A critical reflection on current control of Toxocara canis in household dogs

Summary

Toxocara canis, the roundworm of the dog, is the most common parasitic worm in dogs in the Netherlands. In adult dogs this worm usually causes little or no symptoms. However, the worm can cause serious illness in puppies. Also in humans syndromes are known which are attributable to wandering larvae in the body. Toxocara is therefore considered a zoonotic parasite. Because of its ability to cause disease in young animals and in particular also because of its zoonotic potential, Toxocara is the main reason and target for the current propagated deworming advice in the Netherlands. Dogs up to the age of six months are frequently treated, varying from deworming them once every two weeks to deworming them on monthly basis. This is a higher frequency than is advised for older animals. There is no debate concerning the deworming advice for these young dogs. They are already infected before birth in the uterus and after birth by ingesting milk that contains larvae of Toxocara. All of these mentioned routes of infection may result in a so-called patent infection in a puppy, meaning that a puppy will shed large numbers of eggs with the faeces. In fresh stool, these eggs are not immediately infective. They first need to develop a few weeks in the environment before a larva appears in the eggs and the eggs become infective. After ingestion by a dog, these infective eggs can lead to new infections. The larvae that hatch from the eggs, need to migrate through the body and will enter the lungs. After being coughed up and swallowed, the larvae become adults in the intestines of a dog and can cause another patent infection. Somewhere between three and six months of age, dogs are believed to develop a so-called "age resistance”. This means, when a dog older than six months gets infected via the ingestion of infective eggs, this usually does not lead to adult worms in the gastrointestinal tract of the dog. The infection will remain limited to somewhere in the body where the larvae become dormant. Therefore, most dogs older than six months will not develop patent infections. Hence, it is questioned by owners and veterinarians whether all dogs older than six months need to be dewormed at identical intervals. 

When infective eggs are ingested by other animal species, including humans, this will not lead to adult worms in the intestines. But like in older dogs, the larvae that have hatched from the eggs will start their migration, only to get stuck somewhere in the body and become dormant. Depending on the place where such a larva eventually ends up, this may lead to symptoms. Because humans can be infected and this can sometimes lead to complications the general advice is to deworm each dog older than six months at least four times a year. Despite the fact that 'age resistance' is supposed to be effective in dogs older than six months, it is known that some dogs do develop a patent infection. Some of these cases can be explained, for example in nursing bitches. Here, the reactivated larvae start to migrate through the body. This way they can infect puppies in the uterus and after birth also through the mammary glands while the new born puppies are drinking. When the nursing bitch performs litter care and ingests the faeces of the puppies, she can ingest larvae that have passed and survived the gastro-intestinal tract of the puppies and develop a patent infection herself. An infection of a dog older than six months with larvae differs substantially from an infection with infective eggs. Ingested larvae do not tend to migrate through the body because they already done this in the bitch (infection by infective eggs and migration to the mammary glands) and they are ready to mature in the intestine without further migration. This way the ‘age resistance’ is circumvented. Therefore, a bitch that is performing litter care will most likely develop a patent infection herself. Another explanation for the development of a patent infection in dogs older than six months is when a dog gets infected by consuming a prey animal. In this way, the dog ingests larvae which are located in the muscle tissue or organs of an animal prey. These larvae also do not need to migrate through the dog’s body anymore, but can develop into adult worms directly in the intestine. Again, ‘age resistance’ will be circumvented leading to a patent infection. However, there are cases of dogs older than six months that develop a patent infection which cannot be explained by these two scenario’s.

Various studies have shown that the percentage of household dogs, older than six months, that actually develop a patent Toxocara infection is less than five to ten percent. That would mean that, when blind deworming is practiced, at least 90-95% of the dogs will be dewormed, at any given moment, without indication that there actually are adult worms present in the intestines. The current general advice to deworm all dogs regularly is therefore solely based on those few dogs that actually shed eggs. If we could predict what situations are associated with higher chances of developing patent infection in these dogs, treatment advice might become more focused accompanied by a less frequent use of veterinary drugs without any (diagnostic) evidence.

The questions
The aim of this thesis is to provide some clarification about the need to treat all dogs older than six months, four times a year without the use of diagnostics.
Key questions addressed in this thesis are:
- What is the contribution of dogs older than six months, compared to other animals (cats and foxes) to the contamination of the environment with Toxocara eggs?
- What is the attitude of participating owners towards regular deworming of their dog(s)? When more owners would practice blind deworming, how would this affect the relative contribution of dogs to the overall contamination of the environment with roundworm eggs?
- What factors appear to be associated with the occurrence of patent Toxocara infections in dogs older than six months?
- Are all dogs equally at risk for developing a patent infection or do some dogs more frequently develop a patent infection than others (wormy animals)? And if so, what factors are associated with such recurrent patent infections?

