Worming – where we are and where we should go

The benefits of human-animal interaction are numerous and much circumstantial evidence supports the healing power of pet ownership and its positive influence on ageing, cardiovascular diseases, behavioural, physiological and psychological well-being (Havener et al, 2001; Wu et al, 2002; Bernabei et al, 2013; Creagan et al, 2015).

A study reported significant positive effects of assisted animal therapy (AAT) on the therapeutic progress and recovery process in children and adolescents admitted to a psychiatric hospital for acute mental disorders (Stefanini et al, 2015). In the EU, nearly 27% of 70 million households own at least one dog, and in the UK there are about eight million dogs (The European Pet Food Industry Federation, 2012).

Pet ownership is also rising in the US, with approximately 75% of US households having at least one pet (Creagan et al, 2015) and each household spending an average US$500 (£320) per year on pets, accounting for nearly 1% of the total annual spending for an average income household.

According to the Global Pet Expo an estimated US$58.5b (£37.5b) was spent on pets in 2014, despite the economic recession (Global Pet Expo, 2014), suggesting the high value people place on their pets. People not only value live pets, but also robotic animals, such as Sony’s Aibo dog, which became a popular companion in Japan, and Paro, a robotic baby seal being used therapeutically in the US.

Burden of parasitic diseases

Even though pet ownership can enhance people’s quality of life, pets can be a source of zoonoses, and this is receiving increasing attention from health care professionals, politicians and society (Reaser et al, 2008). Dogs and cats can harbour many internal (endoparasitic helminths: roundworms, hookworms, whipworms and tapeworms) and external (ectoparasitic arthropods: ticks and fleas) parasites. It is normal for a cat or a dog to be infected by one or more species of endoparasites or endo and ectoparasites – a state called hyper-(poly-)parasitism. Most of these parasites can cause morbidity and even death.

For example, the mollusc-borne respiratory nematodes (the canine Angiostrongylus vasorum species – Figure 1 – and the feline Aelurostrongylus abstrusus species), or the intestinal species, such as the roundworm Toxocara canis (Figure 2), the hookworm Ancylostoma caninum, and the whipworm Trichuris vulpis, are important to animal health because of their wide geographical distribution, high pathogenicity and significant clinical impact.

A vasorum is a parasite of both the right ventricle and the pulmonary artery in domestic and wild canids. Infected canids present with various clinical signs, including weight loss, persistent cough, dyspnoea, pneumonia, arrhythmias, thrombosis, disseminated intravascular coagulation and, in severe cases, death.

A caninum causes anaemia (blood loss) and intestinal lesions, and can accidentally infect humans, causing cutaneous larva migrans. Also, humans can be infected by T canis via the accidental ingestion of infective embryonated/larvated Toxocara eggs present in contaminated soil, unwashed hands or raw vegetables. Within humans Toxocara larvae emerge from the eggs and migrate throughout the body, causing damage to tissues they encounter.

Among ectoparasites, fleas (Figure 3) and ticks (Figure 4) are the most commonly encountered external parasites on domestic dogs and cats (Blagburn and Dryden, 2009). Fleas cause discomfort and nuisance to pets and their owners through biting. Also, they can cause other health problems, such as flea allergy dermatitis, act as vectors for a range of human and animal pathogens, such as Bartonella henselae and Rickettsia species, and transmit the tapeworm Dipylidium, and the filarial nematode Acanthocheilonema (formerly Dipetalonema). Cat flea (Ctenocephalides felis) is the most abundant flea species infesting dogs and cats (Rust and Dryden, 1997).

Ticks can transmit a variety of diseases to dogs, such as babesiosis, ehrlichiosis, haemobartonellosis, hepatozoonosis and Lyme disease. These diseases can cause anaemia, lameness, weakness, lethargy, organ failure, paralysis and death.

Multimodal management of parasitic infections

Treatment and control of parasites in companion animals is more than just an ethical or moral issue. Anthelmintic drugs play the largest role in the management of parasitic infections. However, therapeutic interventions (pharmacological therapy) using dewormers, along with other non-pharmacological therapies, including evidence-based treatment, tailored treatment, accurate and timely diagnosis, and engaging pet owners and professionals, should be instituted to provide optimal parasite management outcomes with the least detrimental risks.

Pharmacological therapy

Many chemotherapeutic products, with various mechanisms of action, are available to treat various parasite infections. Some are endectocides, made either by having one active ingredient with a broad spectrum of activity or by combining active ingredients.

