years, with domestic dogs fed offal from macropodids, whilst the other had had contact with a wildcaught dingo pup 5 years previously. Other reports of hydatid transmission from wildlife to humans have been reviewed by Jenkins and Macpherson [3].
4. Native Carnivores 4.1. Dasyurids
6. Use of praziquantel baits to treat wild canids around camping grounds
A recent survey of E. granulosus coproantigens in the faeces of wild, spotted-tailed quolls (Dasyrurus maculatus) failed to detect a positive sample, despite finding the remains of swamp wallaby (W. bicolor), in the faeces of some of the quolls [15]. Previous attempts to experimentally infect other dasyrurid species, namely, the Tasmanian devil (Sarcophilus harrisii) and the crest-tailed marsupial rat (Dasyuroides burnei), were unsuccessful [15], suggesting dasyruids, as a group, may be refractory to infection with E. granulosus. Thylacines were dasyurids and still common in Tasmania when Europeans arrived. Hydatid disease was present in Tasmanian sheep during settlement (as it was in mainland sheep) and thylacines,
In many parts of eastern Australia, the use of parks and forests by the general public and tourists for activities such as camping and barbecues (in designated areas) is becoming more popular. Dingoes and foxes are attracted to these places to scavenge food scraps once campers have departed. If a campsite or picnic area occurs in the home range of a pack of wild dogs and/or a fox, the highly territorial nature of these species ensures the same animals visit the area repeatedly. This presents a realistic opportunity to control E. granulosus infection in these animals through the use of baits containing praziquantel being distributed at 4 –6 weekly intervals in and around these bush recreational areas. Praziquantel baits have
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been used for treating wild red foxes (V. vulpes) in a trial in Germany. The study clearly demonstrated the possibility of substantially reducing the prevalence of E. multilocularis in wild foxes [19] through the use of medicated baits. However, this effect could only be sustained with continued regular use of praziquantel baits, once baiting ceased foxes became reinfected within a few months. 7. Prospects Since E. granulosus occurs commonly in wildlife over a large part of Australia (often in inaccessible country), it is unlikely the parasite could ever be eradicated. The best that could be expected is to undertake practical control measures as required and rely on good public education. Control measures could include the use of the EG95 vaccine [20] in sheep on farms adjacent to parks and forests containing wild dogs, the use of praziquantel baits around camping grounds in parks and forests and the removal of foxes and wild dogs from urban areas. Acknowledgment This paper is dedicated to the memory of Dr. D.D. Banks. References [1] Jenkins DJ. Hydatid control in Australia: where it began, what we have achieved and where to from here. Int J Parasitol 2005;35:733 – 40. [2] Corbett L. The dingo in Australia and Asia. Sydney’ University of New South Wales Press; 1995. [3] Jenkins DJ, Macpherson CNL. Transmission ecology of Echinococcus in Australia and Africa. Parasitology 2003;127:S63 – 72. [4] Beard T, Bramble AJ, Middleton MJ. Eradication in our time: a log book of the Tasmanian hydatid control programs, 1962 – 1996. Hobart’ Department of Primary Industry, Water and Environment; 2001. [5] Jenkins DJ, Morris B. Echinococcus granulosus in wildlife in and around the Kosciuszko National Park. Aust Vet J 2003;81:81 – 5. [6] Jenkins DJ, Morris B. Unusually heavy infection of Echinococcus granulosus in wild dogs in south eastern Australia. Aust Vet J 1991; 68:36 – 7.
[7] Durie PH, Riek RF. The role of the dingo and wallaby in the infestation of cattle with hydatids (Echinococcus granulosus (Batsch1786) Rudolphi 1805) in Queensland. Aust Vet J 1995;28:249 – 54. [8] Banks DD. Epidemiology of Echinococcus granulosus in Tropical Queensland. PhD Thesis, James Cook University of North Queensland 1984. [9] Baldock FC, Thompson RCA, Kumaratilake LM, Shield J. Echinococcus granulosus in farm dogs and dingoes in south eastern Queensland. Aust Vet J 1985;62:335 – 7. [10] Brown B, Copeman DB. Zoonotic importance of parasites in wild dogs caught in the vicinity of Townsville. Aust Vet J 2003;81:700 – 2. [11] Johnson PM, Spear R, Beveridge I. Mortality in wild and captive rockwallabies and nailtail wallabies due to hydatid disease caused by Echinococcus granulosus. Aust Mammal 1998;20:419 – 23. [12] Grainger J, Jenkins DJ. Transmission of hydatid disease to sheep from wild dogs in Victoria. Int J Parasitol 1996;26:1263 – 70. [13] Jenkins DJ, Thompson RCA. Hydatid cyst development in an experimentally infected wild rabbit. Vet Rec 1995;137:148 – 9. [14] Jenkins DJ, Craig N. The role of foxes (Vulpes vulpes) in the epidemiology of Echinococcus granulosus in urban environments. Med J Aust 1992;157:754 – 6. [15] Jenkins DJ, Murray AJ, Claridge AW, Story GA, Bradshaw H, Craig PS. The contribution of spotted-tailed quolls (Dasyurus maculatus) to the transmission of Echinococcus granulosus in the Byadbo Wilderness Area, Koscuiszko National Park, Australia. Wldf Res 2005;32:37 – 41. [16] Jenkins DJ, He D, McKinlay A, Bradshaw H, Craig PS. Detection of Echinococcus granulosus coproantigens in faeces from naturally infected rural domestic dogs in south eastern New South Wales and eastern Victoria, Australia. Aust Vet J in press. [17] Jenkins DJ, Power K. Human hydatidosis in New South Wales and the Australian capital territory, 1987 – 1992. Med J Aust 1996;164:18 – 21. [18] Hope M, Bowles J, Prociv P, McManus DP. A genetic comparison of human and wildlife isolates of Echinococcus granulosus in Queensland: public health implications. Med J Aust 1992;156:27 – 30. [19] Schelling U, Frank W, Will R, Romig T, Lucius R. Chemotherapy with praziquantel has the potential to reduce the prevalence of Echinococcus multilocularis in wild foxes (Vulpes vulpes). Ann Trop Med Parasitol 1997;91:179 – 86. [20] Lightowlers MW, Jensen O, Fernandez E, Iriate JA, Woolard DJ, Gaucci CG, et al. Vaccination trials in Australia and Argentina confirm the effectiveness of the EG95 vaccine in sheep. Int J Parasitol 1999; 29:531 – 4.