Since 2012, when the restrictions on pets travelling were relaxed, there has been an increase in the number of pets travelling abroad and being imported – legally and illegally. This is partly due to a demand for cheap pedigree dogs (Dogs Trust 2017) and a trend for adopting rescue dogs from abroad. This activity increases the likelihood of introducing new parasites into the UK. So it is crucial for the veterinary profession to be vigilant for parasitic disease and vectors (such as ticks) to reduce the risk of novel parasites becoming established, reduce zoonotic risk and improve clinical outcomes for infected patients. By doing this module you will:
be aware of the parasitic diseases that may be found in an imported pet
know what clinical signs to look out for
be aware of the effective treatments, and how to get them
find out where to get further information and specialist advice.
Veterinary professionals are most likely to encounter imported cats and dogs in one of three ways:
Puppies imported legally. The minimum travel age for pets is 15 weeks (i.e. 12 weeks – the minimum age for rabies vaccination – plus 3 weeks) (Animal and Plant Health Agency). Puppies can be imported legally into the UK under the Pet Travel Scheme (PETS) if they are microchipped, rabies vaccinated, and (if from a non-EU/unlisted country) also rabies antibody-tested after vaccination. They should also have been treated for tapeworm 1–5 days before entry into the UK. Even if a puppy has been legally imported, all of these criteria should be checked, because rabies vaccination and tapeworm treatment for Echinococcus multilocularis are a vital part of zoonotic disease control. Owners may be under the misapprehension that their pet has been certified ‘disease free’, to be eligible for travel under PETS.
Puppies or kittens imported illegally. Any documentation should be thoroughly checked. However, falsified pet passports may difficult to distinguish from genuine passports and cannot be relied upon to accurately report a puppy’s age. Puppies suspected of being too young to legally travel on the scheme should be reported to Trading Standards.
Rescue dogs imported legally. There is a growing trend for rescuing stray adult dogs from abroad. The welfare of street dogs in some Mediterranean and eastern European countries is often poor and rescue organisations seek to rescue and rehome them, often in another country. They may be taken to practices in the UK for health checks by their new owners. It is also important to be aware of the possibility that farmed puppies may be trafficked under the guise of rescue organisations.
The following sections describe the exotic parasites and vectors that have been found recently on pets that have entered the UK from abroad.
Dermacentor reticulatus ticks are a vector for the protozoan Babesia canis, a cause of potentially life-threatening anaemia (babesiosis) in dogs. Babesia exclusively infects erythrocytes, which can lead to immune-mediated haemolytic anaemia. Dogs typically present with pale mucous membranes, jaundice, fever and an enlarged liver or spleen. There may be depression, anorexia, red or dark brown urine associated with haemoglobinuria, and gum petechiation assocated thrombocytopaenia (ESCCAP 2012). Babesia infection is often lifelong and disease relapse is common, so dogs with acute disease may present months or years after travel. The prevalence of feline Babesia species such as Babesia felis is high in South Africa and endemic in other African countries. Cats imported from these countries may have clinical babesiosis with mild to moderate anaemia in the absence of fever (ESCCAP 2012).
Rhipicephalus sanguineus ticks are being seen regularly on imported and travelled dogs (Abdullah et al 2016). They can carry a wide range of organisms pathogenic to dogs, including the Gram-negative intracellular bacteria Ehrlichia canis. Travelled and imported dogs presenting with lymphadenopathy and pyrexia should be checked for R. sanguineus ticks, and house infestation considered a possibility. Acute and chronic ehrlichiosis, and also tick-borne encephalitis (a viral disease carried by Ixodes ricinus ticks) may present with signs associated with meningitis and meningoencephalitis, including ataxia, seizures, paresis, hyperesthesia, cranial nerve deficits and vestibular signs. These may present in dogs with a recent history of travel, or in the case of chronic ehrlichiosis, months or years later. It is important to recognise the acute signs of E. canis infection in dogs, because without treatment it may progress to the chronic, often fatal form.
