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MURDOCH RESEARCH REPOSITORY

This is the author’s final version of the work, as accepted for publication following peer review but without the publisher’s layout or pagination. The definitive version is available at http://dx.doi.org/10.1016/j.pt.2013.09.006

Thompson, R.C.A. (2014) Parasites and : ripe for exploitation. Trends in Parasitology, 30 (1). pp. 1-3.

http://researchrepository.murdoch.edu.au/20310/

Copyright: 2013 Elsevier Ltd.

Parasites and food: ripe for exploitation

R.C. Andrew Thompson

School of Veterinary and Life Sciences, Murdoch University, Murdoch, WA 6150, Australia

Parasites are often exploited for emotive or political purposes. This is especially so for a number of foodborne parasitic zoonoses, where this exploitation may not necessarily best serve the public good.

Keywords: Toxoplasma; Taenia solium; Trichinella; foodborne; media; politics

The media

Toxoplasma must be one of the most susceptible parasites for media exploitation. The association of Toxoplasma with congenital disease and abortion during pregnancy was understood from the late

1930s but once the role of the cat as the definitive host was reported in 1969 [1] the cat has been vilified in the media with alarmist and often misleading reports. Admittedly, it has taken longer to determine the importance of foodborne transmission in the epidemiology of Toxoplasma infections in humans, but this risk factor has been known for at least the past 30 years. Cats generally shed oocysts only once in their lifetime, for a period of approximately 2 weeks [2], and thus the chances of transmission to humans is limited although oocysts can survive in the environment for variable periods depending on temperature and moisture (reviewed in [3]). Given the diversity of intermediate hosts that can act as sources of meat for human consumption and the reported high rates of infection in various domestic and wild food animals globally, transmission via food is an important risk factor.

Further, transmission is not necessarily as a consequence of eating raw or undercooked meat, but handling meat during food preparation and not washing hands is also an important risk factor

(reviewed in [3]). But, it would seem that given the chance, the media will grasp the opportunity to denigrate the cat and distort the facts knowing that the emotional aspects will guarantee a readership. This happened recently following the release of a UK Government report by the Food Standards

Agency on Toxoplasma in the Food Chain. The Agency's media release did not mention the cat

(http://www.food.gov.uk/news-updates/news/2012/sep/toxoplasma#.UjExC-ASgtw), and the focus of the full report (www.food.gov.uk/multimedia/pdfs/committee/acmsfrtaxopasm.pdf) was on the importance of foodborne transmission, yet the report resulted in a global burst of hysterical, cat orientated, media reports with headlines such as ‘Cat infection being passed on to thousands’

(http://news.sky.com/story/980722/cat-infection-being-passed-on-to-thousands; Figure 1). This was further compounded by publication of a review on Toxoplasma oocyst contamination in the USA[4], where the risk posed to vulnerable populations from eating undercooked or raw meat was not accurately portrayed, even if oocyst shedding by cats is a source of meat contamination, although vertical transmission must also be considered [5].

Urban expansion and the recolonization of wildlife habitats in urban areas by wildlife species will expose them to Toxoplasma [6]. Sources of infection include environmental contamination by domestic cats but also food, particularly meat scraps left in gardens to encourage wildlife. In Perth, recent cases of neurological disease in bandicoots taken to wildlife carers has been shown to be due to Toxoplasma infection, most likely as a result of eating household scraps, but local media reports put the blame on cats (http://www.inmycommunity.com.au/news-and-views/local-news/Bandicoots- under-threat/7614966/), thus missing an opportunity for community education [7].

There is clearly a need to educate and limit such misleading media reports. It was therefore gratifying to see that a recent media splurge concerning a parasite-infected rock star proved very educational

(http://www.news.com.au/entertainment/music/frenzal-rhomb-frontman-jay-whalley-reveals-pig- tapeworm-egg-infected-his-brain/story-e6frfn09-1226587106839). The band member required surgery to remove a cysticercus ofTaenia solium from his brain forcing the band to cancel a tour of

Australia. This received considerable media exposure including detailed interviews with the affected band member. The fact that he is a vegetarian and his questioning of how he could have therefore become infected with a ‘pig tapeworm’ resulted in the valuable explanation by the quoted doctor that T. solium eggs are shed by human definitive hosts, and poor personal hygiene is a risk factor for Figure 1. Cats are not the enemy. Some media reports following release of a UK Government report

by the Food Standards Agency on Toxoplasma in the Food Chain, in 2012.

contracting neurocysticercosis, something that is not often stressed in information given to tourists

going to areas where T. solium is endemic.

