CASE NOTES


REVISITING THE TRANSMISSION OF TAENIA OVIS (SHEEP MEASLES) IN AUSTRALIA

David J Jenkins, School of Animal and Veterinary Sciences, Charles Sturt University, Wagga Wagga, NSW

Posted Flock & Herd June 2015

INTRODUCTION

Taenia ovis infection in sheep is of no apparent veterinary importance and in contrast to Echinococcus granulosus, dogs infected with adult T. ovis pose no risk to human health. The importance of T. ovis is financial losses for the Australian sheep meat industry through downgrading and condemnation of meat and hearts. T. ovis infection is also a potential impediment to international trade of sheep meat.

Adult T. ovis reside in the small intestine of domestic dogs and tapeworm eggs are passed onto pasture via the faeces from infected dogs. Eggs of T. ovis remain viable on pasture for at least 300 days where they are distributed further by agents such as wind and rain and coprophagous flies. Sheep are infected through accidentally ingesting T. ovis eggs whilst grazing.

Cysts in sheep muscles are small (approx. 4-6mm), blister-like lesions, each containing a single tapeworm head, occuring most commonly, in hearts and diaphragms. However, in heavy infections cysts can be found in muscle throughout the body of the sheep. It takes about two months of development for cysts to become infective to dogs, remaining infective for only 2-3 months. As time passes the immune system of the sheep kills the cysts which form into pus-filled abscesses, that later mineralize, transforming from gritty masses to hard calcified nodules. From a consumer's perspective, none of these cystic manifestations in meat are acceptable.

Although domestic dogs are considered the main definitive host of T. ovis, recently collected data strongly suggests this may not be the case1. The only other potential candidates are wildlife carnivores, namely foxes (Vulpes vulpes) and wild dogs (dingoes (Canis lupus dingo) and dingo/domestic dog hybrids). The possibility of wild canids being implicated in transmission is further strengthened by data generated in the National Sheep Health Monitoring Program2. The lowest number of lines of sheep infected with sheep measles was reported from Tasmania a jurisdiction where wild dogs (dingoes and dingo/dog hybrids) are absent and foxes, if present, are in numbers so small as to be an unimportant in transmission*.

The status of foxes as definitive hosts for T. ovis in Australia remains controversial because tapeworm identification, in all previous studies has been based on rostellar hook length measurements, a diagnostic method considered unreliable due to the considerable overlap in hook length between species.

As with rural domestic dogs, past studies on wild dogs concerning intestinal helminth infections commonly focused only on E. granulosus. However, none of the authors reporting the presence of cestodes ever mentioned T. ovis.

For more accurate/reliable identification of cestodes in canids a multiplex PCR assay has been developed to identify a variety of cestodes based on amplification of mitochondrial DNA sequences from eggs or worm tissue. The focus of our study, through the use of molecular methods, was a survey of taeniid cestodes in foxes and wild dogs for infection with T. ovis2. In addition, we examined faeces from rural domestic dogs for the presence of taeniid eggs, identified to species with this method3. Dietary analysis of foxes collected in one area where a T.ovis-infected fox was recovered was undertaken to obtain detailed data on the frequency foxes consume sheep/lambs2.

RESULTS AND DISCUSSION

A total of 499 foxes and 52 wild dogs were examined during the study. The number of foxes and wild dogs collected from the various collection sites ranged widely (foxes = 3 to 102; wild dogs = 1 to 20).

Few of the foxes collected were infected with Taenia species The prevalence of Taenia species recovered from wild dogs was higher (ACT 50%, NSW 48.0%).

Two hundred and forty five faecal samples from rural dogs were received from owners and tested. One dog from Tasmania was found infected with T. ovis, the only dog in the study identified with Taenia infection. Using sequence data, T. ovis was identified in two foxes but not in any wild dogs. One fox was from Jugiong, NSW and the other from Katanning, WA.