Veterinarians are often faced with the need to treat and prevent both external (fleas) and internal (intestinal and cardiorespiratory worms) parasites. Endectocide products can be used to control both worms and ectoparasites. The precise spectrum of activity varies according to the active ingredients. Matching the spectrum of activity to the infection present or the risk for individual animals is a key part of managing a parasite infection. Other factors include drug activity against juvenile and adult stages of parasite and convenience of administration. Drugs used for treatment or prevention of companion animal parasites, including active ingredients and the spectrum of activity of products in the NOAH Compendium, are available on the European Scientific Counsel Companion Animal Parasites (ESCCAP) website (www.esccap.org).

Non-pharmacological approaches

Why tailored deworming is important to management

The appropriate frequency of deworming is often debated, and this is because no one answer will fit all situations. Where it is crucial to minimise risk of patent infection (such as when control of zoonotic infection is essential) then re-treatment at a frequency close to the prepatent period (often monthly for convenience) will help to achieve this.

However, no treatment can have absolute efficacy. Also, some parasites, such as Crenosoma vulpis, the fox lungworm, have a prepatent period of 18 to 21 days. For this parasite, monthly use of anthelmintic might not be effective in preventing the development of clinical disease in dogs. In other situations, this frequency of treatment would be overkill, particularly where other management and decontamination measures are already in place to reduce the risk of infection.

No scientific evidence exists of the frequency of treatment in these lower risk situations.

A balance is needed between minimising zoonotic and animal health risk, while managing environmental contamination and minimising the risk of selection for drug resistance. Apart from evidence of resistance to pyrantel in canine hookworms, drug resistance has not been reported for worms affecting pets, perhaps because of a decreased intensity of treatment compared to farm animals.

In contrast, evidence for resistance of cat fleas against some ectoparasiticides has been reported. Therefore, the cost of treatment and the potential for resistance selection must be balanced against the health risks to achieve a management regimen that works well for an individual animal or group of animals.

Risk assessment andpet owner compliance

Before prescribing nematicidal and/or cestocidal treatment, proper risk assessment must be made of the worm species present or expected to be present in the animal. All pet health care providers should stay up to date with information about the various aspects of the parasites they expect to encounter in small animal practices, so they can provide appropriate advice to their clients.

Working with pet owners to gain knowledge of the animal’s lifestyle and its management is also essential to predict the risk of parasitic infection and should be taken into consideration when designing a deworming regimen to mitigate potential risks.

For example, the life cycle of many worm species starts in faeces, and thus, if faeces are disposed of hygienically the risk of infective stages in the environment will be reduced.

Also, some animals can be at a higher risk of certain infections at certain ages. For instance, the clinical impact of Toxocara is likely to be highest for puppies and kittens, with high parasite load infections, compared to older animals. Puppies also are at a higher risk of infection with A vasorum, probably due to their exploratory behaviour bringing them in contact with slugs (the intermediate host that harbour the parasite’s infective stage). Animals given uncooked meat or offal are at increased risk of acquiring tapeworm infection.

Travelling pets are at a higher risk for exotic ticks (Figure 5) and tick-borne diseases, especially after the removal of the obligatory tick treatment in the Pet Travel Scheme in January 2012. Also, travelling pets are at a risk of acquiring the fox tapeworm, Echinococcus multilocularis, the causative agent of alveolar echinococcosis – one of the most severe parasitic zoonoses in the northern hemisphere (Eckert et al, 2000). The parasite is endemic in 18 countries of the EU (Casulli et al, 2010; Combes et al, 2012). However, E multilocularis has not been detected in the UK.

Due to its significant socioeconomic and public health impact, efficient methods must be used to prevent introduction of this serious parasite into the UK. The present EU regulation allows the UK to maintain national rules for the entry of dogs and cats over a transitional period to protect against imported E multilocularis infection. Maintaining E multilocularis-free status is necessary for keeping the present import requirement.

Another important parasite is A vasorum, which has a growing importance due to its clinical impact and geographical emergence and is spreading in both endemic regions and areas previously free of infection in the UK and in Europe.

This nematode represents a potential threat to native dogs and also via the importation of infected hosts. Hence, veterinarians might need to consider the use of chemopreventive approaches for canine angiostrongylosis, especially in areas known to be endemic. Considering the possibility of intermediate and paratenic hosts of A vasorum being present throughout the year, the opportunity of all-year-round controls may be taken into account.

Role of diagnosis in parasite management

Accurate and timely diagnosis often leads to better treatment outcomes. However, issues surrounding laboratory detection and identification of disease-causing parasites continue to trouble clinical parasitologists and small animal clinicians. Most parasitic infections are diagnosed at a far advanced stage when the life cycle has already been completed and the damage has happened.

