Register      Login
Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

Zoonotic and economically significant pathogens of peri-urban wild dogs across north-eastern New South Wales and south-eastern Queensland, Australia

Lana Harriott https://orcid.org/0000-0002-9058-5668 A B E , Matthew Gentle B , Rebecca Traub C , Ricardo J. Soares Magalhães A D and Rowland Cobbold A
+ Author Affiliations
- Author Affiliations

A School of Veterinary Science, University of Queensland, Gatton, Qld 4343, Australia.

B Pest Animal Research Centre, Biosecurity Queensland, Department of Agriculture and Fisheries, 203 Tor Street, Toowoomba, Qld 4350, Australia.

C Faculty of Veterinary and Agricultural Science, University of Melbourne, Parkville, Vic. 3010, Australia.

D Child Health Research Centre, University of Queensland, South Brisbane, Qld 4101, Australia.

E Corresponding author. Email: Lana.Harriott@daf.qld.gov.au

Wildlife Research 46(3) 212-221 https://doi.org/10.1071/WR18110
Submitted: 6 July 2018  Accepted: 18 January 2019   Published: 19 March 2019

Abstract

Context: Peri-urban wild dogs are known to reside within high-risk and densely populated regions and are capable of harbouring a variety of zoonotic pathogens. Despite recognising the potential of peri-urban wild dogs to carry zoonotic pathogens, limited prevalence data are currently available to assist in understanding the potential risks that peri-urban wild dogs pose within developed communities.

Aims: The aim of the present research was to establish the current status of key zoonotic and economically significant pathogens in peri-urban wild dogs.

Methods: Two hundred and one peri-urban wild dog cadavers were collected from south-eastern Queensland and northern New South Wales. In addition, whole blood, serum and faecal samples were also collected. Pathogens were identified through several morphological, microbiological and molecular methods.

Key results: Helminth parasites were detected within 79.6% of peri-urban wild dogs; Echinococcus granulosus was the most common pathogen, with adult worms being detected within 50.7 ± 6.9% of intestines, followed by Spirometra erinacei (36.6 ± 6.4%); hookworms, including Ancylostoma caninum and Uncinaria stenocephala (28.8 ± 7.1%); Toxocara canis (5.4 ± 3.1%) and Taenia spp., including T. serialis and T. pisiformis (4.5 ± 2.8%). Bacterial pathogens detected included methicillin-resistant Escherichia coli (20.0 ± 10.1%), Salmonella spp. (3.7 ± 4.0%) and methicillin-sensitive Staphylococcus aureus (3.3 ± 2.7%).

Conclusions: The present study is the most comprehensive investigation of zoonotic pathogen carriage in peri-urban wild dogs in Australia. Parasitic infections in peri-urban wild dogs are common, with tapeworms representing the majority of intestinal pathogens. Important zoonotic bacterial pathogens are carried by peri-urban wild dogs, although at a much lower prevalence than are parasites.

Implications: The presence of these pathogens in free-ranging peri-urban dog populations suggests a strong potential for public health risk, most notably from E. granulosus. These data are inherently important as baseline information, which is essential to guide risk-based management of peri-urban wild dog impacts.

Additional keywords: disease, dingoes, parasites, bacteria, Echinococcus granulosus, free-ranging dogs.


References

ABS (2018). ‘3218.0: Regional Population Growth, Australia, 2016–17.’ Released 24 April 2018. Available at http://www.abs.gov.au/AUSSTATS/abs@.nsf/Lookup/3218.0Main+Features12016-17?OpenDocument [Verified 30 September 2018].

