Pet ownership has become an increasingly common part of the daily life of a significant proportion of the population. As of 2022, 62% and 70% of UK and US households, respectively, are estimated to have one or more pets, with a growing recognition of the many benefits that pets can bring to the household (Veterinary Advantage, 2021; UK Pet Food, 2022). This mutually beneficial relationship can be compromised when the pet becomes a source of infection risk to their owners (Boyden, 2022a). Although this risk is generally low for most pet owners, some individuals, such as children, older people, individuals with compromised immune systems and pregnant women, are particularly vulnerable to certain zoonotic pathogens carried by pets and may develop severe illness (Stull et al, 2015). Pet welfare can also be compromised by pathogens and heavy parasite burdens.
Emerging zoonotic and arthropod-borne infections are a growing threat to human health throughout the world, including in the UK (Elsheikha et al, 2012; Elsheikha, 2013). The past 10 years have seen veterinary practices around the country report an increase in a range of exotic infections, including the blood protozoan Babesia canis (B. canis). More recently, the bacterium Brucella canis (Br. canis) has dominated the attention of the public as well as veterinary professionals and authorities (Boyden, 2022a). Additionally, tick and mosquito distributions have changed, perhaps as a result of climate change, patterns of migratory birds and movement of pets and humans (Baylis, 2017; UK Health Security Agency, 2023). This comes with accompanying threats to the UK from emerging diseases such as West Nile virus and tick-borne encephalitis, with more yet to be discovered. This is a reminder of the rapid pace at which the landscape of diseases caused by parasites and other infectious agents has changed. Increasing understanding of the pathogens that might present a greater or new risk is vital, as is providing guidance in the light of best available evidence to help protect the health of animals and humans.
The UK government is increasingly being asked to do more to address the increasing risk of exotic infections. On 13th March 2023, the British Veterinary Association President Malcolm Morley spoke at the British Veterinary Association's annual London dinner, emphasising the risks posed by newly emerging infections, highlighting Br. canis as a clear danger to dogs and public health. Dr Morley also urged the government to deliver the Kept Animals Bill. Among other measures, this bill calls for the implementation of pre-import testing for Br. canis. Early detection, leading to early intervention, can minimise the adverse impact of exotic infections on both animal and human health.
On 17th May 2023, the European Scientific Counsel for Companion Animal Parasites UK and Ireland convened a roundtable discussion at the House of Lords focused on the importance of new regulations to fight pathogens that are exotic to the UK caused by uncontrolled importation of dogs and the risks they pose to the public and animal health. The discussion brought together key stakeholders to discuss the current evidence and most feasible approaches that will likely empower the veterinary profession as they tackle emerging diseases. This article summarises the topics discussed during the meeting.
A historical account
In the early 19th century, rabies was widespread, and the quarantine of imported dogs for 6 months was essential to eradicate endemic rabies from the UK. With the increase in pet travel and 93 different countries approved for the Pet Travel Scheme, the number of pets entering the UK has risen from from 85 786 dogs pre-Pet Travel Scheme in 2011, 152 075 in 2013, 287 016 in 2017 to 307 357 dogs in 2018 (UK Parliament, 2019; Veterinary Practice, 2019). With such significant numbers of imported dogs, there is an increased risk of Leishmania, Br. canis, Echinococcus multilocularis and even potentially rabies if smuggling continues without certified paperwork being present. Early regulations to prevent the introduction of exotic infections into the UK by imported dogs date back to 1901. With the turn of the new millennium, there was a major change in the UK quarantine regulations since the 1901 Importation of Dogs Act. In February 2000, the UK adopted the Pet Travel Scheme to enable dogs, cats and ferrets with the appropriate documentation to move between the UK and certain countries. The Pet Travel Scheme was established to prevent the importation of rabies, zoonotic tick-borne infections and the introduction of the cestode E. multilocularis, which is endemic in continental Europe and can cause potentially fatal disease, known as alveolar echinococcosis, when humans ingest infective eggs shed in the faeces of infected dogs (Elsheikha et al, 2012). Although the Pet Travel Scheme has been instrumental in minimising the risk of exotic diseases, some serious infections, including leishmaniosis, heartworm (Dirofilaria immitis), babesiosis (B. canis) and ehrlichiosis (Ehrlichia canis) have been detected in dogs in the UK (Wright, 2023). There are myriad other zoonotic and veterinary pathogens not covered by the Pet Travel Scheme (which later dropped compulsory tick treatment).