Data collected in this study confirms that a sylvatic transmission pathway for T. ovis, utilising foxes as definitive hosts is operating in Australia. The role of domestic dogs in the transmission of T. ovis in Australia has not been investigated for over 40 years, during which time palatable and nutritionally balanced dry dog foods have been developed and the highly efficient cestocidal drug, praziquantel, has become widely available. These developments have had a profound impact on the prevalence of canine intestinal worm infection. This is the likely reason eggs of Taenia species tapeworm were found only in one faecal sample in this study. The almost complete absence of Taenia of any species in dogs sampled in all jurisdictions is of interest, suggesting the role of domestic dogs in the transmission of T. ovis, is currently less important than in previous decades. These data are corroborated by other recently obtained data1 from a study of 1,425 rural domestic dogs from all states of eastern Australia. In this study, only 11 dogs were found infected with Taenia species, and of these, none was infected with T. ovis. In Tasmania, wild dogs are absent and foxes, if present, are in such small numbers as to be irrelevant regarding T. ovis transmission. Domestic dogs are the only widely available definitive host for T. ovis in Tasmania. It is of interest that Tasmania also has the lowest occurrence of T. ovis in lines of sheep slaughtered in Australia (National Sheep Health Monitoring Survey2). These data add weight to the importance of wild canids in the transmission of T. ovis on mainland Australia.

Our data regarding T. ovis infection in foxes revealed T. ovis infection in 2 animals, one from NSW and one from WA. The single worm present in each fox was mature with gravid segments; one infection was confirmed to be patent with eggs present in the host faeces. Faeces were not collected from the other fox. Foxes were collected from multiple sites in both NSW and WA but the sample sizes from the locations in each jurisdiction varied widely. In each jurisdiction, the T. ovis-infected fox was found in the location where the largest sample was collected, giving a prevalence level in each location of approximately one percent.

The presence of sheep or lamb's wool in fox intestines was identified macroscopically in 3.5% of NSW foxes and in 22.3% of WA foxes examined. One point two percent of intestines of the Jugiong foxes also contained sheep wool (seen macroscopically), however, based on detailed microscopic analysis of intestinal and stomach contents of 36 of the same foxes from Jugiong it was found many more foxes had been consuming sheep or lambs. Sheep remains were seen in 22.2% of the 36 intestinal contents examined microscopically, compared to 1.2% seen macroscopically. However, predated or scavenged lambs less than 2 months old are unlikely to be important in the transmission of T. ovis because the parasite will not have developed sufficiently to be infective to a definitive host. However, predating or scavenging of older lambs would be a likely scenario for exposing foxes to infection with T. ovis. Taenia ovis metacestodes in carcasses of older adult sheep are more likely to be non-infective having been killed by the immune system of the sheep.

In view of our findings, the most practical parasite control strategy, would be maintaining conventional control for domestic dogs, but in addition, to also vaccinate sheep. In 1989 data were published on a recombinant vaccine for sheep against T. ovis4. This highly efficient vaccine was registered for use in New Zealand but never in Australia. Since most of the financial loss due to sheep measles in New Zealand was borne by the processors and not the farmers, farmers were not motivated to buy the vaccine. If the vaccine can be produced in a form attractive to producers and there is wide uptake, there is little doubt, levels of sheep measles infection in Australian sheep would fall rapidly.

(*Foxes were illegally introduced into Tasmania about 12 years ago, there followed an intensive 1080 baiting program. If still present fox numbers in Tasmania are at such low density as to be irrelevant in the transmission of sheep measles)

ACKNOWLEDGEMENTS

The author thanks Meat and Livestock Australia for funding the study and is indebted to the Sheep Health Monitoring Survey, co-ordinated by Animal Health Australia on behalf of Wool Producers Australia and the Sheep Meat Council of Australia, for providing abattoir infection data, a crucial aspect to the success of this study.

REFERENCES

  1. Jenkins DJ, Lievaart JJ, Boufana B, Lett WS, Bradshaw H, Armua-Fernandez MT. Echinococcus granulosus and other intestinal helminths - prevalence and management in rural dogs of eastern Australia, the current situation. Aust Vet J 2014 Aug; 92(8):292-8
  2. The national sheep health monitoring project. AHA. 2011
  3. Jenkins DJ, Urwin NAR, Williams TM, Mitchel KL, Lievaart JJ, Armua-Fernandez M-T. 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. Int J Parasitol: Para and Wldlf 2014 (in press)
  4. Johnson KS, Harrison GBL, Lightowlers MW, O'Hoy KL, Cougle WG, Dempster RP, Lawrence SB, Vinton JG, Heath DD, Rickard MD. Vaccination against ovine cysticercosis using a defined recombinant antigen. Nature 1989;338:585-587

 


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