Everyday parasites in companion animals

27 September 2013
14 mins read
Volume 4 · Issue 7

Abstract

Owning pets in the UK and Ireland is very beneficial for some, but does bring risks and responsibilities. Over recent years, parasites endemic to the UK have been overshadowed by exotic parasites. This article turns the reader's attention back to these ‘everyday parasites’, exploring the effects of infestation/infection, lifecycles, identification and control of fleas, ticks, mites, tapeworms and Toxocara spp. The diagnostic and control challenges faced by pet owners and veterinarians are explored from the perspective of the One Health initiative.

As Robertson et al (2000) have reviewed, pets offer a significant range of benefits to mankind. In comparison to non-pet owners, pet owners visit their doctor less often, use smaller number of medications and have lower blood pressure and cholesterol levels. Pets also add to the physical, social and emotional development of children and the happiness of their owners, in particular elderly people. However, pet owning also brings risks such as those associated with pet parasites. These parasitic risks require appropriate management to prevent disease in pets and, since many of these parasites are potential human zoonoses, also humans. Pet parasite control therefore links in to the One Health concept, whereby an interdisciplinary approach is encouraged to improve communication and health care across human health, animal health and environmental health (One Health Initiative, 2013). The One Heath initiative is expected to vastly advance health care.

Over the recent past, particularly since the changes to the PETS travel scheme in January 2012, when mandatory tick treatment was removed, the primary focus has often been on exotic or imported infections. In some way this may have led to those everyday parasites, already endemic in the UK, slipping below the radar. This is understandable as they may not have the attractive headline grabbing quality of the new or imported infections. To redress this, this article will focus on the everyday parasites, including how readily they are identified, what their significance is and the suitable methods for their management and control.

Ectoparasites

Fleas

Ctenocephalides felis, also known as the cat flea, are wingless, laterally flattened, blood sucking parasites. C.felis is the most commonly reported flea species on cats in the world. In many parts of the UK, but less so in Ireland, C. felis has displaced the dog flea, Ctenocephalides canis, as it is less fastidious in its requirements. Thus for dogs in the UK the most common flea is now the cat flea (C. felis), then followed by the dog flea (C. canis). In a study carried out in 2005 by Bond et al (2007), it was reported that 93.15% of fleas found on dogs were C. felis. Occasionally mixed infestations of the two species are observed. Other infestations can also be noted including hedgehog fleas (Archaeopsylla erinacei) and other less common flea species, such as the poultry flea (Echidnophaga gallinacea), the rabbit flea (Spilopsyllus cuniculi) and the human flea (Pulex irritans). S. cuniculi are sometimes seen on the pinnae of cats, appearing as small immobile dark spots most readily seen on pale coloured cats. Cat fleas can also infest small mammals including rabbits and ferrets.

Effect of infestation

During the feeding process fleas can cause direct damage to skin and subcutaneous tissues and cause inflammation. Clinical signs are typically pruritus, erythema, excoriation, papules, lichenification, scale and crusting. Intermittent or continuous exposure can result in the development of flea allergy dermatitis (FAD). Affected animals are allergic to allergens in flea saliva, with severity varying between individuals (Rust, 2005).

Fleas are also reported vectors of pathogens such as Rickettsia felis and Bartonella henselae (cat scratch disease). Both cat and dog fleas act as intermediate hosts for the tapeworm Dipylidium caninum. Fleas can cause anaemia where infestation is particularly heavy. Clinical signs develop depending on the factors indicated in Table 1.


Key factors
Frequency of flea exposure
Duration of flea infestation
Presence of secondary infections or other concurrent skin disease
Degree of hypersensitivity

Life cycle

Only the adult stages can be found on the host; pupae, larvae and eggs can be found in cracks on the floor, with pupae often covered in dust and debris. The life cycle stages are shown in Figure 1. Relative humidity must be between 50% and 95% with the larval stage most prone to desiccation. Above 95% humidity there is a risk of fungal overgrowth. The tolerated temperature range for environmental stages is between 4°C and 35°C. The development from egg to adult can take as little as 14 days or as much as 140 days, depending on the abiotic variables. Indoor environments with central heating or carpeted floors may be suitable for flea development throughout the year. Moreover, from approximately March to November, fleas may be able to multiply outdoors in suitable locations, partly explaining their increased prevalence during the warmer months (Rust, 2005).

Figure 1. Flea life cycle stages.

