Vector-borne diseases (VBDs) of pets are illnesses caused by viruses, bacteria, protozoa and helminths transmitted through the action of arthropod vectors such as ticks, fleas, mosquitoes and sand flies. Pathogens that can be transmitted by the bites of arthropods include, for example, tick-borne bacteria (Ehrlichia spp., Anaplasma spp. and Rickettsia spp.), protozoa (Babesia spp., Cytauxzoon spp. and Hepatozoon spp.) and viruses (various encephalitis viruses); flea-borne bacteria (Bartonella spp.); sand fly-transmitted protozoa (Leishmania infantum); and mosquito-borne viruses (e.g. West Nile virus) and nematodes (Dirofilaria spp.). Many can cause severe or even fatal clinical disease in companion animals, while others have an important zoonotic potential. Factors such as stray animals, increased movements, import and travels of pets, climate change and intensification of the international trade of goods are modifying the epizootiology of VBDs in Europe. While the Mediterranean basin is a major epidemiologic hub for VBDs, the realistic risk of establishment of VBDs in other regions traditionally considered free of these infections should not be overlooked.
The real threat posed by VBDs can be underestimated in everyday small animal clinical veterinary practice, due to limited knowledge of veterinary practitioners and to possibly overlapping clinical features with other diseases that occur more commonly in certain epizootiological settings.
In the UK, for some years the pet travel scheme (PETS) has allowed movements of companion animals to and from EU countries with no quarantine, provided that pet owners meet specific requirements to avoid importation of non-endemic zoonotic pathogens (https://www.gov.uk/take-pet-abroad). The scheme is EU-based, and while non EU countries are included, whether they are ‘listed’ or ‘unlisted’ is decided on a case by case basis. Thus, the effect of ‘Brexit’ on the PETS at the end of 2020 will need to be clearly evaluated.
Up to the present time, this scheme has simplified pet movements from and to the UK, while keeping at the same time a strong guard against specific significant diseases. Given the high popularity of vacation spots such as the Mediterranean Basin or France, the scheme is designed with consideration of diseases particularly present in those regions. This means that some epizootiological risks due to travels from and to other regions (e.g. Eastern Europe) may be underestimated, as some parasites are not considered under this scheme (Wright and Elsheikha, 2017). Additionally, even when strictly applied, the scheme may miss some VBDs of clinical relevance regardless of the geographic areas of interest.
This article briefly reviews the most important VBDs of dogs and cats that are endemic in Europe, in the perspective of risks of spreading and/or importation in the UK, along with the key principles of epizootiological surveillance and control.
Ticks and tick-borne diseases
Brown dog tick Rhipicephalus sanguineus
According to the European Centre for Disease Prevention and Control (ECDC) (https://www.ecdc.europa.eu/en/home), the brown dog tick Rhipicephalus sanguineus, which is one of the most important tick species worldwide, is not endemic in the UK. This tick is an efficient vector of various pathogens of companion animals, such as Ehrlichia canis, Anaplasma platys, Rickettsia conorii, Babesia vogeli and Hepatozoon canis.
The brown dog tick is moving northwards in Europe and, in addition to Eastern Europe and Mediterranean countries (Figure 1), it is present in Switzerland and in some areas of Germany. The possible risk of introduction of R. sanguineus in the UK was confirmed by the records of a house infestation in England caused by a dog that had been imported from Spain (Hansford et al, 2015). In that particular case it was suggested that tick nymphs had survived the treatment the dog received before entering the UK, then developed to adulthood, continuing their biological cycle. Another dog imported in the UK from a rescue centre in Greece was found heavily infested by larvae despite having supposedly been treated with an effective formulation (Wright et al, 2018b). These cases are of great importance if one considers that some pathogens may be transmitted trans-stadially (from one tick stage to the other), or transovarially (from an adult female to the eggs, and thereby to the larvae).
Diseases transmitted by R. sanguineus are endemic in Southern Europe, for example in Spain, Italy and Greece (Diakou et al, 2017; 2019; Estrada-Peña et al, 2017; Traversa et al, 2017), but autochthonous cases in central and eastern Europe can no longer be considered to be a surprise. Altogether, this scenario indicates that VBDs transmitted by the brown dog tick have the potential to enter the UK, either with adopted dogs or with animals who return home after travelling into continental Europe, with a high risk of local establishment. As key examples, cases of unexpected B. vogeli and E. canis infections in the UK in untravelled dogs have been known since 2006 and 2013 respectively (Holm et al, 2006; Wilson et al, 2013).
