Since the introduction of the Pet Travel Scheme (PETS), pet travel throughout Europe and the exchange of pets between countries has increased. This has occurred at a time of increased human migration and climate change, providing favourable conditions for the rapid spread of parasitic diseases and their vectors. Parasites considered as Southern European infections such as Dirofilaria immitis and Leishmania infantum are increasingly presenting in Scandinavian Veterinary clinics in travelled or imported pets. In addition, parasites not previously seen in Europe such as Linguatula serrata are also becoming increasingly prevalent and may be seen in imported animals.

Veterinary professionals must, therefore, be aware of exotic pathogens being present in these pets, be able to recognise relevant clinical signs and rapidly diagnose infection. This will improve prognosis in individual pets and reduce the risk of exotic parasites establishing new endemic foci.

Dirofilaria immitis (Heartworm)

Dirofilaria immitis is a filarial heartworm primarily of canids but also can infect ferrets and felines. It is endemic throughout Southern and Eastern Europe, and is a significant cause of heart disease in infected pets, and of bronchitis in cats. Transmission occurs through feeding by Culicine mosquitoes. Acute clinical signs occur through migration of larvae to the pulmonary artery, potentially leading to thromboembolism, Caval syndrome and subsequent pulmonary hypertension. Worm death can lead to anaphylaxis and thrombo embolism. Typical resulting acute clinical signs include sudden death, anorexia, weakness, dyspnoea, a jugular pulse and a weak femoral pulse, anaemia, haemoglobinuria, vomiting, and rarely pleural effusion.

Chronic signs are due to inflammatory responses in response to migrating larvae and aberrant migration. These tend to be respiratory in nature and include coughing, dyspnoea, anorexia, vomiting, and rarely chylothorax. Chronic respiratory signs tend to be more common in cats.

Although it is not endemic in Scandinavia, increasing numbers of Scandinavian pets are traveling to, and being imported from endemic countries. Although the culicine mosquito vector is endemic in most European countries, a colder climate in Northern Europe has prevented heartworm from becoming endemic. This is because the development of Dirofilaria microfilariae to the L3 larval stage requires 29 days at a constant 18 degrees centigrade (Lloyd 2011). Climate change, however, has allowed spread of the parasite northwards, raising the possibility that if this trend continues, that endemic foci could establish in parts of Southern Scandinavia. The Climate Division of the Norwegian Meteorological Institute reported that in certain parts of the country, the average temperature could be sufficiently high enough to allow development of the D. immitis larvae to reach the infective L3 stage in Norwegian mosquito species and endemic foci along the coast of southern Norway potentially be established. Blood antigen testing on 80 dogs imported into Norway from Eastern Europe found 7.5% to be positive for D. immitis, suggesting that a significant number of infected dogs are entering the country. This picture is also likely to be similar in other Scandinavian countries (Vatne 2014).

For this reason, Veterinary professionals must be aware of the possibility of infection in pets imported from Southern and Eastern Europe, or that have visited there. Pets having visited endemic countries need to be tested for heartworm if they have not been on preventative treatment so decisions can be made regarding future treatment and the risk of mosquito vectors being exposed to infection can be reduced.

A number of diagnostic test are available for heartworm diagnosis.

• Examination of blood for microfilaria - Direct smears are a highly specific test in experienced hands but also insensitive. Concentration techniques including filtration methods, Knott’s test (a form of sedimentation test) and buffy coat examination make direct blood examination more sensitive in canine patients but still extremely insensitive in the cat due to low circulating levels of microfilariae. If microfilariae are detected, the larvae must be distinguished from D. repens (Table 1) which will also be present in endemic countries.
• Ultrasound examination - The cuticles of adult heart worms are highly echogenic and so in experienced hands echocardiography can be very sensitive and specific. However, in cases with low burdens or with in experienced ultranosographers sensitivity will decrease.
• Antigen serology - This test is considered the gold standard in the living canine patient. It is highly specific and in canine patients, also highly sensitive. Although specificity still approaches 100% in cats, it is much less sensitive with as few as 36% of positive cases being identified. This has led to a new antigen test, the IDEXX SNAP® Feline Heartworm Antigen Test being developed and claims to have an increase of 15% in sensitivity over conventional antigen tests.
• Antibody serology - This is the most sensitive blood test available for heartworm diagnosis in cats (Atkins 1999). A positive result may indicate past or present exposure to infection and should be interpreted in relation to clinical signs and other diagnostic tests.

Table 1. Differentiating diagnostic features of Dirofilaria immitis and Dirofilaria repens microfilariae in the blood of dogs

Treatment of infections with adult worms requires surgical removal or treatment with an adulticide, the latter being contraindicated in cats. Steroids may be required for management of bronchitic signs in feline patients. Prophylaxis is desirable in travelling pets to reduce the risk of adult infection establishing.