Identification

Many owners do not realise that their pet has a flea infestation (Bond et al, 2007). Moreover, a proportion of those whose animals were carrying fleas did not realise that the immature stages of fleas develop in the domestic environment (Bond et al, 2007).

Infection may be diagnosed by combing the animal's coat and seeing fleas or by placing debris onto damp white paper or tissue. Flea faeces will appear as black spots surrounded by a red ring of undigested blood. FAD can be confirmed by a combination of the presence of fleas or faeces (although the excess grooming present in some animals makes it very difficult to find either fleas or flea faeces on some individuals) and a response to treatment, together with elimination of other differential diagnoses. Where it is difficult to find signs of fleas on the animal then allergy tests may assist in confirming the diagnosis.

Control

The annual cost of flea control for pets is estimated to exceed 1 billion dollars in the USA and 1.1 billion Euros in Western Europe (Rust, 2005). Since the 1990s there has been a major increase in the number of flea control treatments available, including insect growth regulators (IGRs) such as methoprene and lufenuron (insect-developmental inhibitor), insecticides such as fipronil (phenylpyrazole), pyriprole, metaflumizone, indoxacarb, nitenpyram, imidacloprid (chloronicotinyl) and selamectin (avermectin) (Rust, 2005).

Control of flea infestations depends on a combination of treatment and other management measures such as hoovering and washing of a pet's bedding to reduce the number of immature stages in the environment. Often treatment needs repeating at intervals, typically monthly, to ensure an infestation is controlled. Ensuring control of the pre-emerged adult stage, causing the so-called ‘pupal window’ (ESCCAP, 2010a), is critical to control an infestation. This stage is typically found in locations which are inaccessible either to insecticides or cleaning and may cause apparent treatment failure as they emerge from the environment and infest the animal. Other causes of apparent treatment failure are summarised in Table 2. Depending on the scenario and likelihood of reinfestation, pets may be monitored for fleas and treated when necessary or preventive treatments administered (ESCCAP, 2010a). Preventative use of host-targeted insecticides for pets may be valuable in pets that have access to outdoor environments.


Reason
Fleas High level of environmental infestation, due to relatively low specificity of this parasite
Irregular release, sub dosing or reduced concentration of the active ingredients on patient's body, also incorrect product application
Wide range of hosts
Extreme resistant pupae in the environment (4-6 months), with consequent emergence of new adult fleas
Failure to treat all pets in the household
Aquisition of reinfestation from the outdoor environment
Ticks High level of environmental infestation, due to relatively low specificity of this parasite
Irregular release, sub dosing or reduced concentration of the active ingredients on patient's body, also incorrect product application

Ticks

Ticks are arachnids divided in two families: Ixodidae, ‘hard ticks’, and Argasidae, ‘soft ticks’. The ticks that affect companion animals are ‘hard ticks.

A female tick can measure up to 1 cm when fully engorged and an engorged Dermacentor spp. may be even larger. The most common ticks in the UK are Ixodes ricinus (the sheep tick), Ixodes hexagonus (the hedgehog tick), Ixodes canisuga and Dermacentor reticulatus (the marsh tick) (Smith et al, 2011).

Effects of infestation

Ticks are important as vectors of tick-borne diseases (TBDs) to pets and to humans. In the UK, I. ricinus is important in the transmission of Borrelia burgdorferi, the Lyme disease agent and Anaplasma phagocytophilum, the cause of granulocytic anaplasmosis. The predilection sites of ticks to bite are around the face, ears, axillae, interdigital, inguinal and perianal regions. Tick attachment sites may become infected or micro-abscesses may develop, particularly where a tick has been incompletely removed.

Life cycle

Ticks found in the UK are three-host ticks (Figure 2) and each stage feeds on a new host for a period of approximately 1 to 2 weeks. In the case of I. ricinus, eggs are laid in the environment and then six-legged larvae emerge and seek a suitable host (rodents and birds) to feed on. Once engorged, they return to the environment to moult to eight-legged nymphs. These too seek a suitable host (rabbits and deer) to feed on. They too then return to the environment to moult to eight-legged adults. They mate and seek for a suitable host (livestock, humans or pets) to have a single blood meal of 2 weeks and then the females return to the environment to lay their eggs. Ticks can thrive only if there is a suitable microclimate and host density. They have two traditional peaks of activity during the year: March to June and August to November.

Figure 2. UK tick life cycle.