Increasing disease risk with imported dogs
Along with human movement and the number of dogs being relocated from international rescue centres, there is an unquantifiable risk from potential novel pathogens and vectors arriving in the UK. In addition, climate change, rising temperature and the way land is used have a potential effect on insect, tick and wildlife reservoirs. With bird migration, an increase in the prevalence of pathogens such as Borrelia species, tick-borne encephalitis virus and B. canis is expected to continue (Hasle, 2013; Wilhelmsson et al, 2020). Heartworm (D. immitis) is now in the UK, with many veterinarians unsure how to approach its management. Unfortunately, there is a lack of surveillance, and the risk factors associated with many of these infections are poorly known. The Animal and Plant Health Agency (2024), in collaboration with the European Scientific Counsel for Companion Animal Parasites UK and Ireland, are offering a free identification service for Thelazia callipaeda, Dirofilaria repens and Linguatula serrata from veterinary practices in England and Wales, aiming to determine whether untravelled animals test positive.
What is driving up the increased risk of exotic diseases?
To date, all cases of Dirofilaria have been from imported dogs (Animal and Plant Health Agency, 2022). However, there is a long pre-patent period for Dirofilaria spp. (Webber and Hawking, 1955) and dogs may test negative when coming through quarantine or before importation. A high percentage of canine filarioid infection was found in shelter dogs from Southern Romania, with D. repens having the highest abundance (11.7%), followed by D. immitis (4.7%) and Acanthoheilonema reconditum (1.3%) (Cimpan et al, 2022). Routine surveillance and collation of practice data on Dirofilaria spp. are currently lacking in the UK.
Patient-side heartworm antigen testing is not expensive and there is an increasing desire in the veterinary profession to report cases; however, there is currently no central database to report to. Nevertheless, worms from any cases should be sent to the Animal and Plant Health Agency for logging and identification. DACTARI (Dog and Cat Travel and Risk Information) previously provided a database where cases could be inputted with minimal effort but was not widely used at the time. A similar central reporting database now would be more likely to gain traction among the veterinary profession if launched. In the meantime, the European Scientific Counsel for Companion Animal Parasites and the British Veterinary Association continue to raise awareness regarding exotic parasites in imported dogs and the importance of testing (Boyden, 2015; 2022a; 2022b).
Rhipicephalus infestations can occur in UK homes if introduced via imported pets. This is because they can complete their life cycle quickly given the right conditions and can feed on a variety of hosts (Elsheikha et al, 2012). There is a significant zoonotic risk once infestation is established. The tick surveillance scheme is invaluable in recording R. sanguineus ticks found in the UK (UK Government, 2024). However, it is voluntary, so raising awareness of the risks this tick poses and the importance of submitting ticks, if found, is essential.
European case reporting maps have shown large numbers of leishmaniosis cases in non-endemic countries because of infected imported dogs. Leishmania can be transmitted venereally and congenitally (Naucke and Lorentz, 2012), through blood transfusion (de Freitas et al, 2006) and possibly from dog bites (Naucke et al, 2016). There is also increasing evidence for direct contact transmission between dogs, such as licking and open wounds. This was the suspected route of transmission in the latest reported case of leishmaniosis in an untravelled UK dog (McKenna et al, 2019; McGrotty et al, 2023). Therefore, veterinary staff cannot be complacent about the possibility of transmission occurring in the UK in the absence of the sandfly vector.
Br. canis is of interest and is important to control. Br. canis is endemic in eastern and southern Europe, but there is potential for it to arrive in any European country. Cases can be subclinical and when importing dogs from high-endemic areas, the risk is unknown as there is no surveillance being conducted. Zoonotic risk is low but significant and there is a real need for screening before importation (Middlemiss, 2021; Boyden, 2022b). Current guidance suggests that cases can be managed without euthanasia if the owner understands the risks, the pet is neutered and proper hygiene is maintained. There is a low, but significant, zoonotic risk for veterinary professionals helping infected dogs, particularly if they are exposed to reproductive fluids. As such, there is a lot of concern in the profession about handling dogs that may be positive, and risks need to be assessed, while keeping them in perspective.