Allen, B. L., Goullet, M., Allen, L. R., Lisle, A., and Leung, L. K. P. (2013). Dingoes at the doorstep: preliminary data on the ecology of dingoes in urban areas. Landscape and Urban Planning 119, 131–135.
Dingoes at the doorstep: preliminary data on the ecology of dingoes in urban areas.Crossref | GoogleScholarGoogle Scholar |

Allen, B. L., Carmelito, E., Amos, M., Goullet, M. S., Allen, L. R., Speed, J., Gentle, M., and Leung, L. K. P. (2016). Diet of dingoes and other wild dogs in peri-urban areas of north-eastern Australia. Scientific Reports 6, 23028.
Diet of dingoes and other wild dogs in peri-urban areas of north-eastern Australia.Crossref | GoogleScholarGoogle Scholar | 26964762PubMed |

Arundel, J. H. (1972). A review of cysticercoses of sheep and cattle in Australia. Australian Veterinary Journal 48, 140–155.
A review of cysticercoses of sheep and cattle in Australia.Crossref | GoogleScholarGoogle Scholar | 4563121PubMed |

Baldock, F. C., Thompson, R. C., Kumaratilake, L. M., and Shield, J. (1985). Echinococcus granulosus in farm dogs and dingoes in south eastern Queensland. Australian Veterinary Journal 62, 335–337.
Echinococcus granulosus in farm dogs and dingoes in south eastern Queensland.Crossref | GoogleScholarGoogle Scholar | 4084146PubMed |

Bateman, P. W., and Fleming, P. A. (2012). Big city life: carnivores in urban environments. Journal of Zoology 287, 1–23.
Big city life: carnivores in urban environments.Crossref | GoogleScholarGoogle Scholar |

Bengsen, A. J., Gentle, M. N., Mitchell, J. L., Pearson, H. E., and Saunders, G. R. (2014). Impacts and management of wild pigs Sus scrofa in Australia. Mammal Review 44, 135–147.
Impacts and management of wild pigs Sus scrofa in Australia.Crossref | GoogleScholarGoogle Scholar |

Bowman, D. D. (2013). ‘Georgis’ Parasitology for Veterinarians.’ 10th edn. (Elsevier, Saunders: St Louis, MI.)

Brown, B., and Copeman, D. B. (2003). Zoonotic importance of parasites in wild dogs caught in the vicinity of Townsville. Australian Veterinary Journal 81, 700–702.
| 15086114PubMed |

Chen, J., Xu, M. J., Zhou, D. H., Song, H. Q., Wang, C. R., and Zhu, X. Q. (2012). Canine and feline parasitic zoonoses in China. Parasites & Vectors 5, 152–159.

Choy, D. L., and Buxton, M. (2013). Farming the city fringe: Dilemmas for peri-urban planning. In ‘Food Security in Australia: Challenges and Prospects for the Future’. (Eds Q. Farmar-Bowers, V. Higgins, and J. Millar.) pp. 397–412. (Springer US: Boston, MA.)

Claerebout, E., Casaert, S., Dalemans, A. C., De Wilde, N., Levecke, B., Vercruysse, J., and Geurden, T. (2009). Giardia and other intestinal parasites in different dog populations in northern Belgium. Veterinary Parasitology 161, 41–46.
Giardia and other intestinal parasites in different dog populations in northern Belgium.Crossref | GoogleScholarGoogle Scholar | 19155136PubMed |

Coman, B. J. (1972). Helminth parasites of the dingo and feral dog in Victoria with some notes on diet of the host. Australian Veterinary Journal 48, 456–461.
Helminth parasites of the dingo and feral dog in Victoria with some notes on diet of the host.Crossref | GoogleScholarGoogle Scholar | 4674382PubMed |

Congdon, P., and Lloyd, P. (2011). Toxocara infection in the United States: the relevance of poverty, geography and demography as risk factors, and implications for estimating county prevalence. International Journal of Public Health 56, 15–24.
Toxocara infection in the United States: the relevance of poverty, geography and demography as risk factors, and implications for estimating county prevalence.Crossref | GoogleScholarGoogle Scholar | 20422250PubMed |

Deplazes, P., van Knapen, F., Schweiger, A., and Overgaauw, P. A. M. (2011). Role of pet dogs and cats in the transmission of helminthic zoonoses in Europe, with a focus on echinococcosis and toxocarosis. Veterinary Parasitology 182, 41–53.
Role of pet dogs and cats in the transmission of helminthic zoonoses in Europe, with a focus on echinococcosis and toxocarosis.Crossref | GoogleScholarGoogle Scholar | 21813243PubMed |