Identification

Ticks may be identified by possessing a hypostome: the part of their mouthparts with backward directed ‘teeth’ which is a characteristic of ticks. As with other acari, the thorax and abdomen is fused with a small capitulum at the enterior end. Larval (or ‘seed’) ticks have three pairs of legs but nymphs and adult ticks possess four pairs of legs. The most common ticks in the UK, Ixodes spp., are characterised by a groove running anterior to the anus on the ventral side of the tick. Other features such as the shape of the coxae of the legs and of the palps are used to identify ticks to species level.

Control

There are a number of acaricides available to treat tick infestations in the UK that contain a single ingredient and there are others that contain multiple ingredients to broaden their spectrum (Beugnet and Franc, 2012). One example is indoxacarb: an insecticide-only molecule which produces a blockade of Na+ channels, causing inhibition of nerve activity and lethal paralysis and active only after bio activation by the insects' enzymes. Recently, a combination with permethrin has been developed to add tick elimination to the marketing claim. Active ingredients and their associated trade names are shown in Table 3.


Chemical family Active ingredient Activity spectrum Species Trade name*
Ticks Fleas
Pyrethroids Permethrin X DOG Advantix®
Neonicotinoids Imidacloprid X DOG,CAT Advantage® Advocate®
Advantix® Seresto®
Milbemycins Moxidectin X DOG,CAT Advocate®
Neonicotinoids Nitenpyram X DOG,CAT Capstar®
Phenylpyrazoles Fipronil X X DOG,CAT Frontline® Fiprocat®
Frontline Combo® Fipnil®
Effipro® Fiprospot®
Eliminall® Flevox®
Fiprodog® Certifect®
Juvenile hormone analogue (S)-Methoprene X DOG,CAT Certifect® Frontline Combo®
Neonicotinoids Pyriprole X X DOG Prac-tic®
Semicarbazone Metaflumizone X DOG,CAT Promeris® Promeris Duo®
Oxadiazine Indoxacarb X DOG,CAT Activyl®
Avermectins Selamectin X DOG,CAT Stronghold®
Pyrethroids Deltamethrin X DOG Scalibor®
Pyrethroids Flumethrin X DOG,CAT Seresto®
Benzoylurea Lufenuron X DOG,CAT Program® Program Plus®
Spinosyns Spinosad X DOG Comfortis®
Formamidines Amitraz X DOG Promeris Duo® Certifect®

The parameters for tick control are described in Table 4. Control in the future may incorporate biological control, although to date this remains elusive (Willadsen, 2006). Of particular interest have been fungi of the genus Beauveria and Metarhizium, but there are problems facing the practicality of these agents being manufactured and distributed and the stability of using living agents in the field.


Prevention
Acaricides on animals (and in the environment for Ixodes canisuga), bearing in mind integrated strategies
Non-chemical strategies, environment management such as cleaning (kennel tick Ixides canisuga)
Avoid tick-infested environments, use of tick repellents such as permethrin (and DEET for humans)
If visiting tick-infested areas, check for any attached tick, physical examination. Removal with a proprietry tick removal device

But what happens when you get cases of reinfestation in pets and angry pet owners enquiring for a solution? As Beugnet and Franc (2012) have shown, there have not been any confirmed cases of drug resistance to recent topical ectoparasiticides over the past 10 years. Failures in the control of tick and flea infestations are to be attributed to ecological and biological reasons. These are specified in Table 2.

Mites

The ear mite, Otodectes cynotis, is another of the parasites that are endemic in both dogs and cats the UK, although there do not appear to be any recent prevalence figures. The other mites, Sarcoptes scabiei, are common in some geographic areas which may be associated with infection in the local fox population. The harvest mite, Neotrombicula autumnalis, is common in some localities such as the Cotswolds, Malvern Hills and Edinburgh in late summer.

Effect of infestation

Some dogs and particularly some cats tolerate O. Cynotis without obvious clinical signs, though there may be dark brown wax with the appearance of coffee grounds in the external ear canal of affected individuals. Other animals may shake their heads or scratch their pinnae. Haematoma may develop as a result.

S. scabiei infestation is normally highly pruritic and results in a marked increase in scratching and rubbing of the affected area. Affected areas typically appear erythematous then crusted with areas of hair loss. A proportion of affected animals show a positive pinna pedal reflex.

Infestation with harvest mites is also markedly pruritic and produces a localised dermatitis in the areas where the mites feed.