Patent roundworm infections can be determined by performing coproscopical examination of fecal samples. When roundworm eggs are present in the faeces it is usually considered as a patent roundworm infection. However, literature shows that it is not uncommon for dogs to eat things such as faeces from other animals or preys, which may contain parasite eggs. Clearly, such ingested eggs do not originate from an actual infection of the dog itself, but just pass the gastro-intestinal tract. When these passing eggs are morphologically very different this does not pose a problem. However, interpretation of results from coproscopical examination of faeces becomes much more problematic when a dog eats faeces from another dog or cat containing roundworm eggs. Those eggs are usually indistinguishable from those Toxocara eggs that result from an actual infection of the dog itself. Therefore, passing roundworm eggs will lead to a false-positive diagnosis of a Toxocara infection. Consequently, an additional question in need of an answer for a proper interpretation of the results was:
- How often are roundworm eggs in the faeces of a dog the result of eating faeces from a dog or cat with a patent infection, and to what extent did this influence the results in the present study?

To answer the questions mentioned above, 570 owners submitted a faecal sample of their dog(s) and answered a monthly questionnaire. This resulted in 938 dogs from which one up to 38 faecal samples were investigated and corresponding questionnaires were analyzed.

The results
To calculate the relative contribution to the environmental contamination with Toxocara eggs of dogs older than six months, data are required from other potential definitive hosts for this roundworm . Chapters 2, 3 and 4 focus on the contribution of dogs as well as foxes and cats. Chapter 2 deals with the first faecal sample and questionnaire that was submitted from household dogs (over six months old). For this study, data and coproscopical results were available from 916 dogs. The percentage of dogs shedding Toxocara eggs was 4.6%. Several factors appeared to be associated with the shedding of eggs. The probability that dogs older than twelve months were shedding was significantly lower than dogs in the age category of six to twelve months. The percentage of time that dogs were allowed to walk off-leash showed a clear association with the risk of shedding Toxocara eggs. Eating faeces from other animals and recent stay in a kennel or pet hotel were also associated with a higher probability of shedding eggs. No clear relationship could be detected between how frequent dogs were dewormed before they participated in the study and the probability of excreting Toxocara eggs. However, in the group of dogs, which were not recently being kenneled, had relatively little walking time off-leash, and that did not eat faeces from other animals a deworming frequency of four times a year appeared to be slightly associated with the absence of patent infections. 

From these results it can be concluded, that not every dog shares the same risk of shedding Toxocara eggs. This may partly explain the lack of association between the applied deworming frequency and the probability of having a patent infection. 

How the participating owners dealt with and felt about deworming their dog(s) and cleaning up the faeces of their dog(s) is also addressed in chapter 2. Most of the owners mentioned that the dog’s health is the main reason for deworming their dog. Only 16% of the participating owners followed the advice given by ESCCAP (European Scientific Counsel Companion Animal Parasites) to deworm four times a year on average. The disseminated deworming advice, including the main reason for this deworming advice, is not reflected in the answers of most participants. Whether participating owners did not agree with it or were not aware of it was not clear. Effective Toxocara control cannot, under the given circumstances, be expected from current recommendations, which are not mandatory for dog owners. Moreover, there is no defined minimum level of knowledge required for retail points that sell anthelmintics over the counter without any veterinary involvement. 
Among the other definitive host species are foxes and cats. Foxes can have a patent infection with the same species of roundworm as dogs. Cats, however, have their own species of roundworms, which is also zoonotic. So, both foxes and cats contribute to the overall contamination of the environment with Toxocara eggs in the Netherlands. Chapter 3 focuses on the fox population. Foxes that were killed in the east of the country, were examined for parasites. Where the prevalence of egg shedding in dogs was almost 5%, in foxes no less than 61% were found to shed these roundworm eggs. So, although the number of dogs in the Netherlands exceeds the number of foxes by far, foxes can because of the high prevalence still contribute significantly to the contamination of the environment with Toxocara eggs. In household cats that were studied in chapter 4, about 7% shed Toxocara eggs. It should be borne in mind that the studied population of cats were all cats that used the litter box. This could have biased the outcomes. Because of logistic reasons concerning the difficulty of collecting samples and obtaining information, stray cats were not included in the study. Therefore, a prevalence of 7% probably will lead to an underestimation of the actual contribution of cats to the environmental contamination.

All the percentages of Toxocara egg shedding animals as mentioned above are based on the presence of eggs after microscopic examination of faecal samples. In chapter 5 the question is raised to what extent eating faeces by dogs could influence the outcome of this diagnostic method. Coprophagy, as eating faeces is called, is common in dogs, uncommon in cats and for foxes information is lacking. When a faecal sample tested positive for parasite eggs, this could be explained either by a true patent infection or by eggs that were ingested by a dog and apparently passed the gastro-intestinal tract unaltered. Almost half of the participating owners recognized coprophagic behavior in their own dog(s). Interference with the outcomes of our diagnostic procedure was therefore to be expected. When a faecal sample tested positive for parasite eggs, the owner was asked for a new sample that was taken after a period of three days in which the owner prevented the dog from eating things from the ground. If this confirmation sample also tested positive for the same type of parasite eggs, an infection was considered "confirmed". However, if the eggs were not present in the confirmation sample, or this sample contained different types of eggs, it was considered "negative". Of the Toxocara positive stool samples, 49% of the confirmation samples tested negative, meaning that no Toxocara eggs could be diagnosed. Therefore, in the analyses of further results of the studies coprophagy was always included as an important factor in dogs.