The protozoan Leishmania infantum is transmitted by sandflies. Leishmaniosis is a chronic disease with a variety of presentations and periods of remission. Signs, which are due to immune complex deposition in various organs, include lymphadenopathy, skin lesions, weight loss, enlarged spleen and signs associated with glomerulonephritis (ESCCAP 2012). Less commonly there may be polyarthritis, thrombocytopaenia, ocular inclusion bodies, uveitis and neurological signs associated with spinal and central nervous system granulomas. Signs may take months or years to develop so foreign travel may not be recent. Leishmania may also be transmitted venereally from dog to bitch and from an infected mother to her pups (Naucke & Lorenz 2012).
Thelazia callipaeda is a vector-borne eye worm with hosts that include dogs, cats and humans. The first confirmed cases in the UK were recently recorded in dogs imported from Romania, Italy and France (Graham-Brown et al. 2017). The primary fruit fly vector Phortica variegate has been recorded in the UK and conditions are favourable for spread. Disease is caused by direct inoculation of larvae into the eye of the animal. Although often subclinical, ocular thelaziosis can commonly cause conjunctivitis, keratitis, epiphora, eyelid oedema, corneal ulceration and, in serious cases, blindness. Close examination of the conjunctiva will often reveal worms actively moving on the surface. All imported cats and dogs should be checked for low grade or subclinical infections to prevent exposure of the fruit fly vector in the UK to this parasite.
The filarial nematode Dirofilaria repens, which is transmitted by mosquitoes, is a zoonosis. The first cases were recently confirmed in UK dogs imported from Corfu and Romania (Wright 2017; Agapito et al. 2017). Infection is commonly subclinical but clinical signs can occur. Dermatitis is the most common presentation, as multifocal nodules in the skin or papular dermatitis, which may reoccur seasonally for years after infection and lead to pruritus, erythema, papules and focal or multifocal alopecia. Less commonly there may be hyperkeratosis, crusting, distinct nodules, acanthosis and secondary pyoderma. Migration of worms to other parts of the body can lead to other signs including conjunctivitis, anorexia, vomiting, fever, lethargy and lymphadenopathy. Ocular migration of worms into the vitreous humour is uncommon but does occur and therefore D. repens should be considered as a differential diagnosis if worms are seen in the eye as well as in dogs presenting with dermatitis that have travelled abroad. Infected dogs act as reservoirs of infection for the mosquito vector, which is present in the UK. If infected dogs continue to enter the UK and are not treated quickly, UK mosquito populations may be exposed to the parasite and the disease could become endemic.
Dirofilaria immitis infections are often seen in imported dogs, but the mosquito vector currently does not survive for long enough in the UK to allow it to become endemic, although with an increasingly mild climate, this could change in the future. The most common clinical signs in infected dogs are coughing, rapid or laboured breathing, and exercise intolerance. Acute clinical signs are associated with thromboembolism, subsequent pulmonary hypertension and caval syndrome (due to parasites located in the venae cavae and right atrium). Worm death can lead to thromboembolism and anaphylaxis. Typical acute clinical signs include anorexia, weakness, breathing difficulty, vomiting and, rarely, respiratory signs linked to pleural effusion, and sudden death. Chronic signs are sometimes due to respiratory inflammation and include coughing, dyspnoea, anorexia, vomiting and rarely chylothorax. Chronic respiratory signs tend to be more common in cats (ESCCAP 2012).
Several cases of the nasal pentastomid Linguatula serrata (tongueworm – the common name for the tongue-shaped adult worm) have been seen in the UK recently in dogs imported from Romania (Mitchell et al. 2016; Thomas 2018). Infection is acquired through the consumption of raw meat and offal in endemic countries. L. serrata is a zoonosis. Infection in dogs and cats is commonly subclinical. However, there can be rhinitis and nasopharingitis with associated chronic sneezing and/or coughing, purulent nasal discharge and epistaxis. It is crucial that these signs are detected early in affected dogs to limit zoonotic exposure to owners and others in contact with the animal and who may ingest infective eggs in the nasal discharge or from faecal contamination.
Potential consequences of parasite infection
The following sections describe the treatments for exotic parasites.