With increased dog relocation and favourable environmental conditions, the range of parasites and vectors of European dogs are expanding and driving up this trend. Education, surveillance and legislation all have a role in reducing the spread and with adequate enforcement, veterinary staff can be encouraged to engage with charities to do the tests necessary for these changes to be effective.
The need for effective management of importation of dogs into the UK
A change to the rules to the Pet Travel Scheme in 2012 paved the way to the current situation. Since 2012, there has been no requirement for a rabies (serology) blood test. This has resulted in the preparation time before travel reducing from 7 months to 3 weeks after vaccination.
Puppies younger than 15 weeks are now entering the UK from central and eastern Europe on an ongoing basis. There was a 61% increase in the number of dogs entering the UK via the Pet Travel Scheme in the first year after harmonisation of controls with the rest of the European Union (Defra, 2011). Between 2011 and 2013, the number of dogs imported from Lithuania rose by 780%, while imports from Hungary increased by 663% during the same period (Dogs Trust, 2014). The concern is that the Pet Travel Scheme is being used as a cover to illegally import puppies for commercial gain. Puppies are entering without the correct treatments and with falsified data on the pet passports. Poor enforcement, insufficient penalties and checks mean heavily pregnant dogs are also being imported with their puppies, which are then sold as UK-bred.
There is ongoing concern around the risk of importation of non-endemic disease, particularly with the rescue of adult dogs for rehoming. Diseases of concern include brucellosis, leishmaniosis, alveolar echinococcosis, babesiosis and heartworm.
There is a problem with the required ‘document and identity’ checks on arrival not being fit for purpose as they do not require a visual check of the animal. A toy dog successfully made 3 out of 4 trips with the microchip located inside the dog carrier. How can underage puppies, dogs with mutilations (eg cropped ears) or pregnant dogs be identified without looking at the animal?
The Kept Animals Bill, which has now been dropped, would have seen a reduction in the number of pets allowed to travel with an owner from five to three. It would also have implemented an increase to the minimum age of entry, a ban on the importation of animals with mutilations and a reduction in the stage of pregnancy at which an animal can travel. The ongoing challenge or problems from a lack of visual checks and the low penalties imposed would not have been addressed with the legislation. Furthermore, illegal importers can claim their animals back to go on to sell them for a profit.
DACTARI was a system set up by Defra to record the prevalence of non-endemic diseases following the introduction of the Pet Travel Scheme. While the principle was good, it relied on veterinarians reporting rather than laboratory-supplied data. The Small Animal Veterinary Surveillance Network has been more successful at mining veterinary practice records, but a more comprehensive central case recording system is required to fully understand the prevalence of these diseases in the UK.
Dogs Trust began screening for Br. canis in May 2021. To date, there have been 11 seropositive dogs out of 550 tested. Those 11 positive dogs include 3 pregnant females, 1 Puppy Pilot Scheme, 1 handover, 1 freedom foster dog and 5 pre-intake handovers. Pre-intake positives were reported to the Animal and Plant Health Agency as required, and referred to the owner's veterinarian, but they were lost to follow up. Concern was raised that the owners could change veterinarian and not disclose the Br. canis status. A searchable microchip database could be considered for positive cases. There is still so much that is unknown about Br. canis, which is a growing public health concern.
There is concern regarding the lack of control of imported dogs (Loeb and Gray, 2022). With no check of commercial imports at the ports, there is scope for the system to be abused by carrying more dogs than the number certified on the paperwork.
From a disease perspective, the importation of a puppy is less of a potential problem than an adult dog. However, there is a concern that the exception to that rule is Br. canis. Puppies are being born to imported pregnant bitches, with the risk of vertical transmission of disease to the puppies being high (Makloski, 2011; The Kennel Club, 2024). These pups are then sold as UK-bred and may go on to breed, so tracing these cases can be problematic.
The rescue charity stance on dog importation
Paws2Rescue is not typical of many other importers as they do a lot to help improve conditions for animals to stay in their own countries, rather than simply importing. They have four clinics, sanctuaries, vet clinics where they have neutered over 15 000 animals. The question is, why do people want to import? Some members of the public want to be seen to save a life and there's an associated emotional pull with the plight of many of these animals. The life of many Romanian dogs means life on a chain, malnourished, abused and street dogs often end up in kill shelters. These dogs deserve the chance of a happy family life too. UK charities often will not rehome dogs to people who have young families, live in a flat or are elderly.