Ornate tick Dermacentor reticulatus
Another tick species that requires attention is Dermacentor reticulatus, the ornate tick, that, according to the maps published by ECDC and recent descriptions (Smith et al, 2012), is present in Wales and limited areas of Southern England.
This tick is a proven vector of Babesia canis, a haemoprotozoan that causes a severe haemolytic disease in dogs. The endemic cases of B. canis recently recorded in South England and Wales in dogs with no history of travel (Phipps et al, 2016; de Marco et al, 2017) provid a realistic alarm bell ringing for potentially nationwide spreading of this pathogen.
Until a few years ago B. canis was an exotic pathogen to the UK, known as a disease in imported dogs only (Shaw et al, 2003). How this pathogen first infected tick populations in the Southern UK remains unknown, but the key point is that its distribution in the UK is likely to increase in the near future, because B. canis and its vector are endemic across mainland Europe and may (re-)enter the UK with travelling dogs.
Ixodes spp.
Ticks belonging to the Ixodes genus, especially Ixodes ricinus, are common in habitats with deciduous woodlands, heaths and forests, especially in humid areas. In the UK, where the current climate allows questing and feeding of Ixodes ticks all year round, I. ricinus is highly prevalent (Wright et al, 2018a), while it is scarcely present in Mediterranean regions where summers are dry. This tick is an efficient vector of Anaplasma phagocytophilum, Borrelia burgdorferi and tick-borne encephalitis virus (TBEV). While the presence of A. phagocytophilum and B. burgdorferi in UK has been known, it is only recently that TBEV has been recorded in the UK (Holding et al, 2020). Although the origin of this virus in the UK is unknown, imported rescue dogs of unknown health status have been hypothesised as the potential source. This is of relevance as Ixodes spp. ticks are endemic across all of northern Europe, where TBE is also endemic.
Babesia spp.
It is interesting to note that a recent case of Babesia microti-like (known also as Babesia vulpes or Theileria annae) infection has been described in a dog that had never travelled outside UK (MacLeod and Wright, 2019).
This record is also of biological relevance, because the vector(s) is/are still undefined but various Ixodes spp., along with D. reticulatus and R. sanguineus, are suspected to have a role in its transmission (Baneth et al, 2019). Also, it seems that dog-to-dog transmissions play an important role in the epizootiology of this infection (Barash et al, 2019). This means that, once some vector-borne pathogens enter into an area previously free of the parasite, the presence of efficient vectors is not a completely necessary requirement for their spread. This could be true also for L. infantum (see below).
Ticks and cats
Ticks and tick-borne diseases are generally considered to be health issues for dogs rather than for cats. Nonetheless, the aforementioned tick species may feed on cats as well, and some pathogens that they transmit to dogs (e.g. A. phagocytophilum) also may cause clinical signs in cats. Additionally, a recent study has proved that in the UK I. ricinus may infest cats earlier in the year (i.e. by March) than dogs (Wright et al, 2018a). There are data showing that cats are prone to be parasitised by ticks infected with pathogens such as Babesia spp. and Borrelia spp. throughout the UK, especially when living in green spaces providing a suitable habitat for Ixodes spp. (Shaw et al, 2005; Davies et al, 2017).
The risk of introduction and/or spreading of other neglected pathogens of cats should not also be excluded. This could be the case for Cytauxzoon spp. and Hepatozoon spp. protozoa that, under certain epizootiological conditions, may find in wildlife their natural reservoirs, and in tick species feeding on both domestic and wild animals their vectors. For instance, this could be a realistic threat in the UK, considering the existence of populations of the Scottish wildcat (Felis silvestris grampia), as well as a large feral cat (Felis catus) population. It is important to note that Ixodes spp. ticks feeding on cats in UK have been recently found to be infected by A. phagocytophilum and by Hepatozoon spp. (Duplan et al, 2018). As the role of tick species as vectors of Cytauxzoon spp. and Hepatozoon spp. affecting felids in Europe is not completely understood, vigilance should be kept high, as potentially ticks prevalent in the UK may have the potential to transmit these parasites to cats.
In general, feral cats in the UK should be considered important reservoirs for tick-borne infections.