The treatment for B. canis infection is the antiprotozoal drug imidocarb (ESCCAP 2012). ESCCAP (The European Scientific Counsel Companion Animal Parasites) recommends a dose of 5–6mg/kg by intramuscular or subcutaneous injection repeated after 2 weeks (ESCCAP 2012). Other doses have been recommended: the BSAVA Formulary recommends 6.6mg/kg repeated after 2–3 weeks, which is the dose approved in the USA (BSAVA 2017; Plumb’s 2018). Clinical improvement is said to occur within 48 hours in the absence of hepatic, renal and vascular complications (ESCCAP 2012). Adverse effects of imidocarb include pain during injection and mild cholinergic signs (salivation, nasal drip and brief episodes of vomiting). Less common effects include panting, diarrhoea, restlessness, and injection site inflammation (more common after the second dose and, rarely, may ulcerate). Hypoglycemia has been reported and, rarely, severe renal tubular or hepatic necrosis, and severe cholinergic signs (Plumb’s 2018). Cholinergic adverse effects can be treated with an antimuscarinic (e.g. atropine or glycopyrrolate) if necessary (Plumb’s 2018).
If imidocarb cannot be obtained immediately, there are anecdotal reports that the antibiotic clindamycin (which is active against a wide range of protozoa) may have some efficacy. The suggested dose for dogs is 12.5mg/kg by mouth twice daily for at least 2 weeks (Plumb’s 2018). Clindamycin may cause adverse gastrointestinal effects.
Treatment may not completely eliminate the parasite, leaving infected dogs as low level subclinical carriers. This is important to bear in mind because infected dogs may have subsequent relapses and act as potential reservoirs of infection.
Where to get the medicine. Imidocarb is licensed in the UK for the treatment of cattle (Imizol SPC). There are several oral forms of clindamycin licensed for use in dogs, but not for this indication.
The treatment of choice for E. canis infection is doxycycline 10mg/kg by mouth once daily for 4 weeks (ESCCAP 2010; Ronaxan SPC). Complete eradication of the pathogen is not always achieved but treatment leads to a resolution of the clinical signs and a reduction in bacterial load. A longer duration of treatment may be needed in severe and chronic ehrlichiosis (Ronaxan SPC – unlicensed use). Adverse effects of doxycycline include vomiting, oesophagitis and oesophageal ulcerations (Ronaxan SPC). The likelihood of oesophageal effects can be reduced by ensuring the tablets are washed down into the stomach with food or water (Plumb’s 2018). Photodermatitis can occur after exposure to sunlight. Ronaxan SPC)
Where to get the medicine. The Ronaxan brand of doxycycline tablets is authorised in the UK for the treatment of Erlichia canis infection in dogs (Ronaxan SPC).
International guidelines on the management of leishmaniosis in dogs recommend treatment with allopurinol by mouth for 6–18 months usually together with either meglumine antimoniate by subcutaneous injection for 4–6 weeks or miltefosine by mouth for 4 weeks (ESCCAP 2010; Leishvet 2018). Treatment with any of these drugs is unlikely to completely clear the organism in dogs, but can substantially reduce the parasitic load. There may be an improvement within a few weeks of starting treatment but clinical cure is only achieved after several months, and relapses are common. Dogs remain infected even when a clinical cure is achieved (ESCCAP 2012). Supportive treatment for hepatic and renal dysfunction function may be needed. The optimal treatment of leishmaniosis in cats is not known.
Allopurinol is a purine analogue of adenosine nucleotides that blocks RNA synthesis in Leishmania parasites, leading to inhibition of parasite multiplication. Vomiting is the most common adverse effect seen in dogs. Other gastrointestinal signs (inappetence, diarrhoea) may also be seen. Allopurinol treatment in dogs can lead to increased urinary xanthine levels (Torres et al. 2011).
Meglumine antimoniate inhibits leishmanial enzymes required for glycolic and fatty acid metabolism. The main adverse effects are injection-site reactions (abscesses, cellulitis), lethargy and gastrointestinal effects. It may potentially cause nephrotoxicity (Plumb’s 2018).
Miltefosine has an unknown mode of action. Vomiting is the most common adverse effect; it may also cause diarrhoea and inappettance.
Domperidone is licensed in some countries for the treatment of leishmaniosis and so dogs imported already on treatment may be on a regimen including this drug. It may have effects on cell-mediated immunity, possibly via effects on prolactin through dopamine antagonism (Plumb’s 2018). Evidence on the efficacy of domperidone is mixed but it is an alternative if none of the conventional drugs are tolerated.
