23 Nov 2015

Controversies and practicalities of human toxocarosis control

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Ian Wright

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Controversies and practicalities of human toxocarosis control

Figure 3. Providing public waste bins labelled as suitable for dog waste promotes responsible ownership.

ABSTRACT

Toxocara species are a group of intestinal nematodes infecting dogs (T canis) and cats (T cati). They are the cause of human toxocarosis, a significant zoonosis that can lead to visceral, ocular and neurological larval migrans as well as the condition known as covert toxocarosis.

The ocular form of the disease has a relatively high public profile and toxocarosis remains an enigmatic, controversial and emotive disease that continues to debilitate members of the UK public year on year.

Some aspects of toxocarosis control are very clear, while others are mired in controversy. It is the task of the veterinary professional to weigh the evidence surrounding Toxocara species transmission and disease risk, and then give clear, concise recommendations to keep pets healthy and the pet-owning public safe.

This article discusses what is known about toxocarosis and its more controversial aspects. It also considers what recommendations can be made from current evidence.

Few topics in the field of veterinary public health are as emotive as human toxocarosis. Pictures of blinded children in the newspapers lead to accusing eyes upon dogs in parks and communal areas and the fear contact with dogs may lead to debilitating illness.

Conversely, many dog owners and pro-dog societies consider toxocarosis as the stick anti-dog lobbyists use to beat them with and to reduce their freedom to roam where they choose.

It is the task of the veterinary professional to unpick these arguments and give clear, concise recommendations to keep pets healthy and the pet-owning public safe.

Life cycle and transmission

Figure 1. Toxocara species adults.
Figure 1. Toxocara species adults.

The life cycle for T canis is complex. Adult worms (Figure 1) live in the small intestine and shed eggs into the environment via the faeces of the host. When first shed, the eggs are unembryonated (Figure 2) and are not infective.

Progression to the embryonated L3 stage is required for infection, so fresh faeces do not present a zoonotic risk. Embryonation takes place in two to seven weeks under optimum conditions.

Although dogs may be infected by ingesting embryonated eggs, the most important route of canine infection is transplacental. As a result, prevalence of infection in pups born to untreated dams can reach close to 100%. Dogs may also become infected by transmammary infection or consuming paratenic hosts such as rodents. The latter is more important in T cati transmission where the feline host frequently hunts and transplacental transmission does not occur. Transmammary infection ensures high prevalence in puppies and kittens that have not had anthelmintic treatment.

As cats and dogs age, they develop a degree of immunity to the parasite, which reduces the chances of worms producing eggs and, as a result, the prevalence of patent infection in adult pets is frequently less than 20%. This can vary substantially, with prevalence of T canis in western Europe varying between 3.5% and 34% and T cati between 8% and 76% (Overgaauw and Van Knapen, 2013). This prevalence is not static, with shedding of ova being intermittent so adult pets act as a reservoir of infection.

Human toxocarosis

Toxocara species infection can lead to a number of disease syndromes in people.

Visceral larval migrans

Migrating larvae can lodge in the lungs or liver, leading to respiratory signs and/or hepatomegaly associated with a high eosinophilia. Other organs may be affected, such as the heart leading to myocarditis. Fever, weight loss, abdominal pain, anorexia and lethargy are all common in diagnosed patients, with the potential for respiratory and cardiac signs.

Ocular larval migrans

Perhaps the best known consequence of infection. Migrating larvae in the eye set up granulomatous reactions. Associated endophthalmitis, choroidoretinitis, uveitis and retinal detachment can then occur, leading to progressive visual loss, strabismus and blepharospasm.

Neurological larval migrans

Migrating larvae in the nervous system can lead to infarction and menigioencephalitis. Behavioural changes, changes in sleep patterns and seizures have all been linked to Toxocara species infection.

Covert toxocarosis

Seropositivity can be associated with a mild or moderate eosinophilia and associated mild multiple clinical signs that may or may not be due to migrating larvae. Abdominal pain, headache, cough, lethargy and a rash, with or without pruritus, have all been reported in eosinophilic, seropositive patients.