Regardless of the diagnostic methodology, it is important to reach a specific and timely diagnosis, based on a combination of historical information, physical examination, laboratory tests and, in some infections, imaging.

For most parasitic infections laboratory diagnosis depends on the detection of eggs (for example, Toxocara) or larvae (such as A vasorum) in the faeces using McMaster technique or Baermann’s technique, respectively. The likelihood of diagnosing some parasites where daily excretion of eggs or larvae may be irregular may be enhanced by sampling over two or three days where needed. Occasionally, where there is a prepatent infection or low-level intermittent shedding faecal examination may not be accurate. Thus, a negative result does not rule out the possibility of a worm infection being present. Where “true” heartworm caused by adult Dirofilaria immitis is suspected, normally associated with a history of travel to endemic areas, then a blood sample for the juvenile stage (microfilaria), antigen or antibody detection is performed. Where a specific diagnosis is made, therapy must be implemented.

The situation becomes more challenging when animals develop a symptomatic infection. Then the question is what is an appropriate management strategy to prevent clinical signs, environmental contamination with eggs or larvae and zoonotic transmission. Risk assessment can be based on faecal examination, which will identify patent helminth infections present in sufficient numbers at the time of treatment, and/or an assessment of the likelihood of infection based on knowledge of the animal’s lifestyle, the parasites it is likely to be exposed to and the risk those parasites pose, either to the same animal or other animals.

Another consideration is the risk of zoonotic infection and its prevention. For instance, more attention should be given to the prevention of worm infections (for example, Toxocara) in a puppy living in a household with small children, elderly or immune-compromised individuals.

Theoretical assessment of the likely exposure is more useful than diagnostics for some parasites, such as tapeworms (cestodes) where diagnostic methods remain insufficiently sensitive, and in situations where prevention of patent infection is needed. Nevertheless, any approach should be subjected to cost-benefit analysis and aligned with public health priorities.

Making the most of digital technologies

Mobile and other digital communication technologies have transformed the social fabric of life.

According to the Office for National Statistics about 38 million individuals in the UK (about 76% of the population) accessed the internet every day during 2014 (www.ons.gov.uk/ons/dcp171778_373584.pdf). That is two million more than in 2013 and 21 million more than in 2006.

Nearly seven out of every 10 adults (68%) use a mobile phone, portable computer and/or hand-held device to access the internet on the go. Worldwide, 12.5 billion mobile devices were sold in 2010, with 25 billion phones expected to be on the market this year (2015), offering more than three phones for every individual and a projected seven phones per person by the year 2020 (Topol et al, 2015).

This trend indicates the huge potential of smart devices and apps as a source of health promotion or protection interventions.

ESCCAP (www.esccap.org) and ESCCAP UK and Ireland are good examples of how online platforms can be exploited to raise awareness among pet owners and animal health professionals, with the focus on effective parasite control and advice on travelling pets (www.esccap.org/travelling-pets-advice/).

ESCCAP is a leading independent pet health and parasites information website in Europe. In the US, CAPC (www.capcvet.org) provides up-to-date educational resources to pet owners and veterinary professionals about the diagnosis, treatment and control of parasitic infections.

Involvement of knowledgeable parasitology specialists and veterinarians in developing and updating online resources is important because it ensures information provided to clients is correct.

Summary and future directions

While not all parasites have a high public health profile, they all carry potential to cause disease and present challenges to animal health. Frequent contacts with pets create opportunities for the exchange of zoonotic diseases between humans and pets. A multimodal approach is the way forward if we are to advance our efforts for efficient control of parasites.
Enhanced veterinary care is needed to minimise the risk of zoonotic diseases. The potential of communication technologies to transform the face of the animal health care by serving as a means for delivering specific health interventions or raising the awareness of pet owners is huge.

Veterinarians, veterinary nurses and SQPs cannot alone control parasitic diseases. Compliance and cooperation of pet owners is essential. Controversy exists regarding the current and future practice of prescribing anthelmintics.

The optimal approach for deworming has not been determined, and appropriate treatment decisions in cases where there are certain risks are not clear.

Future studies using a personalised risk assessment approach to guide treatment protocols may provide the answers for clinicians and veterinary parasitologists keen to determine the best approach to treating pets with parasite infections.

It seems inevitable there will be a paradigm shift from uni-modal parasite control strategy to more multimodal integrated approaches. However, while efforts are under way to improve deworming strategies, it is unrealistic to expect change to happen in one day, especially when it concerns a balance between evidence versus opinion or experience and innovation versus tradition.

Acknowledgement

Because of space limitation, I was unable to comprehensively cite many worthy contributions to the field.