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Unravelling the epidemiology of tick paralysis in Australia: Application of passive surveillance and GIS

Michael P. Ward1* and Mark R. Kelman1
  • 1 Sydney School of Veterinary Science, Faculty of Science, The University of Sydney, Australia

Introduction Tick paralysis is a neuromuscular disease, which occurs commonly in companion animals in endemic areas in Australia. The typical presentation is rapid ascending flaccid paralysis, with death occurring due to respiratory failure (Masina and Broady, 1999; Stone et al., 1986). It is a serious condition, and is distressing for pet owners. I. holocyclus is the most widespread tick species in Australia causing paralysis. It undergoes a 3-stage, approximately 3 year lifecycle consisting of both free living and host stages. Endemic areas of tick paralysis are found along the eastern seaboard of Australia, from Victoria to Queensland, particularly the coastal regions of New South Wales and southern Queensland (Eppleston et al., 2013). The distribution of I. holocyclus is defined by the presence of host species, climate and vegetation. Areas with high annual precipitation and high minimum average temperatures favour the free living stages of I. holocyclus (Heath, 1981), and low vegetation and scrub coverage provide protection (Doube, 1975; Eppleston et al., 2013). Brazier et al., 2014 An association between tick paralysis cases in pets within the urban environment of Brisbane, Queensland and parklands and recreational areas with natural vegetation has been reported (Gerasimova et al., 2018). Native wildlife – particularly bandicoots – are the natural hosts of I. holocyclus and are able to carry multiple ticks without being affected (Stone et al., 1989). Due to continuing habitat fragmentation from increasing urbanisation, these hosts have been brought into proximity with humans and consequently their pets (FitzGibbon and Jones, 2006). The objective of the current study was to determine whether evidence exists to support the anecdotal association between the distribution of the long-nosed bandicoot (Perameles nasuta) and occurrence of tick paralysis cases in pet dogs. Materials and methods Cases of canine and feline tick paralysis reported by Australian veterinarians were sourced from Disease WatchDog (Ward and Kelman, 2011). This passive surveillance system was designed to allow veterinarians and their staff to report on a range of common disease conditions in dogs and cats. Data included case date, residential postcode and Australian state, and number of cases. Cases were restricted to those canine cases with a reported date of diagnosis between 1 January 2011 and 31 December 2016 (5 complete years of data reporting), with a residential state of New South Wales (including the Australian Capital Territory, which is entirely surrounded by New South Wales). The number of cases reported from each postcode were summed. This distribution of cases reported per postcode was then joined with a postcode polygon shape file (WDA 1994; ArcMap 10.5, Redlands CA) and a symbol map proportional to number of cases reported was created. The predicted distribution of bandicoots was derived from a study described by Simpson et al. (2019). Briefly, occurrences of long-nosed bandicoots (Perameles nasuta) were obtained from the Global Biodiversity Information Facility (www.gbif.org). The ecological niche of bandicoots was then quantified using a Maxent machine learning algorithm, using the following variables (ranked in order of importance): precipitation (wettest quarter), distance to open shrubland, disease to barren/sparsely vegetated areas, distance to permanent wetlands and mean temperature (coolest quarter). This model produced an area under the curve of 0.859 (Simpson et al., 2019; Appendix A, Supplementary file 1, Table 1). The resulting bandicoot niche probability function raster was converted to a binary raster with the value 1 (i.e. suitable habitat) if the probability of species habitat suitability was ≥0.85 and 0 (i.e. unsuitable habitat) if the probability was <0.85 (Simpson et al., 2019). The raster map of bandicoot habitat suitability was then joined with the polygon map of reported tick paralysis cases by postcode. For each postcode, the mean, minimum and maximum bandicoot habitat suitability metrics were extracted. The association between reported tick paralysis cases and bandicoot habitat suitability was explored using Spearman rank correlation (Statistix 8.0. Analytical Software, Tallahassee FL). Results A total of 13,782 cases of tick paralysis were reported in Disease WatchDog; 11,998 (87%) of these were reported during the study period, and of these, 7,916 (66%) were reported from New South Wales (including the Australian Capital Territory). There were 6,123 cases reported in dogs during the study period and from the study area, and this subset of data was used in further analyses. Cases were reported from 199 postcodes within New South Wales (including the Australian Capital Territory). This ranged from one to 983 cases. The distribution of cases reported per postcode was skewed: mean 31 (95% CI, 16─45) and median 4 (interquartile range, 1─19). Cases were predominantly reported from eastern coastal area of New South Wales (Figure 1A), but the distribution did not display global spatial clustering (Moran’s I = 0.04, P = 0.5582), with. Large numbers of cases (>200) were reported from postcodes on the north coast (2450 – 983; 2484 – 306; 2463 – 204), central coast (2259 – 262; 2290 – 210) and south coast (2540 – 545; 2537 – 752). These 7 postcodes accounted for >50% of all reported cases. Bandicoot habitat suitability is shown in Figure 1B. For all 628 postcodes in New South Souths (including the Australian Capital Territory), the correlation between the number of cases reported and the minimum, mean and maximum bandicoot habitat suitability index was 0.201, 0.438 and 0.519, respectively. All correlations were significantly (P<0.0001) > 0. For the subset of 199 postcodes from which one or more cases of tick paralysis were reported, the correlation between the number of cases reported and the minimum, mean and maximum bandicoot habitat suitability index was 0.152, 0.369 and 0.453, respectively. Again, all correlations were significantly (P<0.0001) > 0. Conclusions Anecdotally, bandicoots have been suggested as a reservoir species of I. holocyclus, and therefore it has been assumed that areas supporting larger populations of this bandicoots present a greater risk of tick paralysis in pet populations residing within these areas. The current study provides evidence to support this hypothesis. However, it is an ecological study and other factors might confound the moderately strong associations found. In addition, surveillance bias might exist whereby veterinarians residing in areas of large bandicoot population might be more likely to report cases of tick paralysis in pet animals. Nevertheless, the evidence that bandicoots play a role in tick paralysis in pets residing in the same area is compelling.