Dybing, N. A., Fleming, P. A., and Adams, P. J. (2013). Environmental conditions predict helminth prevalence in red foxes in Western Australia. International Journal for Parasitology. Parasites and Wildlife 2, 165–172.
Environmental conditions predict helminth prevalence in red foxes in Western Australia.Crossref | GoogleScholarGoogle Scholar | 24533331PubMed |

Fajardo, V., Gonzalez, I., Martin, I., Rojas, M., Hernandez, P. E., Garcia, T., and Martin, R. (2008). Real-time PCR for detection and quantification of red deer (Cervus elaphus), fallow deer (Dama dama), and roe deer (Capreolus capreolus) in meat mixtures. Meat Science 79, 289–298.
Real-time PCR for detection and quantification of red deer (Cervus elaphus), fallow deer (Dama dama), and roe deer (Capreolus capreolus) in meat mixtures.Crossref | GoogleScholarGoogle Scholar | 22062757PubMed |

Faust, E. C., D’Antoni, J. S., Odom, V., Miller, M. J., Peres, C., Sawitz, W., Thomen, L. F., Tobie, J., and Walker, J. H. (1938). A critical study of clinical laboratory technics for the diagnosis of protozoan cysts and helminth eggs in feces: I. Preliminary communication. The American Journal of Tropical Medicine and Hygiene s1–18, 169–183.

Fish, L., Mazuz, M., Molad, T., Savitsky, I., and Shkap, V. (2007). Isolation of Neospora caninum from dairy zero grazing cattle in Israel. Veterinary Parasitology 149, 167–171.
Isolation of Neospora caninum from dairy zero grazing cattle in Israel.Crossref | GoogleScholarGoogle Scholar | 17850972PubMed |

Fleming, P. J. S., Allen, B. L., Allen, L. R., Ballard, G.-A., Bengsen, A., Gentle, M. N., McLeod, L., Meek, P. D., and Saunders, G. R. (2014). Management of wild canids in Australia: free-ranging dogs and red foxes. In ‘Carnivores of Australia: Past, Present and Future’. (Eds A. Glen and C. Dickson.) pp. 149–207. (CSIRO Publishing: Melbourne.)

Gibbs, H. C. (1982). Mechanisms of survival of nematode parasites with emphasis on hypobiosis. Veterinary Parasitology 11, 25–48.
Mechanisms of survival of nematode parasites with emphasis on hypobiosis.Crossref | GoogleScholarGoogle Scholar | 6891524PubMed |

Gibbs, H. C., and Gibbs, K. E. (1959). The effects of temperature on the development of the free-living stages of Dochmoides stenocephala (Railliet, 1884) (Ancylostomidae: Nematoda). Canadian Journal of Zoology 37, 247–257.
The effects of temperature on the development of the free-living stages of Dochmoides stenocephala (Railliet, 1884) (Ancylostomidae: Nematoda).Crossref | GoogleScholarGoogle Scholar |

Harriott, L. (2018). Prevalence, risk factors and geographical distribution of zoonotic pathogens carried by peri-urban wild dogs. PhD Thesis, School of Veterinary Science, The University of Queensland, Gatton, Qld.

Hii, S. F., Kopp, S. R., Abdad, M. Y., Thompson, M. F., O’Leary, C. A., Rees, R. L., and Traub, R. J. (2011). Molecular evidence supports the role of dogs as potential reservoirs for Rickettsia felis. Vector Borne and Zoonotic Diseases (Larchmont, N.Y.) 11, 1007–1012.
Molecular evidence supports the role of dogs as potential reservoirs for Rickettsia felis.Crossref | GoogleScholarGoogle Scholar |

Ing, M. B., Schantz, P. M., and Turner, J. A. (1998). Human coenurosis in North America: case reports and review. Clinical Infectious Diseases 27, 519–523.
Human coenurosis in North America: case reports and review.Crossref | GoogleScholarGoogle Scholar | 9770151PubMed |

Inpankaew, T., Schär, F., Khieu, V., Muth, S., Dalsgaard, A., Marti, H., Traub, R. J., and Odermatt, P. (2014). Simple fecal flotation is a superior alternative to quadruple Kato Katz smear examination for the detection of hookworm eggs in human stool. PLoS Neglected Tropical Diseases 8, e3313.
Simple fecal flotation is a superior alternative to quadruple Kato Katz smear examination for the detection of hookworm eggs in human stool.Crossref | GoogleScholarGoogle Scholar | 25521997PubMed |

