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InFocus

Screening for exotic parasites in imported pets

An understanding of what parasites are arriving in the UK, which to screen for and their clinical presentations is essential for early detection, diagnosis and treatment of exotic clinical infections

While the COVID pandemic and Brexit have seen a dramatic decrease in pets travelling abroad from the UK, the numbers of pets rescued from abroad and imported into the UK has increased. This, in combination with expanding European and global parasite distributions, increases the risk of novel parasites being introduced into the UK. Early recognition of clinical signs and diagnosis of exotic vector-borne infections is important to minimise zoonotic exposure risk, limit the potential for exotic parasites to establish in the UK and help plan for the clinical management of the imported pet.

To manage these risks, the European Scientific Counsel for Companion Animal Parasites (ESCCAP) UK & Ireland has formulated four key steps (the “four pillars”) when dealing with imported pets on arrival in the UK:

  1. 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
  2. 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 Echinococcus multilocularis is eliminated from imported pets, whatever the timing of their compulsory treatment. Tick treatment will increase the likelihood of attached ticks being killed if they are missed on examination
  3. Recognise clinical signs relevant to diseases in the countries visited or country of origin. Thorough and comprehensive clinical exam of imported pets will identify relevant clinical signs for potential exotic infections
  4. Screening for Leishmania spp. and exotic tick-borne diseases in imported dogs. Screening for parasites will lead to early diagnosis, preparing the owner for what could be a lifetime of potential treatment and any associated zoonotic risk, and will limit wider spread through effective tick control

Exotic ticks and tick-borne diseases

Recorded UK cases and risk of establishment

Pockets of the tick Dermacentor reticulatus have been long established in the UK in West Wales, Devon, Essex and London (Medlock et al., 2017). D. reticulatus is the vector for Babesia canis, a cause of potentially life-threatening anaemia in dogs, and while B. canis had been absent from the UK, these ticks present an opportunity for it to become endemic if introduced through imported dogs that may be infected or carrying infected ticks. This risk has become reality with an endemic focus of B. canis infection establishing in Harlow, Essex, with B. canis being confirmed in local Dermacentor ticks and in untravelled dogs (Phipps et al., 2016). Further untravelled cases were confirmed in Romford in 2016 and Ware in 2017 (Woodmansey, 2017).

D. reticulatus is the vector for Babesia canis, a cause of potentially life-threatening anaemia in dogs, and while B. canis had been absent from the UK, these ticks present an opportunity for it to become endemic if introduced through imported dogs that may be infected or carrying infected ticks

Rhipicephalus sanguineus ticks, capable of carrying a wide range of tick-borne diseases pathogenic to dogs including Ehrlichia canis, Anaplasma platys, Hepatozoon spp. and Babesia vogeli, are frequently being found on travelled and imported dogs. ESCCAP UK & Ireland has also seen an increased number of Ehrlichia canis cases reported in travelled dogs. Although it is unlikely that R. sanguineus would currently establish outdoor endemic populations in the UK, it can infest UK homes in a similar way to fleas (Hansford et al., 2017). This is a concern, as these ticks may also carry zoonotic pathogens such as Rickettsia conorii, the cause of Mediterranean spotted fever.

Ixodes spp. ticks, while already endemic across the UK, may be carrying tick-borne encephalitis. Its presence in imported pets or ticks presents a risk of it establishing in the UK in the endemic Ixodes spp. population. At least two endemic foci are already thought to have established in the New and Thetford forests (Holding et al., 2020).