The relative contribution of dogs to the environmental contamination with Toxocara eggs in the Netherlands, compared to that of domestic cats, stray cats and foxes, is estimated in chapter 6. Data from previous studies and from literature were used as input for a new model to refine a previously described model. Our new model indicated that the dog indeed is contributing most (39%) to the environmental contamination with Toxocara eggs in the Netherlands. However, this position was lost when the household cats and stray cats were considered as one group. In this case, the cat appears to be responsible for 46% of the eggs in the environment. Depending on the degree of urbanization of an area it can differ to which extent an animal species is responsible for the major part of contamination of the environment. This model could also be used to simulate the effect of different percentages of owners deworming their dogs at different frequencies on the relative contribution of household dogs. The same thing was possible for the compliance of owners to cleaning up faeces after their dog. This showed that if 90% of the dog owners that do not deworm their dogs four times a year would actually do so, the contribution of the household dogs would drop from 39% to only 28%. For a more substantial decrease in the relative contribution the majority of dog owners need to deworm their dogs more often than four times per year. This does not seem to be realistic at present times. Cleaning up the faeces of dogs by their owners has a similar effect as deworming monthly. Under the current circumstances, with anthelmintics for dogs being freely available, cleaning up faeces probably fits more easily into a Toxocara control policy because it is more easy to check than deworming dogs on a voluntary basis.
Do all dogs, older than six months of age, contribute equally to the environmental contamination or do some dogs appear to have patent infections more frequently than others? This question is addressed in chapter 7. All available faecal samples (n=12,968) and answers to the questionnaires were analyzed for this purpose. The majority of the dogs (67.9%) did not show a patent infection during the period they participated in this study. From the other dogs a total of 585 faecal samples tested positive for Toxocara eggs. Of these, 421 samples came from dogs with more than one patent infection during the study. This group of frequently shedding dogs (14.6% of the group of participating dogs) was responsible for 72% of the Toxocara positive samples. By identifying these dogs, that show recurrent patent Toxocara infections and by treating these dogs more frequently, a greater efficacy can be expected compared to treating all animals blindly four times a year. 
It seems likely that the recurrent patent infections are somehow associated with risk factors impacting the functionality of the immune response of a dog. When the immune system is somehow compromised, larvae already present in a dog’s body may become reactivated. Indeed, recurrent infections appeared to be associated with, for example, the administration of corticosteroids, changes in the lifestyle/function of a dog, and a proxy of owners visiting a veterinary practice on a regular basis. The more sporadically occurring patent infections, by contrast, seem to be associated among other things to eating stuff from the environment (including faeces), percentage of time walking off-leash and dietary influences. Finally, a remarkable seasonal pattern in the incidence of patent infections was observed during the study, with an annual peak in wintertime. Although this could not be fully explained, it indicates that the effect of a blind deworming strategy may vary by season.

Conclusions and prospects for the future
Dogs are largely responsible for the environmental contamination with Toxocara eggs. Owners should be aware that this can compromise public health. The majority of the participating owners, however, did not recognize public health as the main reason for deworming their dog. Only a limited number of owners dewormed their dog(s) according to the recommended four times a year. And only a small group of the participating owners acknowledged to clean up faeces from their dogs on a regular basis. An important conclusion is that both cats and foxes are responsible for a considerable part of the contribution to the overall contamination of the environment with Toxocara eggs. Strategies to control disease due to Toxocara infections in humans must therefore also aim for controlling this roundworm in (stray) cats and foxes.
Not all dogs appear to be equally at risk for developing patent Toxocara infections. For the majority of the participating dogs it did not appear to be necessary to get dewormed four times a year. Regular faecal examination could help to identify dogs showing recurrent patent infections. The frequency, however, in which coproscopical examination should be performed is likely to be high and voluntary cooperation of owners to do so is not expected because of higher costs. There is a need for studies how to improve the involvement of owners in programs based on performing regular coproscopical examination, as well as in better cleaning up faeces from their own dog(s). Targeted deworming is already advocated, for example for dogs younger than six months or in lactating bitches. ESCCAP also created a crude decision tree for a more customized deworming. The risk factors listed in Chapters 2 and 7 can be used to further refine such decision trees, both in terms of blind anthelmintic treatment as in creating customized preventive health care including coproscopical monitoring, which should lead to a substantial reduction in unnecessary use of medicine.

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