This study represents the first reported dataset of exotic parasites in a group of dogs imported into the UK rather than individual or small groups of case reports. Such datasets are vital in establishing the prevalence of exotic parasites entering the UK in imported dogs, their geographic origin distribution and to facilitate investigation of risk factors for their presence.
Overall, 24% of the dogs tested positive for an infection listed in Table 4. Five of the six infections detected are currently not thought to be endemic in the UK and all of the detected infections are potentially pathogenic in dogs.
Importation of Br.canis is of particular concern, given its zoonotic potential, economic impact and risk of establishment in the UK. As a result, the RSPCA sought guidance from APHA on Brucella screening. BR.canis (canine brucellosis) is an important cause of abortions and infertility in dogs and has been recognised as the cause of significant economic loss in infected kennels. Canine brucellosis is mainly caused by Br.canis, and sporadically by Brucella melitensis, Brucella suis, and Brucella abortus. Brucella canis infected dogs can transmit the disease even after the bacteremia has ceased and without presenting clinical symptoms of the disease and it is also considered to be a zoonosis. The UK is currently considered to be free of Br.canis though two clinical cases were reported in 2017 .
APHA advised that Br.canis screening would be highly prudent before considering rehoming imported dogs to members of the public. An alert was issued to the veterinary profession by the UK Chief Veterinary Officer following the APHA's involvement in an investigation of cases in 2020. The risk of infection with other Brucella species was also discussed. Concerns were raised over the possibility that Brucella canis could become endemic in the UK.
It was felt that dogs may be at high risk of acquiring infection with B. abortus, B. melitensis or B. suis if they live on farms where these pathogens are present, particularly if they come in to contact with abortion material or if they are used for hunting feral pigs and wild boar. In the vast majority of cases, antibodies to B. abortus, B. melitensis or B. suis will not be detected by the Br.canis serological assay (and vice versa). In the absence of history of this nature, it was felt that screening for species of Brucella, other than Br.canis, was not necessary in imported dogs. Therefore, dogs in this cohort were screened for Br.canis only.
Any dogs that had a positive antibody tire on initial screening had a repeat sample sent to the APHA lab at Weybridge approximately 5 weeks after the first sample was analysed. From the 4 samples submitted, two of these dogs tested negative while two tested positive on APHA’s SAT for Br.canis antibody.APHA informed the RSPCA that these dogs should be euthanased on infection control grounds. The RSPCA had been unable to identify an owner of one of the dogs while informed consent for euthanasia was gained for the other. If there had been issues with gaining consent for euthanasia, APHA would have issued a destruction order. Both dogs were sedated and examined prior to euthanasia and were found to be clinically normal other than minor dental trauma in one, one with a mild cough and one mildly underweight with a puncture wound on the pinna (registered as skin disease in the table). Hence it is important to note that clinical signs attributable to Brucella canis infection may not be apparent on physical examination of imported dogs.
Leishmania infantum was identified in 14 positive dogs (10.5%), the most diagnosed parasite with all but two cases being diagnosed in dogs whose microchip originated in Romania. While this does not mean that these infections all originated in Romania, L.infantum is now considered to be at least seasonally endemic in the country . It is important therefore that UK vets consider the possibility of L.infantum infection in imported dogs. Dogs on presentation may be subclinical as clinical signs take months and sometimes years after infection to manifest. Early recognition of infection by diagnostic screening of imported dogs would allow monitoring of kidney function and antibody titres so treatment can be initiated at an early clinical stage. This has been demonstrated to improve prognostic outcomes, particularly if significant proteinuria and renal failure can be avoided . Identification of infected dogs is also important to prevent transmission to other UK dogs. Although the sand fly vector is currently not currently thought to be present in the UK, non-vectoral transmission via venereal and transplacental transmission, blood transfusion and possibly dog bites can also occur. Two cases of unexplained horizontal transmission have already occurred in untraveled UK dogs [14, 15]. Early identification of positive dogs means that measures to limit spread can be implemented such as excluding infected dogs from breeding and from being blood donors.
Hepatazoon canis was identified in 10 dogs (9.6%), all of which had a Romanian microchip. This parasite is not considered endemic in Romania, so this finding supports the suggestion that Romania may be acting as a hub for dogs being relocated from other countries. It is important that UK vets, however, are aware of its possible presence in dogs imported from Romania and consider it as a differential if these dogs present with fever or lymphadenopathy. Imported dogs can be screened for the parasite through blood smears with 0.5-5% of neutrophils commonly infected, although this figure can be as high as 100% .
Ehrlichia canis, which is endemic in Romania was only present in 2 (1.5%) of dogs tested. Nonetheless this pathogen is highly pathogenic and often fatal if chronic ehrlichiosis develops. This can occur months or years after initial infection and can be avoided if acute infections are treated adequately. Screening of imported dogs is therefore important, both to treat dogs suffering from acute ehrlichiosis and to monitor chronically infected dogs so that chronic disease can be treated early to maximise positive outcomes. Both H.canis and E.canis have been recorded in imported dogs [22, 23] but are not thought to be currently endemic. The tick Rhipicephalus sanguineus which is required for transmission is not endemic in the UK outside of individual household infestations. It is however, important that imported dogs are checked and treated for ticks as R.sanguineus can establish in UK homes and then go on to transmit these pathogens.