Clinical signs and zoonotic risk

Common clinical signs associated with imported tick-borne diseases are:

FIGURE (1) Haemoglobinuria (urine dark brown in appearance) is associated with some exotic tick-borne diseases, such as infection with Babesia spp. Image courtesy of Pedro Serra and NationWide Laboratories
  • Anaemia and thrombocytopeniaBabesia spp. infection can lead to immune-mediated haemolytic anaemia in dogs with subsequent regenerative anaemias developing. These are most commonly acute and typically present with pale mucous membranes, icterus, fever and hepatosplenomegaly. Associated depression and anorexia may be present, as well as dark brown urine associated with haemoglobinuria (Figure 1). Concurrent thrombocytopenia may be present with petechiation on the gums. Imported dogs with these signs should raise suspicion of Babesia spp. infection. It is also a common sign in chronic ehrlichiosis. Travel history will often be present for acute infections but may have occurred months or years previously in chronic cases. Anaplasma platys is a cause of cyclic thrombocytopenia in dogs so this should be considered as a differential diagnosis in travelled dogs suffering from recurrent bouts of thrombocytopenia

  • Lymphadenopathy and pyrexia – Many clinical tick-borne infections present with lymphadenopathy and pyrexia including E. canis, Hepatozoon spp., A. platys and Babesia spp. It is especially important to recognise these acute signs of E. canis infection as without treatment it may progress to the chronic, often fatal form in dogs

  • Neurological signsTick-borne encephalitis and both acute and chronic ehrlichiosis may present with signs associated with meningitis and meningoencephalitis. These include ataxia, seizures, paresis, hyperaesthesia, 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 previously.

Zoonotic risk in the absence of tick vectors in households is minimal but establishment of R. sanguineus ticks in homes presents the possibility of larvae and nymphs feeding on human occupants unnoticed. This may lead to exposure to zoonotic rickettsial pathogens.

Diagnosis

Blood smear examination carries a high sensitivity and specificity for Hepatozoon canis detection and Babesia canis in clinical cases. Screening for Ehrlichia canis and Anaplasma platys, however, requires PCR or serology testing. Serology is highly sensitive and specific for detecting exposure to the parasite. Quantitative serology is useful in the case of E. canis infection where a four-fold increase in test titres taken two weeks apart is indicative of active infection. Blood PCR is also a highly specific and sensitive test for both parasites. 

Leishmania infantum

Recent recorded cases and risk of establishment

While the sand fly vector of leishmaniosis is not currently thought to be endemic in the UK, infected dogs in the UK also pose an unquantified transmission risk as horizontal transmission has been recorded in its absence (McKenna, 2019; Wright and Baker, 2019). It is currently unknown how these infections occur, but it has been speculated that transmission may occur through dog bites (Karkamo et al., 2014; Daval et al., 2016) or through mechanical fly transmission. Endemic foci can also be maintained through venereal and congenital routes, as well as via blood transfusion. If large numbers of dogs are kept together in the UK or are kept in densely canine populated areas, then the odds of transmission by these routes will increase. This is a concern as many of the Leishmania-infected dogs confirmed in the UK are in urban areas of the south of England (Shaw et al., 2009; Silvestrini et al., 2016). 

Clinical signs and zoonotic risk

Leishmaniosis 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 lymphadenopathy, cutaneous signs (eg generalised and focal alopecia, hyperkeratosis, dermal ulcers and periocular alopecia), weight loss, splenomegaly and renal signs associated with glomerulonephritis. Less commonly, polyarthritis, thrombocytopenia, ocular inclusion bodies, uveitis and neurological signs associated with spinal and CNS granulomas may be present. These signs will develop months, and in some cases years, after initial infection.

Zoonotic risk in the absence of the sand fly vector is very small but still possible, so good hand hygiene should be maintained around infected dogs exhibiting clinical signs.

Fine needle aspirate techniques can unambiguously demonstrate the presence of the amastigote stage of Leishmania in Giemsa or Diff-Quik stained smears obtained from superficial lymph nodes or bone marrow aspirates of clinically affected animals

Fine needle aspirate techniques can unambiguously demonstrate the presence of the amastigote stage of Leishmania in Giemsa or Diff-Quik stained smears obtained from superficial lymph nodes or bone marrow aspirates of clinically affected animals. However, this method can be insensitive and time-consuming. Histology performed on tissue samples carries a higher sensitivity. The main histopathological finding in the affected tissues is lymphoplasmacytic inflammatory reaction associated with macrophages infected with a large number of Leishmania amastigotes. Histopathological lesions are most commonly found in the spleen, lymph nodes, bone marrow, liver, gastrointestinal tract and skin.