Jenkins, D. J., and Morris, B. (1991). Unusually heavy infections of Echinococcus granulosus in wild dogs in south-eastern Australia Australian Veterinary Journal 68, 36–37.
Unusually heavy infections of Echinococcus granulosus in wild dogs in south-eastern AustraliaCrossref | GoogleScholarGoogle Scholar | 2018455PubMed |

Jenkins, D. J., Allen, L., and Goullet, M. (2008). Encroachment of Echinococcus granulosus into urban areas in eastern Queensland, Australia. Australian Veterinary Journal 86, 294–300.
Encroachment of Echinococcus granulosus into urban areas in eastern Queensland, Australia.Crossref | GoogleScholarGoogle Scholar | 18673469PubMed |

Jenkins, D. J., Lievaart, J. J., Boufana, B., Lett, W. S., Bradshaw, H., and Armua-Fernandez, M. T. (2014a). Echinococcus granulosus and other intestinal helminths: current status of prevalence and management in rural dogs of eastern Australia. Australian Veterinary Journal 92, 292–298.
Echinococcus granulosus and other intestinal helminths: current status of prevalence and management in rural dogs of eastern Australia.Crossref | GoogleScholarGoogle Scholar | 25066196PubMed |

Jenkins, D. J., Urwin, N. A. R., Williams, T. M., Mitchell, K. L., Lievaart, J. J., and Armua-Fernandez, M. T. (2014b). Red foxes (Vulpes vulpes) and wild dogs (dingoes (Canis lupus dingo) and dingo/domestic dog hybrids), as sylvatic hosts for Australian Taenia hydatigena and Taenia ovis. International Journal for Parasitology. Parasites and Wildlife 3, 75–80.
Red foxes (Vulpes vulpes) and wild dogs (dingoes (Canis lupus dingo) and dingo/domestic dog hybrids), as sylvatic hosts for Australian Taenia hydatigena and Taenia ovis.Crossref | GoogleScholarGoogle Scholar | 25161904PubMed |

Koenig, J., Shine, R., and Shea, G. (2001). The ecology of an Australian reptile icon: how do blue-tongued lizards (Tiliqua scincoides) survive in suburbia? Wildlife Research 28, 214–227.
The ecology of an Australian reptile icon: how do blue-tongued lizards (Tiliqua scincoides) survive in suburbia?Crossref | GoogleScholarGoogle Scholar |

Koichi, K., Sangha, K. K., Cottrell, A., and Gordon, I. J. (2012). Aboriginal rangers’ perspectives on feral pigs: are they a pest or a resource? A case study in the wet tropics World Heritage Area of northern Queensland. Journal of Australian Indigenous Issues 15, 2–19.

Lee, S. H., We, J. S., Sohn, W. M., Hong, S. T., and Chai, J. Y. (1990). Experimental life history of Spirometra erinacei. Korean Journal of Parasitology 28, 161–173.
Experimental life history of Spirometra erinacei.Crossref | GoogleScholarGoogle Scholar | 2095198PubMed |

Low Choy, D., Sutherland, C., Scott, S., Rolley, K., Gleeson, B., Dodson, J., and Sipe, N. (2007). ‘Change and Continuity in Peri-urban Australia. Peri-urban Case Study: South East Queensland.’ Urban Research Program. (Griffith University: Brisbane, Qld.)

Malik, S., Coombs, G. W., O’Brien, F. G., Peng, H., and Barton, M. D. (2006). Molecular typing of methicillin-resistant staphylococci isolated from cats and dogs. The Journal of Antimicrobial Chemotherapy 58, 428–431.
Molecular typing of methicillin-resistant staphylococci isolated from cats and dogs.Crossref | GoogleScholarGoogle Scholar | 16782740PubMed |