All of these mites can infest humans, but ear mite infestation of humans is extremely rare and canine scabies tends to be self limiting in humans.

Life cycle

All of the mites, with one exception, found on dogs and cats are permanent ectoparasites with all of their life cycle spent on the host. In these species, female mites lay eggs which hatch into immature mites which go through a series of developmental stages before becoming adults. Eggs are laid in the locality of the infestation, with female Sarcoptes mites creating new burrows in the skin surface specifically for this purpose.

The exception is the harvest mite where it is only the larval stage which is parasitic. Larvae are abundant in late summer and parasitise a variety of hosts for a number of days before dropping off to continue their development as free living mites.

Identification

Ear mites may be seen as small white mites against the dark wax of the ear canal using an auroscope. Alternatively, a sample of debris from the ear can be examined microscopically for mites.

Microscopic examination of deep skin scrapes from the edges of affected areas are necessary to see the short-legged Sarcoptes mites, characterised by spines and pegs on their backs. These mites are not normal skin inhabitants and so finding one mite is diagnostic.

Clumps of Neotrombicula mites can be seen as orange dots against the skin of the animal. Each mite has an orange colour and it may be possible to examine the mite microscopically, although they tend to be fragile when removed. Like other larval mites, each has three pairs of legs.

Control

Mite infestations require specific treatment to eliminate the infestation. There are treatments specifically licensed to treat Otodectes and Sarcoptes infestations and, depending on the treatment, repetition may be necessary to eliminate young mites protected in the egg at the time of the original treatment.

There are no treatments specifically licensed to treat harvest mite infestation, although fipronil and metaflumizone and amitraz (dogs only) have both been reported to be effective.

Endoparasites Toxocara spp.

Adult Toxocara spp. are found in the small intestine of dogs and cats cats following the ingestion of eggs from the environment or larvae in paratenic hosts. Toxocara canis is endemic in the dog population with the majority of puppies infected (Barriga, 1991). Toxocara cati is endemic in cats. Overgaauw and van Knapen (2013) have reported that infection rates of T. canis and T. cati vary greatly. T. canis infection rates range from 3.5% to 34% in dogs from different epidemiological environments: including pets, shelter, stray and rural dogs. T. cati infection rates range from 8% to 76% in cats.

Effect of infection

Low level infections are well tolerated in dogs and cats, particularly in adult animals. Larvae typically go through a migratory phase prior to developing to adulthood in the intestine and the effect of larval migration through the lungs of cats has recently been investigated by Ray Dillon et al (2013). These authors demonstrated that migrating larvae can have marked effects on respiratory function. Heavy infections of adult worms can cause stunting and intestinal obstruction or intussusception.

Classically there are three syndromes reported following human infection with Toxocara larvae. Infection with large numbers of larvae can give rise to visceral larva migrans (VLM), while larval migration through the eye results in ocular larva migrans (OLM). Good et al (2004) reported a study in Ireland in schoolchildren with confirmed ocular toxocarosis. The third syndrome is covert larva migrans, a syndrome with more poorly defined symptoms. The evidence for the impact of larva migrans is spread across the literature, particularly as there are a number of organ systems that may be affected. For example, Bede et al (2008) reported an association between chronic cough and toxocarosis.

Evidence for an effect on childhood learning and ability has recently been published. A study carried out in the United States involved a nationally representative sample of the population in which 3949 children from 6–16 years of age were tested for Toxocara spp. antibodies. Their cognitive function was assessed by measuring components with two standardised tests: the Weschler Intelligence Scale for Children-Revised (WISC-R) and the Wide Range Achievement Test-Revised (WRAT-R). Infected children scored significantly less than their counterparts in maths, reading, block design performance and verbal digit span. A strong association was seen between Toxocara spp. seropositivity and reduced cognitive function. In this study the researchers looked for confounding factors and failed to find any (Walsh and Haseeb, 2012), however the reason for this association is the subject of further investigations.

Life cycle

The complete life cycle of Toxocara spp. can be seen in Figure 3.

Figure 3. Complete life cycle of Toxocara spp.

Identification

Patent Toxocara spp. infections (infections where there is at least one adult female laying eggs) can be identified by the presence of characteristically dark eggs, each measuring about 90 µm in diameter with a characteristically thick shell with a pitted surface in faecal samples. Immature infections and male worm-only infections may be missed with this method. Occasionally whole worms are vomited or passed in faeces. These may measure up to about 10 cm and possess three lips at the anterior end, together with two small ‘wings’ or alae on either side of the anterior end of the worm. Where none of these signs are available for examination a crude assessment of likelihood may be made, with puppies and young dogs under 6 months most likely to be infected and a smaller proportion of adult dogs likely to be infected.