Dirofilaria immitis was identified in 5 (4.1%) of dogs. Increasing numbers of imported dogs infected with D.immitis are being reported to the European Scientific Counsel for Companion Animal Parasites (ESCCAP) UK & Ireland, with many of them coming from Eastern Europe. Dirofilaria immitis has spread through Eastern Europe with Romania now having been confirmed as endemic for the parasite . The mosquito vectors required for transmission are present throughout Europe but it is currently not warm enough for D.immitis to complete its life cycle in the UK . It is vital to screen imported pets for the parasite however, as adult worms can cause heart and respiratory disease as well as sudden death through thromboembolism. Identification of the parasite allows effective treatment protocols to be put in place while minimising the risk of thromboembolism through strict rest of the patient. Dogs with undiagnosed heartworm infection can also suffer anaphylaxis as a result of routine use of macrocyclic lactones for other parasite prevention .
Three (2.3%) of the dogs tested were positive for B.canis. Babesia.canis is transmitted by the tick Dermacentor reticulatus and is endemic throughout mainland Europe. Pockets of D.reticulatus have been long established in West Wales, Devon, and the South East of England and while B.canis had been absent from the UK, these ticks present an opportunity for it to become endemic if introduced through dogs entering the UK from abroad. An endemic focus of Babesia canis infection established in Harlow, Essex in 2015, with B.canis confirmed in local Dermacentor ticks and in untravelled dogs . Further untravelled cases were confirmed in Romford in 2016 and Ware in 2017 . This demonstrates the importance of vigilance for B.canis in imported dogs to prevent exposure of local populations of D.reticulatus ticks, but also so infected dogs can be monitored for the development of immune mediated haemolytic anaemia and thrombocytopenia . Treatment initiated early for clinical babesiosis improves prognostic outcomes .
Only four dogs were found to have co-infections. Other studies have found E.canis infection to be a risk factor for L.infantum infection. This is not supported by this study. It is possible that those dogs infected with L.infantum and those infected with H.canis were exposed in different regions/countries and opportunity for exposure to both pathogens did not occur. This is not possible to confirm however, without an accurate travel history for the tested dogs.
There was no association found between the pathogens detected and presenting clinical signs in this group for dogs. This is concerning as veterinary professionals rely in part on recognition of relevant clinical signs to alert them to potential exotic infections in imported pets. The lack of a relationship in this study emphasises the importance of screening for exotic pathogens if these are to be detected. The exception was L.infantum where A high proportion of L.infantum positive dogs had ocular and dermatological signs. If dogs with dermatological and/or ocular signs had both been used collectively as criteria for testing alongside poor body condition score and pyrexia, then all but one of the Leishmania positive dogs would have been identified.
Large numbers of dogs in the group had ocular (22.8%) and dermatological (19.7%) signs. This is of concern as D.repens and T.callipaeda may have been responsible for some of these cases and gone undetected. Dogs having spent time in countries endemic for these parasites with ocular and/or dermatological signs should be thoroughly examined for these parasites and in the case of D.repens, a modified knotts test performed.
Of the 129 dogs tested for rabies serology 94 (72.8%) had a titre less than 0.5 IU/ml, with 24 (18.6%) having a titre less than 0.1IU/ml. Whilst it cannot be assumed that a low titre equates to no protection against rabies, the proportion of dogs with low titres is of concern. Previous studies have shown that there are differences between vaccines  with an overall failure rate of 4.12% (14,035 samples). With this sample showing that 72.8% of the imported dogs did not have a protective titre raised the question whether the dogs had been vaccinated at all. Titres less than 0.1 IU/ml are considered negative for the fluorescent antibody virus neutralisation assay. With the prevalence of disease identified it is also important to question whether the poor response could be associated with underlying disease.
Regarding the 2 dogs diagnosed with canine distemper virus (CDV) the most common route of transmission of CDV is direct contact via the oronasal secretions of infected animals . Indirect transmission plays only a minor role as the virus is quickly inactivated. The concern with this is the similarity in some of the symptoms to those of other neurological conditions in imported dogs particularly rabies. Recent studies  emphasise the risk of introducing vector borne disease and diseases not considered endemic into naïve countries by non-vaccinated rescue dog importations.
The microchips of the majority of dogs (94 of 140) originated in Romania and these dogs accounted for all but two cases of infection recorded. Romania is recognised as a common source of imported rescue dogs, driven in part by the large number of street dogs present there and Government policy of euthanising street dogs that cannot be rapidly rehomed. The large numbers of rescued imported Romanian dogs entering the UK and being presented in veterinary practices means that UK veterinary professionals need to be aware of parasites likely to be present in these dogs, possible presenting clinical signs, the need for diagnostic tests and medical management where appropriate. Although microchips can be traced to an individual country, it does not guarantee the microchipped dogs originated there and may have been imported into a country prior to microchipping. This means pathogens not thought to be endemic in the country where the microchip originated may still be present.