McNeill, A. T., Leung, L. K., Goullet, M. S., Gentle, M. N., and Allen, B. L. (2016). Dingoes at the doorstep: home range sizes and activity patterns of dingoes and other wild dogs around urban areas of north-eastern Australia. Animals (Basel) 6, e48.
Dingoes at the doorstep: home range sizes and activity patterns of dingoes and other wild dogs around urban areas of north-eastern Australia.Crossref | GoogleScholarGoogle Scholar | 27537916PubMed |

Morgan, E. R., Azam, D., and Pegler, K. (2013). Quantifying sources of environmental contamination with Toxocara spp. eggs. Veterinary Parasitology 193, 390–397.
Quantifying sources of environmental contamination with Toxocara spp. eggs.Crossref | GoogleScholarGoogle Scholar | 23333071PubMed |

Morrison, P., Stanton, R., and Pilatti, E. (1988). Echinococcus granulosus infection in wild dogs in south-eastern New South Wales. Australian Veterinary Journal 65, 97–98.
Echinococcus granulosus infection in wild dogs in south-eastern New South Wales.Crossref | GoogleScholarGoogle Scholar | 3401157PubMed |

Newsome, T. M., Ballard, G.-A., Dickman, C. R., Fleming, P. J. S., and van de Ven, R. (2013). Home range, activity and sociality of a top predator, the dingo: a test of the resource dispersion hypothesis. Ecography 36, 914–925.
Home range, activity and sociality of a top predator, the dingo: a test of the resource dispersion hypothesis.Crossref | GoogleScholarGoogle Scholar |

Ng-Nguyen, D., Stevenson, M. A., Dorny, P., Gabriël, S., Vo, T. V., Nguyen, V.-A. T., Phan, T. V., Hii, S. F., and Traub, R. J. (2017). Comparison of a new multiplex real-time PCR with the Kato Katz thick smear and copro-antigen ELISA for the detection and differentiation of Taenia spp. in human stools. PLoS Neglected Tropical Diseases 11, e0005743.
Comparison of a new multiplex real-time PCR with the Kato Katz thick smear and copro-antigen ELISA for the detection and differentiation of Taenia spp. in human stools.Crossref | GoogleScholarGoogle Scholar | 28686662PubMed |

Palmer, C. S., Traub, R. J., Robertson, I. D., Hobbs, R. P., Elliot, A., While, L., Rees, R., and Thompson, R. C. A. (2007). The veterinary and public health significance of hookworm in dogs and cats in Australia and the status of A. ceylanicum. Veterinary Parasitology 145, 304–313.
The veterinary and public health significance of hookworm in dogs and cats in Australia and the status of A. ceylanicum.Crossref | GoogleScholarGoogle Scholar | 17276602PubMed |

Palmer, C. S., Thompson, R. C. A., Traub, R. J., Rees, R., and Robertson, I. D. (2008). National study of the gastrointestinal parasites of dogs and cats in Australia. Veterinary Parasitology 151, 181–190.
National study of the gastrointestinal parasites of dogs and cats in Australia.Crossref | GoogleScholarGoogle Scholar | 18055119PubMed |

Prange, S., Gehrt, S. D., and Wiggers, E. P. (2003). Demographic factors contributing to high raccoon densities in urban landscapes. The Journal of Wildlife Management 67, 324–333.
Demographic factors contributing to high raccoon densities in urban landscapes.Crossref | GoogleScholarGoogle Scholar |

Regis, S. C., Mendonca, L. R., Silva Ndos, S., Dattoli, V. C., Alcantara-Neves, N. M., and Barrouin-Melo, S. M. (2011). Seroprevalence and risk factors for canine toxocariasis by detection of specific IgG as a marker of infection in dogs from Salvador, Brazil. Acta Tropica 120, 46–51.
Seroprevalence and risk factors for canine toxocariasis by detection of specific IgG as a marker of infection in dogs from Salvador, Brazil.Crossref | GoogleScholarGoogle Scholar | 21703221PubMed |

Schweiger, A., Ammann, R. W., Candinas, D., Clavien, P.-A., Eckert, J., Gottstein, B., Halkic, N., Muellhaupt, B., Prinz, B. M., Reichen, J., Tarr, P. E., Torgerson, P. R., and Deplazes, P. (2007). Human alveolar echinococcosis after fox population increase, Switzerland. Emerging Infectious Diseases 13, 878–882.
Human alveolar echinococcosis after fox population increase, Switzerland.Crossref | GoogleScholarGoogle Scholar | 17553227PubMed |