Leishmania infantum

Leishmaniosis is caused by intracellular protozoan parasites of the genus Leishmania with Leishmania infantum being the predominant species in European cats and dogs. It has zoonotic potential and is a significant endemic zoonosis in southern Europe. Transmission occurs primarily through bites from infected phlebotomine sand flies, limiting the distribution of the parasite in Europe to the South of France and Southern Europe. Large numbers of cases however, are being seen outside of endemic areas in imported and travelled pets. Rapid diagnosis of infection is important as transmission can also occur through blood transfusion, vertical and venereal transmission. Identification of subclinical carriers and rapid recognition of relevant clinical signs will allow prevention of these secondary modes of transmission as well as monitoring and treatment, where required, of infected pets.

Leishmaniosis caused by L. infantum is chronic in nature with a variety of presentations and periods of remission. Signs are due to immune complex deposition in various organs and include alopecia, hyperkeratosis, dermal ulcers, polyarthritis, ocular inclusion bodies, uveitis, hepatopathy, glomerulonephritis, and neurological signs associated with spinal and CNS granulomas. Peri ocular alopecia (lunettes) are a classic sign and easily mistaken for atopy.

Leishmaniosis should always be considered as a differential when presented with skin disease, lymphadenopathy or weight loss in dogs that has been present in endemic areas. A number of tests are available to aid in diagnosis.

• PCR - is very specific and highly sensitive when skin biopsies, lymph node or bone marrow aspirates are used but is much less sensitive when used on peripheral blood. PCR testing on conjunctival swabs has proved to be an effective non-invasive technique with sensitivity and specificity of 78.4 and 93.8% respectively (Geisweid et al. 2013).
• Serology - Seropositivity is found in 88–100% of dogs with clinical signs and can indicate a predisposition to developing clinical signs in subclinical dogs. Quantitative antibody testing on serum using IFAT (cut of 1/80 or 1/100) allows monitoring of possible clinical development in sub clinical cases, and monitoring of treatment in dogs that are in remission.
• Biopsies - of skin, lymph nodes, or bone marrow. This is a highly sensitive and specific diagnostic method if multiple sites are taken but also more invasive than other tests.

Urinalysis is also a useful tool, revealing a proteinuria. The amount of protein in the urine is a more useful prognostic indicator than antibody titres.

Treatment carries a varying prognosis depending on progression of disease, hepatic and renal function. Infection is also life long and will require a life time of serological monitoring and possible treatment. Flare ups of disease are common and as a result, euthanasia should be considered as an option in clinically affected dogs if owners are unwilling or unable to undertake a lifetime of managemental care. The zoonotic aspects should also be discussed but kept in perspective, as there has never been a confirmed case of direct human infection from a dog or cat. Improvements in treatment success rates, however, have made treatment a viable option, with the aim of treatment being remission of clinical signs rather than clearance of infection. Infected cats and dogs should never be used for blood transfusions or breeding.

Treatment consists of allopurinol at 10–30 mg/kg in combination with Meglumine antimonite (100 mg/kg intravenous or subcutaneously) every 24 hours for 3–6 weeks or miltefosine orally (2 mg/kg every 24 hours for 4 weeks). The latter has the advantage in renal compromised patients of being metabolised solely by the liver. Gastrointestinal side effects, however, from its use are common. Treatment with allopurinol alone may be required for up to 6 months after resolution of clinical signs to prevent relapse and some patients will need to remain on the drug indefinitely. Supportive treatment for hepatic and renal function may also be required.

Dogs that have travelled without protection or those imported from endemic countries should be antibody tested on arrival so their infection status can be monitored, breeding and blood transfusion can be avoided, and owners can be prepared for the possibility of disease developing.

Tick Borne Diseases Transmitted by Dermacentor reticulatus and Rhipicephalus sanguineus

Pets travelling abroad may come into contact with tick-borne diseases transmitted by Rhipicephalus sanguineus. R. sanguineus has traditionally been restricted to warmer climates in the South of Europe but is moving North with untraveled cases of Ehrlichia canis having been reported in France, Switzerland, and Austria. Although it is unlikely that R. sanguineus would currently establish outdoor endemic populations in Scandinavia, populations can become established in heated homes. Anaplasma platys, Ehrliciha canis, and Hepatozoon canis infection can all present with fever, lymphadenopathy, and thrombocytopaenia and should be considered as a differential in pets presenting with these signs that have travelled in, or been imported from R. sanguineus endemic countries.

Diagnosis can be achieved through blood serology or PCR and treated with doxycycline at 10 mg/l per os sid for 3 weeks. Prognosis is improved with early intervention and if allowed to progress to its chronic form, E. canis is often fatal.

It is essential that pets are treated with an effective tick product during travel, and checked for ticks on return to Scandinavian countries. Checking pets for ticks at least every 24 hours and removing any found with a tick hook will also help to prevent disease transmission. If travelling to R. sanguineus endemic countries, this product should be a licensed pyrethroid repellent as E. canis can be transmitted within hours (Fourie et al. 2013) and should be applied 1 week before travel. Ticks removed should be identified to establish which tick-borne diseases may have been transmitted. Imported pets should be tested for tick-borne diseases by serology or PCR.