Serological detection of specific anti-Leishmania antibodies can be used for routine screening. It permits the detection of a specific antibody response in dogs at around six to eight weeks of infection. Immunofluorescence antibody (IFA) and enzyme-linked immunosorbent assay (ELISA) tests are commercially available. They do not confirm or rule out active infection, but quantitative serology allows the size of response to be measured. If this climbs over time in non-endemic countries, this indicates active infection and is suggestive that clinical leishmaniosis is present or about to develop.

It is, however, important to note that these assays may give false-positive reactions with sera of dogs imported from endemic areas that have been vaccinated against Leishmania and in dogs infected by Trypanosoma cruzi, another protozoan that infects dogs in the Americas.

PCR allows detection of Leishmania DNA in an animal’s tissue. Aspirates of lymph node, bone marrow, spleen, skin biopsies and conjunctival swabs provide better diagnostic sensitivity compared to samples from blood or urine (Solano-Gallego et al., 2011). PCR assays are available at some veterinary diagnostic laboratories and can be used to confirm infection.

Dirofilaria immitis (heartworm)

Recent recorded cases and risk of establishment

Increasing numbers of cases of Dirofilaria immitis in imported dogs are being reported to ESCCAP UK & Ireland. Risk of establishment is currently low as, although mosquitoes capable of transmitting the parasite are present in the UK, the climate has been too cold to allow D. immitis to complete its life cycle; however, climate change may allow establishment in the future. Recognition of clinical signs is also important to initiate appropriate treatment in the affected patient.

Clinical signs and zoonotic risk

Coughing, tachypnoea, dyspnoea and exercise intolerance are the most common clinical signs seen in infected dogs. Acute clinical signs are associated with thromboembolism, subsequent pulmonary hypertension and caval syndrome. Worm death can also lead to thromboembolism and anaphylaxis.

There is no zoonotic risk currently from heartworm in the UK as the parasite is not present in mosquitos.

Diagnosis

Testing for uterine antigen secretions of female adult D. immitis heartworms is a highly specific diagnostic test in infected dogs and highly sensitive in cases of large worm burdens. A second test in newly imported animals six months after arrival is useful to rule out infection. The modified Knott’s test carried out by some external labs concentrates microfilariae in the blood and is a useful test in positive dogs to quantify the numbers of circulating microfilariae. Dogs with high circulating numbers are more likely to suffer anaphylaxis if treated with macrocyclic lactones. Microfilariae of D. repens will also be detected by this method. 

Parasites identified directly though clinical examination

Some worms and worm-like exotic parasites of concern may be identified through clinical examination alone. These include:

  • Thelazia callipaeda T. callipaeda is a vector-borne eye worm with hosts including 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 vector of T. callipaeda is the fruit fly Phortica variegata and has been recorded in the UK with conditions favourable for spread.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 and checking is vital in all imported cats and dogs to detect low-grade or subclinical infections to prevent vector exposure. Early diagnosis will also improve treatment outcomes
FIGURE (2) Adult worms may be present in multifocal nodules, characteristic of Dirofilaria repens infection
  • Dirofilaria repens The first cases of the skin filarial nematode Dirofilaria repens were recently confirmed in UK dogs imported from Corfu and Romania (Wright, 2017; Agapito et al., 2018). While not highly pathogenic, D. repens is a zoonosis and could be transmitted by mosquitoes endemic in the UK. D. repens infection in dogs appears to be spreading across Europe, with a corresponding increase in zoonotic cases. If infected dogs continue to enter the UK and are not treated quickly, there is the possibility for UK mosquito populations to be exposed to the parasite and for the disease to become endemic. Cases of Dirofilaria repens infection are most commonly subclinical, but clinical signs associated with infection can occur. Dermatitis is the most common clinical presentation with multifocal nodules in the skin or papular dermatitis. Less commonly, hyperkeratosis, crusting, distinct nodules, acanthosis and secondary pyoderma can occur. Adult worms may be present in these nodules (Figure 2). Signs may also develop from migration of worms to other parts of the body including conjunctivitis, anorexia, vomiting, fever, lethargy and lymphadenopathy. Ocular migration of worms into the vitreous is uncommon but does occur, and therefore D. repens should be considered as a differential if worms are visualised there and in dogs presenting with dermatitis that have travelled abroad
FIGURE (3) A number of Linguatula serrata cases have been seen in dogs imported from Eastern Europe and Turkey; pictured here is an adult L. serrata. Image courtesy of Pedro Serra and NationWide Laboratories
  • Linguatula serrata A number of nasal pentastomid L. serrata (tongue worm) cases have been seen in the UK imported from Eastern Europe and Turkey (Mitchell et al., 2016; Figure 3). Infection is acquired from the consumption of raw meat and offal in endemic countries. L. serrata is a zoonotic infection with humans acting as intermediate as well as definitive hosts. Most cases of infection in dogs and cats are subclinical. However, large burdens can lead to rhinitis and nasopharyngitis with associated chronic sneezing and/or coughing, purulent nasal discharge and epistaxis. It is vital that these signs are detected early in affected dogs to limit zoonotic exposure to owners and others in contact who may ingest infective eggs in nasal discharge or from faecal contamination. Adult worms may be expulsed from the nose during sneezing or discovered during endoscopy.

Making testing compulsory

While direct infection from Leishmania-positive dogs is unlikely, if sand flies establish in the UK through the effects of climate change, then the risk of endemic establishment and zoonotic risk would grow

Leishmania – quantitative serology, PCR
Dirofilaria immitis – antigen blood test, Knott’s test
Ehrlichia canis and Anaplasma – serology, PCR
Hepatozoon canis – blood smear, PCR
Babesia – PCR
Box (1) Summary of screening tests recommended by ESCCAP UK & Ireland for dogs imported into the UK. Quantitative serology for Leishmania and heartworm antigen testing should be repeated six months after entry into the UK

Pet travel and importation rules have focused on the prevention of novel zoonoses entering the UK and establishing here. As concerning as many exotic parasites are to canine health, they are unlikely to be included in legislation unless their economic and zoonotic impact was considerable. Leishmania meets these criteria as a significant zoonosis that impacts dog breeding and realistically could establish in the UK. While direct infection from Leishmania-positive dogs is unlikely, if sand flies establish in the UK through the effects of climate change, then the risk of endemic establishment and zoonotic risk would grow. ESCCAP UK & Ireland has recommended a list of parasite screening tests for dogs imported into the UK (Box 1).

It is also advised to test imported dogs for Brucella canis, the causative agent of brucellosis in dogs. Once dogs are infected, infection with the bacteria either persists for two to three years before elimination by the immune system, or lifelong infection establishes. The UK is currently considered to be free of Brucella canis though two clinical cases were reported in 2017 (Whatmore et al., 2017). There is concern that increasing numbers of dogs are being imported from endemic countries and economic and zoonotic impact risks are immediate for B. canis: it impacts dog breeding and realistically could establish in the UK as infection can occur though contact with bodily fluids as well as venereal and congenital routes. There have currently been no confirmed cases in the UK resulting from contact with infected dogs, but the consequences of zoonotic exposure can be significant, especially in the immunosuppressed. Serious complications in humans include septic arthritis, osteomyelitis and endocarditis. Brucellosis in dogs is now reportable and can be reported via local APHA Veterinary Investigation Centres.

Conclusion

The growing trend of importation of rescue dogs from abroad means that it is increasingly likely that veterinary professionals will encounter exotic pathogens which present a health risk to individual dogs, members of the public and UK biosecurity as a whole. Veterinary professionals have a vital role in assessing imported dogs for evidence of parasitic infection and putting effective preventative measures in place. While it is not possible to be familiar with every exotic pathogen that may present itself in practice, identifying relevant clinical signs and using screening tests (Box 1) will improve the chances of pathogen detection and management.

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