Smout, F. A., Thompson, R. C. A., and Skerratt, L. F. (2013). First report of Ancylostoma ceylanicum in wild canids. International Journal for Parasitology. Parasites and Wildlife 2, 173–177.
First report of Ancylostoma ceylanicum in wild canids.Crossref | GoogleScholarGoogle Scholar | 24533332PubMed |

Stafford, R. J., and Bell, R. (2011). Monitoring the incidence and causes of disease potentially transmitted by food in Australia: annual report of the OzFoodNet Network, 2011. Communicable Diseases Intelligence 39, e236–e264.

Statham, M., and Statham, H. L. (1997). Movements and habits of brushtail possums (Trichosurus vulpecula Kerr) in an urban area. Wildlife Research 24, 715–726.
Movements and habits of brushtail possums (Trichosurus vulpecula Kerr) in an urban area.Crossref | GoogleScholarGoogle Scholar |

Strommenger, B., Kehrenberg, C., Kettlitz, C., Cuny, C., Verspohl, J., Witte, W., and Schwarz, S. (2006). Molecular characterization of methicillin-resistant Staphylococcus aureus strains from pet animals and their relationship to human isolates. The Journal of Antimicrobial Chemotherapy 57, 461–465.
Molecular characterization of methicillin-resistant Staphylococcus aureus strains from pet animals and their relationship to human isolates.Crossref | GoogleScholarGoogle Scholar | 16387748PubMed |

Torgerson, P. R., and Heath, D. D. (2003). Transmission dynamics and control options for Echinococcus granulosus. Parasitology 127, S143–S158.
Transmission dynamics and control options for Echinococcus granulosus.Crossref | GoogleScholarGoogle Scholar | 15027611PubMed |

Traub, R. J., Robertson, I. D., Irwin, P., Mencke, N., and Thompson, R. C. A. (2004). Application of a species-specific PCR–RFLP to identify Ancylostoma eggs directly from canine faeces. Veterinary Parasitology 123, 245–255.
Application of a species-specific PCR–RFLP to identify Ancylostoma eggs directly from canine faeces.Crossref | GoogleScholarGoogle Scholar | 15325050PubMed |

Traub, R. J., Hobbs, R. P., Adams, P. J., Behnke, J. M., Harris, P. D., and Thompson, R. C. A. (2007). A case of mistaken identity: reappraisal of the species of canid and felid hookworms (Ancylostoma) present in Australia and India. Parasitology 134, 113–119.
A case of mistaken identity: reappraisal of the species of canid and felid hookworms (Ancylostoma) present in Australia and India.Crossref | GoogleScholarGoogle Scholar | 16987431PubMed |

Wachira, T. M., Macpherson, C. N., and Gathuma, J. M. (1991). Release and survival of Echinococcus eggs in different environments in Turkana, and their possible impact on the incidence of hydatidosis in man and livestock. Journal of Helminthology 65, 55–61.
Release and survival of Echinococcus eggs in different environments in Turkana, and their possible impact on the incidence of hydatidosis in man and livestock.Crossref | GoogleScholarGoogle Scholar | 2050986PubMed |

Wang, W., Cuttell, L., Bielefeldt-Ohmann, H., Inpankaew, T., Owen, H., and Traub, R. J. (2013). Diversity of Blastocystis subtypes in dogs in different geographical settings. Parasites & Vectors 6, 215.
Diversity of Blastocystis subtypes in dogs in different geographical settings.Crossref | GoogleScholarGoogle Scholar |

Weese, J. S., Dick, H., Willey, B. M., McGeer, A., Kreiswirth, B. N., Innis, B., and Low, D. E. (2006). Suspected transmission of methicillin-resistant Staphylococcus aureus between domestic pets and humans in veterinary clinics and in the household. Veterinary Microbiology 115, 148–155.
Suspected transmission of methicillin-resistant Staphylococcus aureus between domestic pets and humans in veterinary clinics and in the household.Crossref | GoogleScholarGoogle Scholar | 16464540PubMed |