The key risk to the charity when importing dogs is the possibility of bringing disease into the UK. Other key risks include damage to their reputation, as a rescue or dog having behavioural issues could result in adopters returning dogs to the charity.
Paws2Rescue carry out detailed assessment, testing, vaccination and disease prevention protocols for of all of their dogs that are imported into the UK. The only current legal requirement to import a dog are rabies vaccination and cestode treatment. However, the charity performs haematology and serology testing, vaccination, parasitic disease prophylaxis as well as general health monitoring while they are checked and held in Romania for 30 days. Paws2Rescue have a critical checkpoint procedure for comprehensive vetting, which includes microchipping, monitoring and maintaining constant contact with involved parties. Testing for brucellosis has been conducted by the charity for the last 3 years, with blood tests being sent to an approved laboratory in Germany.
The existing rules regarding testing and treatment of imported dogs
There may be confusion as to why strict rules exist for rabies control but not for Br. canis in imported dogs. Br. canis is a reportable disease, but there is a need for legislation to make pre-import testing compulsory. There is a need to rely on tests being done properly with sample traceability. The optimum time for antibody detection is from 3 months post infection which is why post-import testing is also important. There is a real risk unless movement is stopped – new legislation needs amending and current policy is not fit for purpose. It was suggested that the person importing the animals should pay for policy change. For example, a dog can be taken on Le Shuttle for £22; a proportion of that could potentially fund testing and enforcement of any policy changes alongside the current paperwork it includes. A problem is that falsified paperwork makes illegal imports easier than trafficking drugs or firearms. There is fraudulent testing happening and the pre-testing results are not always reliable. An approved testing site and lab to officialise the testing is required. A requirement to test would be more beneficial than a veterinary recommendation to test.
People who want to import dogs illegally will always find a way to get around the rules; the rules do not change the decision-making process of people who want to do something. Thus, veterinary staff need to be accountable and educate others. It needs to become more socially unacceptable to import dogs, other than from registered charities that are supporting pet welfare in the country of origin. The question then becomes, how do you do that? One approach would be to give adopting from irresponsible importers the same antisocial stigma as drink driving or smoking. Dogs that test positive for brucellosis should not be allowed to enter the UK and must be isolated and neutered. Although a Hazmat suit is not required to treat dogs with brucellosis, appropriate personal protective equipment is important.
Is euthanasia the right thing to do for dogs testing positive in the UK and what are the risks when operating on them?
There is no general answer, but immune compromised or pregnant staff may want to have no contact. The risk from subclinical dogs is low, but is likely to be higher for reproductive surgery. If pre-import testing is performed, at least one test is conducted before they are imported.
Human health must be protected over animal health, but what can be done with these animals if they are not euthanised? There is very little information about how to safely treat, and without a strong policy, the public attitude will decline. Which treatments are most effective when it comes to bacteraemia and, when treating with antimicrobials, knowing when bacteraemia has cleared is a challenge. These are valid points, and a balance needs to be struck. The European Scientific Counsel for Companion Animal Parasites UK and Ireland has been proactive in promoting the need for pre-importation testing, because it is better to counter the problem than ignoring it. Dogs testing positive should be identified and stopped from entering the country.
Conclusions
Protecting pets and their owners in the UK requires veterinarians to have access to appropriate diagnostics and innovative solutions to control and restrict the spread of pet pathogens and zoonotic diseases. The advent of pet-side diagnostic tests, parasite control risk assessment tools and broad-spectrum parasiticides are some of the most important industrial developments over the past decade. Significant improvements in the surveillance, detection and management of parasitic diseases of companion animals have been made in the last 10 years. However, veterinarians cannot win the fight against emerging infections without institutional support. More awareness and firmer regulations are needed to improve the ability of veterinarians to prevent, detect and respond to the risks of the emerging diseases that could negatively impact human health and the health and welfare of pet animals in the UK. A change in regulation and better use of educational and behavioural approaches could benefit pets, veterinary professionals and the public.