Dirofilaria repens

The mosquito vectors for D. repens are already endemic in Scandinavia. but climate has not been suitable for endemic establishment of the parasite. D. repens appears to have less stringent temperature requirements meaning that it is more likely to establish in Northern Europe (Morgan 2016). Definitive hosts are carnivores including dogs and cats. Humans can also be infected through being exposed to mosquito bites. Transmission occurs in a similar manner to D. immitis but with adult worms living in skin nodules and subcutaneous tissues rather than the cardiovascular system. Infection can be subclinical or lead to dermatitis and skin nodules. Less commonly, adult worms migrate to the eyes of the host where they may be visible and may cause conjunctivitis. Prevalence of dirofilariasis in cats tends to be only one tenth of that in dogs and typically occurs in areas of high canine infection rates.

Diagnosis can be achieved through identification of microfilariae in the blood or through biopsy and histological examination of skin lesions and nodules. Moxidectin/imidacloprid spot on preparations are licensed for treatment and surgical removal of adult worms is also sometimes required. Cases have already been reported in Norway from dogs imported from Romania (Vatne 2014) and so vigilance for relevant clinical signs is vital so treatment can be initiated before local mosquito populations are exposed to infection.

Linguatula serrata

This parasite known as a ‘tongue worm’, is actually a pentastomid and is now thought to be more closely related to arthropods than true worms. The adult parasite is an elongated tongue-shape and is found in the nasal cavities or sinuses of dogs and foxes. Infection occurs through the ingestion of nymphs in raw offal of infected intermediate hosts such as ruminants, rabbits, and horses. Eggs from the adult parasite are passed in the faeces or nasal secretions of infected dogs and are immediately infective. Adult parasites are large with females typically 30–130 mm in length. Although the closely related L. artica is endemic in Scandinavian reindeer, L. serrata is not thought to be endemic. Imported cases have been identified, however, in dogs from Romania where raw meat is routinely fed (Gjerde 2013). Although in endemic countries such as in the middle East and Eastern Europe, zoonotic infection occurs primarily through the ingestion of raw or undercooked viscera, with farmers, farm dogs, and ruminants all living in close proximity, it can also occur through ingestion of eggs in the environment or in mucoid nasal discharge. This can lead to a variety of clinical presentations including naso-pharyngitis, blocked nasal passages, visceral pain, and aberrant larval migration to the anterior chamber of the eye (Koehsler et al. 2011).

Rapid diagnosis of infected dogs is, therefore, important to limit zoonotic risk. Diagnosis can be achieved through microscopic examination of nasal secretions for eggs or endoscopy of the nose and pharynx for adult parasites. Treatment is by surgical removal of worms. Milbemycin oxime also appears to have some efficacy and ivermectin has been used to treat reindeer with L. artica.

Overall Strategies for Parasite Prevention in Travelling and Imported Pets

In addition to giving pet owners parasite prevention advice while travelling abroad, Veterinary professionals should:

• Treat imported and travelled dogs for tapeworm - Dogs should be treated for E. multilocularis with praziquantel within a month of arrival from E. multilocularis endemic countries. There is a legal requirement in Finland and Norway.
• Check pets for ticks on arrival from other countries - Checking for ticks and identifying them is vital to limit spread but also to identify possible exposure to tick-borne disease abroad.
• Be aware of relevant clinical signs in travelled and imported pets - Clinical signs should be cross checked against parasitic diseases endemic in visited countries or the country of origin.
• Screen for exotic disease - imported pets should be screened for Leishmania and tick-borne diseases so if clinical disease develops it can be detected early and so exposure to endemic vectors can be limited.

References

1.  Atkins C. The diagnosis of feline heartworm infection. J Am Anim Hosp Assoc. 1999;35:185–187.

2.  Fourie JJ, Stanneck D, Luusa HG, Beugnet F, Wijnveld M, et al. Transmission of Ehrlichia canis by Rhipicephalus sanguineus ticks feeding on dogs and on artificial membranes. Vet Parasitol. 2013;197:595–603.

3.  Geisweid K, Weber K, Sauter-Louis C, Hartmann K. Evaluation of a conjunctival swab polymerase chain reaction for the detection of Leishmanla infantum in dogs in a non-endemic area. Vet J. 2013;198:187–192.

4.  Gjerde B. Phylogenetic position of Linguatula arctica and Linguatula serrata (Pentastomida) as inferred from the nuclear 18S rRNA gene and the mitochondrial cytochrome c oxidase subunit I gene. Parasitol Res. 2013;112:3517–3525.

5.  Koehsler M, Walochnik J, Georgopoulos M, Pruente C, Boeckeler W, et al. Linguatula serrata tongue worm in human eye, Austria. Emerg Infect Dis. 2011;17:870–872.

6.  Lloyd S. Fly-borne parasitic disease: risk for the travelling pet. The Veterinary Nurse. 2011;2:295–301.

7.  Morgan E. Risks from emerging parasitic zoonoses in companion animals. Companion Animal. 2016;21:218–223.

8.  Vatne L. Heartworm infection caused by Dirofilaria immitis in a dog imported to Norway. Norsk Veterinaertidsskrift. 2014;126:615–620.