Where to get the medicine. There are no licensed veterinary forms of allopurinol, but several generic and branded tablets are licensed in the UK for humans (e.g. Zyloric). There is no licensed form of meglumine antimoniate or miltefosine in the UK. Domperidone is a licensed human medicine available as tablets and oral suspension.
Treatment consists of removal of adult worms from the conjunctiva, and medical treatment with milbemycin or moxidectin (Motta et al 2012; Otranto et al 2016).
Where to get the medicine. :A single application of a spot-on containing moxidectin plus imidacloprid (Advocate), or two doses of milbemycin oxime plus praziquantel tablets 1 week apart (several brands available) are licensed for the treatment of T. callipaeda in dogs. Check the Parasiticide Guide for licensed brands.
Discrete subcutaneous nodules containing adult worms can be removed surgically with an excellent prognosis. For dogs with ocular signs, diffuse skin disease or more generalised clinical presentations, medical treatment is needed. Moxidectin plus imidacloprid spot-on preparations are licensed for the treatment of cutaneous dirofilariosis at a monthly dose for 6 months (Advocate SPC). Check the Parasiticide Guide for licensed brands.
Treatment of infection with adult worms requires surgical removal or medical treatment. In endemic countries, intravascular snares and forceps are often used to remove large numbers of worms in the least invasive manner; this is essential in caval syndrome, in which death can occur within 2 days of onset of acute signs. However it requires experience and special equipment, and is reserved for very large worm burdens that lead to acute complications. Consequently, in the UK, medical treatment is usually needed. Published treatment protocols for dogs vary but the essential components are pre-treatment with doxycycline and a macrocyclic lactone, before treatment with melarsomine (the effective treatment for heartworm) (ESCCAP 2012).
The antibiotic doxycycline is used to kill Wolbachia bacteria living in the heartworms. The worms and bacteria have an obligatory symbiotic relationship and doxycycline therapy makes the worms more susceptible to melarsomine treatment (Kramer et al. 2011). A 4-week course of treatment is given before melarsomine therapy. A macrocyclic lactone is used several months before melarsamine to eliminate existing susceptible larvae, and allow older worms (between 2 and 4 months of age) to mature to an age at which they are more susceptible to melarsomine.
Melarsomine is an organic arsenical that is active against immature (stage 5) and adult Dirofilaria worms (Diroban SPC). It is given by deep intramuscular injection using a specific technique. American Heartworm Society guidelines recommend a three-dose regimen of melarsomine (Nelson et al 2017). The drug has a low margin of safety and so careful calculation of dose is needed. Injection-site reactions are common and sometimes severe. It may also cause coughing, depression, inappetance, fever, lung congestion and vomiting.
An alternative treatment to melarsomine is a “slow kill” regimen using doxycycline and moxidectin. This should not be used as first choice treatment because the treatment is lengthy and may be linked to the development of resistance (Bowman et al. 2012). It also carries a risk of anaphylaxis due to the killing of microfilariae from active infection over a long period of time. It should therefore only be used if surgery is not suitable or practical, and melarsomine not available. It is not recommended by AHS (Nelson et al 2014).
AHS guidelines give detailed information on the management of heartworm, including the use of prednisolone to control clinical signs of pulmonary thromboembolism (Nelson et al 2014). The AHS website includes a summary of the current guidelines.
Where to get the medicine. Melarsomine dihydrochloride powder for injection (brand names Immiticide, Diroban) is approved in the USA for use in dogs. Moxidectin + imidacloprid spot-on (Advocate) is licensed for heartworm pre-treatment (i.e. treatment of circulating microfilariae), for which it should be administered monthly for 2 consecutive months (Advocate SPC).
Treatment of tongueworm requires nasal flushing with warm salty water and surgical removal of parasites via endoscopy, but this may not be curative because the worms can attach to the sinuses. There is no known effective medical treatment. A case of Linguatula serrata in a dog imported into the UK from Romania was managed with broad spectrum anthelminitic therapy (fenbendazole and praziquantel/pyrantel) before the parasite was identified, and surgical cleansing of the sinuses, followed by isolation for 1 month; and monthly faecal sampling for 6 months was recommended, with close monitoring of clinical signs (Villedieu et al 2017). Another UK case has been reported to have been successfully treated with moxidectin (Thomas 2018).