Figure 1
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Acknowledgements

Kelly Simpson is thanked for making the bandicoot habitat suitability raster available.

References

Brazier, I., Ward, M.P., Kelman, M., 2014. The association between landscape and climate and reported tick paralysis cases in dogs and cats in Australia. Veterinary Parasitology 204, 339–345 Doube, B.M., 1975. Cattle and the paralysis tick Ixodes holocyclus. Australian Veterinary Journal 51, 511–515. Eppleston, K.R., Ward, M.P., Kelman, M., 2013. Distribution, seasonality and risk factors for tick paralysis in Australian dogs and cats. Veterinary Parasitology 196, 460–468. FitzGibbon, S.I., Jones, D.N., 2006. A community-based wildlife survey: the knowledge and attitudes of residents of suburban Brisbane, with a focus on bandicoots. Wildlife Research 33, 233–241. Gerasimova, M., Kelman, M., Ward, M.P. Are recreational areas a risk factor for tick paralysis in urban environments? Veterinary Parasitology 2018; 254: 7277 Heath, A.C.G., 1981. The temperature and humidity preferences of Haemaphysalis longicornis, ixodes holocyclus and Rhipicephalus sanguineus (ixodidae): Studies on engorged larvae. International Journal of Parasitology 11, 169–175 Masina, S., Broady, K.W., 1999. Tick paralysis: development of a vaccine. International Journal of Parasitology 29, 535–541. Simpson, K.M.J., Mor, S.M., Ward, M.P., Walsh, M.G., 2019. Divergent geography of Salmonella Wangata and Salmonella Typhimurium epidemiology in New South Wales, Australia. One Health 7, 100092. Stone, B.F., Uren, M.F., Neish, A.L., Morrison, J.J., 1986. Toxoid stimulation in dogs of high titres of neutralising antibodies against holocyclotoxin, the paralysing toxin of the Australian paralysis tick Ixodes holocyclus. Australian Veterinary Journal 63, 125–127. Ward, M.P., Kelman, M., 2011. Companion animal disease surveillance: A new solution to an old problem? Spatial and Spatiotemporal Epidemiology 2, 147–157.

Keywords: Tick Paralysis, Dogs, Passive surveillance systems, wildlife, Australia

Conference: GeoVet 2019. Novel spatio-temporal approaches in the era of Big Data, Davis, United States, 8 Oct - 10 Oct, 2019.

Presentation Type: Regular oral presentation

Topic: Spatio-temporal surveillance and modeling approaches

Citation: Ward MP and Kelman MR (2019). Unravelling the epidemiology of tick paralysis in Australia: Application of passive surveillance and GIS. Front. Vet. Sci. Conference Abstract: GeoVet 2019. Novel spatio-temporal approaches in the era of Big Data. doi: 10.3389/conf.fvets.2019.05.00017

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Received: 05 Jun 2019; Published Online: 27 Sep 2019.

* Correspondence: Prof. Michael P Ward, Sydney School of Veterinary Science, Faculty of Science, The University of Sydney, Sydney, New South Wales, Australia, michael.ward@sydney.edu.au