Although it has been proposed people can be infected by eating the undercooked meat of paratenic hosts such as wild game (Sturchler et al, 1990), the most common route of human infection is by ingestion of embryonated eggs. This can occur through the accidental or deliberate consumption of soil (geophagia), the transfer of the sticky eggs on to other objects that may be placed in the mouth (pica) or through contact with contaminated dog hair (direct dog contact).

What everyone can agree on

Figure 2. Unembryonated T canis ova.
Figure 2. Unembryonated T canis ova.

Approximately two cases of confirmed toxocarosis per million people are reported in the UK each year. However, it is likely some cases go undiagnosed each year due to the wide variety of clinical presentations in people. Approximately 2% to 3% of the UK population have seroconverted to the parasite, with unknown consequences, but increased risk factors for asthma, dermatitis and epilepsy are being established.

The most at-risk group in people are children, commonly between one and four years old, but with adults also being affected. Each individual case that leads to blindness or chronic debilitation is a potentially preventable tragic event. Everyone can therefore agree taking steps to prevent this disease is important.

Exposure to infection occurs predominantly through eggs in the environment so limiting exposure to these eggs will reduce transmission. The following four steps will reduce environmental contamination and/or human exposure without any significant adverse consequences and therefore should be a minimum recommendation to clients.

Deworming puppies and kittens

Puppies and kittens provide the largest source of potential infection and, until treated, should all be assumed infected.

Treatment of puppies should start at two weeks old, repeated at two-weekly intervals until two weeks postweaning and then monthly until six months old. This is to eliminate T canis egg shedding from transplacental and transmammary infection and significant populations establishing in the intestine.

Kittens should be treated in the same way, but the first treatment can be given at three weeks old as there is no transplacental transmission. Toxocara species are susceptible to a number of anthelmintics including macrocyclic lactones, tetrahydropyrimidines, benzimidazoles and octadepsipeptides.

Treating adult cats and dogs

Deworming every three months has become the linchpin of parasite control recommendations, but not all veterinary professionals realise this is primarily to reduce Toxocara species ova shedding. Use of an effective anthelmintic every three months has been demonstrated to significantly reduce Toxocara species ova shedding (Wright and Wolfe, 2007).

Although some vets recommend less frequent deworming, there is no evidence less frequent regimes will have any effect on egg output. Therefore, this frequency should be a minimum recommendation in dogs and cats.

Environmental contamination with dog faeces

Figure 3. Providing public waste bins labelled as suitable for dog waste promotes responsible ownership.
Figure 3. Providing public waste bins labelled as suitable for dog waste promotes responsible ownership.

UK county councils are taking the public health threat of dog faeces in public places increasingly seriously. As a result, many councils have instituted measures such as disposal bins (Figure 3), imposing fines for dog fouling and launching press and website-based public education campaigns.

Hygiene around pets

Washing hands after playing on soil and sandpits, petting or handling cats and dogs, and before eating is essential to help block transmission of a number of zoonotic pathogens, including Toxocara species.

It is hard to argue the measures outlined are not beneficial and, if they were all instituted universally, would reduce the transmission of human toxocarosis. A number of issues surrounding the epidemiology and control of the parasite are more controversial and require further examination.

Controversies

Dog access

Banning dogs from children’s playgrounds and sports fields has long been a controversial issue and is often debated in the media (Daily Mail, 2013; BBC, 2010).

These debates quickly become highly emotive, with loud voices on either side of the dog lobby. It is difficult to ban dogs from public park spaces as many dog owners (including the author) enjoy exercising dogs there. However diligent the pet owner, inevitably some residue is left behind when dog faeces are picked up and, even in dewormed dogs, there is the possibility of some egg shedding occurring and being present in this residue.