If there is no suitable authorised veterinary or human medicine in the UK for the treatment of an animal, a veterinary medicine can be imported from the EU, or failing this, a human medicine, or a veterinary medicine from outside the EU (Gov.uk). It is the vet’s responsibility to demonstrate there is no suitable product available and to justify clinical need according to the Cascade. An application for importation takes 2–15 days. If approved, the product can then be obtained from a pharmaceutical company or through an online pharmacy. Merlin Vet is a veterinary wholesaler in the UK that specialises in importing medicines and can help source the required medicines from abroad and advise on the type of import certificate needed.
ESCCAP UK & Ireland recommends four key steps when dealing with imported or travelled pets arriving in the UK. These allow veterinary professionals to discuss management options with owners if parasites are present; improve prognosis of clinical cases; minimise the risk of spread of any disease; and carry out effective disease/parasite surveillance.
Check for ticks and identify any found. Identification of ticks allows the introduction and distribution of exotic tick species to be monitored in the UK but also indicates which tick-borne diseases the imported pet may have potentially been exposed to. Ticks can be sent to Public Health England for identification. Click this link for more information.
Treat dogs again with praziquantel within 30 days of return to the UK and treat for ticks if treatment is not already in place. This will ensure that E. multilocularis is eliminated from imported pets, regardless of the timing of their compulsory treatment or if there is doubt about it having been administered correctly or at all. Tick treatment will increase the likelihood of attached ticks being killed if they are missed on examination. Ticks are easily missed in large or long-coated breeds and in cats and dogs that are reluctant to be examined.
Recognise clinical signs relevant to diseases in the countries visited or country of origin. While it is not possible to be familiar with every exotic parasite a thorough and comprehensive clinical exam of imported pets will identify clinical signs and these can then be compared to parasitic diseases in the countries that the pet has visited.
Screen for Leishmania infantum. and exotic tick-borne diseases in imported dogs. These can have long incubation periods and carrier states. Infection can be lifelong and in some cases can carry a poor prognosis. Screening for these parasites will allow early diagnosis; discussion with the owner about the need for lifelong treatment and any associated zoonotic risk; and limit the wider spread of disease through effective tick control.
Often pets will have been bought in good faith, so broaching the issue of new pets being illegally imported can be difficult. Seek advice from Trading Standards before taking further action. None of the parasites described in this module are notifiable and there is no central agency for data collection on the incidence of imported parasitic infections in companion animals. However surveillance and compilation of data are essential to monitor spread and raise awareness. Veterinary practices that are members can record data through Liverpool University’s SAVSNET scheme. Cases can also be reported to ESCCAP UK & Ireland via the email address on the website, and highlighted through letters to veterinary publications such as the Vet Record and Vet Times. Further information on exotic parasites, pet importation and travel can also be found on the ESCCAP UK & Ireland website.
Owners planning to take pets abroad should be advised about reducing the risks associated with exotic parasites. See the module on Taking pets abroad.
Veterinary professionals in the UK are seeing increasing numbers of dogs and cats that have acquired infections with parasites that are new to the UK. Many of these require lifelong treatment and some need treatment with medicines that are not available in the UK. Early recognition and treatment are key to reducing the risks of parasite spread and transmission to humans as well as better outcomes for patients. Improved awareness and surveillance for parasites among dogs and cats, especially those imported from abroad, will help to tackle already reported parasites and other emerging imported parasites in the future.
If you prefer, you can listen to the whole audio presentation of this module using the following podcast. Don't forget that you can also download the podcast to your iPod, music player, tablet or smartphone using the Download link on the right of the audio player.
How we produced this module
Our modules start with a detailed outline and electronic literature search. We commission a collaborating author, who is a specialist in the module topic, to write a draft module. The collaborating author on this module was Ian Wright. The draft is circulated unsigned to a wide range of commentators, include practising first-opinion vets, other topic specialists, the companies that market any mentioned drugs and other organisations and individuals, as appropriate. They can raise points about the interpretation of evidence, ask questions that are important to clinical practice, and present alternative viewpoints. There is a rigorous editing and checking process and the result is a module that is evidence-based, impartial and relevant to clinical practice. The final module is unsigned because it is the result of collaboration.
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