Control

Puppies that are infected in-utero or via the dam's milk can pass large numbers of eggs into the environment from as early as 2.5–3 weeks, before which diagnoses by faecal sample examination are negative. Therefore, a risk assessment is carried out and infection is assumed. Hence all puppies should be treated with anthelmintics starting when they are 2 weeks of age and then fortnightly until 2 weeks after weaning. Monthly treatments should then commence until the pups reach 6 months of age. This is different to kittens where prenatal infection does not occur and so treatment of all kittens should commence at 3 weeks of age (ESCCAP, 2010b).

Nursing bitches and queens should be treated concurrently with the first treatment of their offspring as they could develop patent infections. As the pre-patent period for Toxocara spp. takes over 4 weeks it is recommended to treat at least once per month in high risk scenarios like households with toddlers and the use of a back garden. In cases with a lower risk of infection then treatment four times a year may be advisable.

Management measures such as picking up and disposing of faeces and covering sandpits assist in preventing contamination of the environment with worm eggs, particularly in children's play areas.

For this reason periodic treatments with anthelmintics, or treatment based on the results of diagnostic faecal samples, are of great value for the control of intestinal helminths. A regular treatment every 4–6 weeks would prevent most patent infections.

Tapeworms

Sources for tapeworms in cats are fleas (for D. caninum) and rodents (for Taenia taeniaeformis), whereas dogs can acquire tapeworms from fleas (for D. caninum), rabbits (for Taenia spp.), ruminants (for Taenia spp. and Echinococcus granulosus) and horses (for Echinococcus equinus). In all cases, infection is acquired through ingestion of the metacestode stage of the tapeworm carried by the intermediate host.

Effect of infection

None of the tapeworms have any major impact on the canine or feline host, although tapeworm segments produced by Taenia spp. and D. caninum seen in the faeces may be unsightly to owners. It is the intermediate host where effects are often more significant. For example, infected dogs defaecating on pasture caused an outbreak of Taenia ovis metacestode infection in sheep (Eichenberger et al, 2011). The metacestode of E. granulosus can infect humans, with hydatid cyst development typically in the liver or lungs following ingestion of eggs passed by dogs. Such cysts are normally removed surgically and are a major event for the affected individual (Budke et al, 2005).

Key points

  • Pet owning brings risk and responsibilities as well as benefits.
  • Everyday parasites are being forgotten.
  • Pet parasite control should link in to the One Health concept.
  • Many owners are unaware when there pet has a flea infestation.
  • Parasites are significant as vectors of diseases.
  • Life cycle

    Every tapeworm needs at least one intermediate host to complete its life cycle (Figure 4).

    Figure 4. Tapeworm life cycle.

    Identification

    D.caninum and Taenia spp. infections may be identified by seeing segments either in faeces or moving around the anal area of the affected pet. Examination between two microscope slides permits differentiation between the two genera as D. caninum has a genital pore on each side of the segment while Taenia spp. have only one per segment. Echinococcus spp. segments are too small to be seen. In faecal samples, eggs of D. caninum are contained in egg packets, while Taenia spp. and Echinococcus spp. eggs are identical. Where necessary, infections can be distinguished using coproantigen or polymerase chain reaction (PCR) methods.

    Control

    Control depends on a combination of treatment and management, for example by feeding dogs and cats on cooked food, controlling flea and louse infestations and preventing access to prey and carcases.

    The treatments available are: praziquantel (for all tapeworms) and fenbendazole (but only for Taenia spp. infections). Where control of access to intermediate hosts is not achieved then signs of reinfection can occur rapidly. For example the prepatent period of D. caninum is only 3 weeks. Thus repeat treatment may be necessary. Where there is a risk of E. granulosus, treatment every 6 weeks will prevent patent infection. More information about E. granulosus control can be found on the Welsh Assembly website (http://wales.gov.uk).

    Conclusion

    The everyday parasites that are already endemic within the pet animal population continue to pose diagnostic and control challenges for owners and veterinary professionals. Their control remains important for both animal and human health and they provide good examples of One Health for animals and human beings and, thus, the value in cooperation between human and veterinary professionals.