Politics

Trichinellosis in humans is typically related to cultural food practices (e.g., [8]), including the

consumption of raw, undercooked, fermented, or cured meat, and there has been an increasing

reliance on testing to demonstrate [9]. With the control ofTrichinella, much of the emphasis has focused on domestic environments and the role of pigs and synanthropic hosts such as the rat in transmission. However, globally, wildlife are now seen as playing the major role in

maintaining cycles of transmission [10]. Anthropogenic activities may exacerbate opportunities for

spillover from wildlife to domestic foci, which may threaten biosecurity for pig producers [7]. Thus,

there are growing demands for producers, not only to demonstrate that their pigs are Trichinellafree

but that there is no risk of Trichinella infection spilling over to their pigs from wildlife. The situation

is exacerbated by the insensitivity of current diagnostic assays used in meat inspection and the

growing demand for free-range pork 11 and 12. It appears that political maneuvering associated with

market access may be serving to artificially inflate this as an issue. This appears to be the case in the

UK where there is a perceived need for data gathering and assessment of Trichinella in UK wildlife

even though it has rarely been detected in the past [13].

In practice, however, end product testing in countries where trichinellosis is endemic is best suited to

initially validate and then verify risk management along the supply chain. There remains the potential

for meat and wildlife testing to be required for trade and market access purposes disguised under the

cloak of food safety. From a global perspective, trade oriented policy should not trump

obligations in dealing with Trichinella in the food supply chain. In less well developed countries

where meat testing and post-processing controls cannot be reliably applied, an emphasis on improving

primary production practices rather than post-slaughter testing would in all likelihood result in a decrease in disease burden. Reduced incidence in humans will not be achieved by advocating for post- slaughter controls in resource poor countries.

Many developing countries are experiencing a boom in tourist numbers together with an increasing local demand for meat. Where Trichinella is endemic in the meat supply chain and local food customs include eating raw or undercooked meat, there is a high risk of becoming infected. This may have particular importance for tourists partaking in ‘food adventurism’. Sage advice for tourists to avoid undercooked, cured, and fermented meat dishes when visiting developing countries would undoubtedly improve the travel experience and prevent tourists returning home with unwanted internal companions. Travel related trichinellosis is well documented 14 and 15, and this advice would equally apply to wild game hunting tourists visiting areas of endemic trichinellosis. Take home message

Foodborne parasites need not be exploited for emotive or political purposes. The public are best served by accurate and measured information upon which to make informed decisions.

References

1. Hutchison, W.M. et al. (1969) Life cycle of Toxoplasma gondii. Br. Med. J. 4, 806 2. Tenter, A.M. et al. (2000) Toxoplasma gondii: from animals to humans. Int. J. Parasitol. 30, 1217– 1258 3. Food Standards Australia New Zealand (2013) Toxoplasma gondii. In Agents of . (2nd edn), pp. 103–114, Food Standards Australia New Zealand 4. Torrey, E.F. and Yolken, R.H. (2013) Toxoplasma oocysts as a public health problem. Trends Parasitol. 29, 380–384 5. Hide, G. et al. (2009) Evidence for high levels of vertical transmission in Toxoplasma gondii. Parasitology 136, 1877–1885 6. Lehrer, E.W. et al. (2010) Prevalence of antibodies to Toxoplasma gondii in woodchucks across an urban-rural gradient. J. Wildl. Dis. 46, 977–980 7. Thompson, R.C.A. (2013) Parasite zoonoses and wildlife: One health, spillover and human activity. Int. J. Parasitol. 43, 1079– 1088 8. Jenkins, E.J. et al. (2013) Tradition and transition: parasitic zoonoses of people and animals in Alaska, northern Canada, and Greenland. Adv. Parasitol. 82, 33–204 9. Dorny, P. et al. (2009) Emerging food-borne parasites. Vet. Parasitol. 163, 196–206 10. Pozio, E. et al. (2009) Molecular taxonomy, phylogeny and biogeography of nematodes in the Trichinella genus. Infect. Genet. Evol. 9, 606–616 11. Newell, D.G. et al. (2010) Food-borne diseases – the challenges of 20 years ago still persist while new ones continue to emerge. Int. J. Food Microbiol. 139, S3–S15 12. van der Giessen, J. et al. (2013) How safe is the meat inspection based on artificial digestion of pooled samples for Trichinella in pork? A scenario from wildlife to a human patient in a non-endemic region of Europe. Vet. Parasitol. 194, 110–112 13. Zimmer, I.A. et al. (2009) Report of Trichinella spiralis in a red fox (Vulpes vulpes) in . Vet. Parasitol. 159, 300–303 14. Anonymous (2006) Outbreak of trichinellosis in French hunters who ate Canadian black bear meat. Can. Commun. Dis. Rep. 32, 109–112 15. Suwansrinon, K. et al. (2007) Human trichinellosis from Laos. J. Travel Med. 14, 274–277