Although as a single event this is unlikely to be significant, over time levels may build up in playgrounds and sports fields, making it difficult to justify not banning dogs from these areas. Also, some dog owners are not responsible and, however small the minority, they have made many sports fields unplayable (West Wales Chronicle, 2015).

Role of cats

It was originally thought T canis alone was the source of human infection by this route, but there is now strong evidence to suggest T cati is significantly involved as well (Fisher, 2003). Although some still consider the role of T cati in human toxocarosis to be controversial, the large number of common antigenic fractions between T canis and T cati and the similarity in mode of transmission would suggest the two parasites have comparable zoonotic risk (Cardillo et al, 2009).

The potential role of T cati in human toxocarosis therefore cannot be ignored or underestimated. Clients should be advised to cover sandpits when not in use, to prevent cats defecating in them and burying their faeces. Cats should be treated for roundworm in a similar fashion to dogs to reduce environmental contamination.

Role of foxes

Although prevalence of T canis in foxes is high and their role in environmental contamination has not been quantified, it is thought to be less than 10% that of dogs. This is due to far fewer foxes than dogs in most populated areas. Therefore, although keeping foxes out of children’s playgrounds and parks with fencing is sensible if possible, it is unlikely fox population control would have any significant impact on human toxocarosis incidence.

Monthly worming

Use of a monthly anthelmintic will reduce egg output by more than 90% and whether this is necessary will depend on the pet’s lifestyle. Those pets hunting, in contact with young children, immune-suppressed individuals or individuals with poor hygiene should be dewormed monthly.

The counter argument is monthly deworming may encourage resistance to anthelmintics. However, the risk of resistance is only reduced if parasites not exposed to anthelmintic are released into the environment to create refugia. This is not achieved by not treating pets negative for parasites. Therefore, although there is an argument for deworming at a frequency that allows some shedding of ova and larvae into the environment, this is hard to justify for those at risk of significant zoonoses such as toxocarosis.

Direct dog contact

A number of studies have found embryonated Toxocara species eggs in the coat of dogs (Wolfe and Wright, 2003; Roddie et al, 2008) suggesting transmission may occur through direct contact with the coat of dogs.

It has been demonstrated subsequently T canis eggs can embryonate in dog fur, but at a lower rate than in soil (Keegan and Holland, 2012). The potential for embryonation and the presence of embryonated eggs in dog fur means prolonged direct contact and poor hygiene around dogs represents an unquantified transmission risk.

These findings have been “sensationalised” by the press (New Scientist, 2003) and condemned as “anti-dog” by pro-dog groups. Although it is unlikely embryonated Toxocara species eggs in fur do not pose as great a risk as those in soil, good hand hygiene will remove any risk this route poses and should be strongly encouraged, especially in young children. This will also help to prevent the transmission of faecal-oral parasites such as Campylobacter species, Giardia species and Toxoplasma gondii.

Dog ownership as a risk factor

Although some studies indicate dog ownership is a risk factor for toxocarosis, others have found no link. It can be assumed if dogs contaminate the environment around them intermittently their whole lives, then owning a dog may increase risk, and this risk would increase with the number of dogs being owned.

However, if precautions such as regular removal of dog faeces from gardens, regular deworming and good hand hygiene are employed, then this increased risk is likely to be minimal.

Research and conclusions

Despite extensive research, much is still unknown about toxocarosis, including how large a role cats and direct contact with dogs play in transmission as well as the link between seroprevalence and disease syndromes in people.

Research must concentrate on the relationship between seroprevalence and zoonotic disease, and the differentiation between toxocarosis caused by T canis and T cati. With this knowledge, the risks posed by exposure to these parasites could be better assessed.

In the meantime, we do know the UK public is being put at risk by inadequate toxocarosis control measures. Ironically, although toxocarosis is a recognised zoonosis among the public, not all pet owners are collecting their pets’ faeces or deworming their pets adequately to reduce transmission risk.

In this respect veterinary professionals have a vital role to educate the public and help reduce the incidence of disease.