Endemic fleas
Fleas (Ctenocephalides felis and Ctenocephalides canis) are cosmopolitan ectoparasites, feeding on dogs and cats, which act as competent vectors for a high number of pathogens (Traversa, 2013). A recent study has shown that flea infestation is a nationwide problem in dogs and cats in the UK, with a relatively high level of infection of fleas by more than one species of Bartonella spp. bacteria, especially in south-central regions, followed by Mycoplasma spp. and Dipylidium caninum (Abdullah et al, 2019).
Fleas remain a constant problem for pet owners and their homes, thus veterinary surgeons should be vigilant not only for well-known flea species and transmitted pathogens (e.g. Bartonella spp.) but also for somewhat overlooked diseases (e.g. mycoplasmosis). This is of importance if one considers that a recent study proved that more than a hundred different wild animal species may harbour cat fleas (Clark et al, 2018). This indicates the huge potential for bridging infections where companion animals and wildlife live in sympatry, as well as possible sharing of transmitted pathogens at the wild-domestic animal interface.
Flying insects
A number of well-known (and less-known) pathogens may be transmitted by various flying insects. The past few years have seen the first cases of some insect-transmitted parasites in the UK, where they were almost unknown or at least unexpected.
Leishmania infantum
Canine leishmaniosis, caused by L. infantum (Figure 2), is a major veterinary threat, especially in the Mediterranean Basin. Its importance in the UK is minor, given the absence of vector sand flies such as Phlebotomus ariasi and Phlebotomus perniciosus (McKenna et al, 2019). Nonetheless, in the UK, dogs with a history of travel to, or importation from, regions that are endemic for L. infantum may be diagnosed with leishmaniosis (Slappendel and Teske, 1999; McKenna et al, 2019). These dogs may represent a source of infection for other animals living nearby, as recently shown by a clinical case of leishmaniosis in a dog that had never travelled outside UK but had lived with a leishmaniotic dog imported from Spain (McKenna et al, 2019). This is of great epizootiological impact, as it was claimed to be the first reported case of canine leishmaniosis in the UK in a dog without a foreign travel history, although previous non-travelled dog-to-dog transmission has been suggested (McKenna et al, 2019). Regardless of when the first case ever of canine leishmaniosis in a non-travelling animal in the UK occurred, it is important to acknowledge that there is a risk of dogs living in the UK becoming infected with L. infantum. Apart from the most important source of infection (i.e. the bite of an infected sand fly), dog-to-dog direct transmission is known to be possible via routes that include blood transfusions; animal bites; and both venereal and vertical transmission. As a key example, the existence and maintenance of autochthonous cases of canine leishmaniosis in the USA, where sand flies are absent, is well known (Toepp et al, 2017).
Last, but not least, it should not be forgotten that L. infantum may also cause illness in cats.
Thelazia callipaeda
Another emblematic example is given by the so-called ‘oriental eyeworm’ Thelazia callipaeda, a nematode transmitted by means of secretophagous drosophilid fruit flies. This nematode may infect the eyes and conjunctival sac of dogs, cats, wild animals and people. In the past 2 decades it has spread in many countries of Europe (e.g. Italy, France, Germany, Switzerland, Spain, Portugal, and eastern European countries), while no cases of ocular thelaziosis were recorded in the UK until a few years ago. In 2016 a dog imported from Romania was diagnosed with T. callipaeda, and in 2017 there were three recorded imported cases (Graham-Brown et al, 2016; 2017).
Importantly, the major vector of T. callipaeda, the fruit fly Phortica variegata, is present in parts of the UK (e.g. in Gloucestershire, Kent and Berkshire), while recent prediction models have indicated suitable conditions in various other UK regions, supporting a realistic threat for a further spread of T. callipaeda if the nematode arrives more frequently with pet movements (Morgan, 2016; Graham-Brown et al, 2017; Palfreyman et al, 2018). Again, T. callipaeda also may infect cats (Figure 3), in which the disease may be somewhat more difficult to diagnose than in dogs.
Dirofilaria spp.
The UK has historically been free of mosquito-borne infections caused by the canine heartworm Dirofilaria immitis and by the less pathogenic (but more zoonotic) subcutaneous worm Dirofilaria repens. This is the result of the cold climate of north-central Europe that negatively impacts the Dirofilaria life cycle, despite the presence of mosquitoes capable of transmitting these parasites in the UK.
Dirofilaria spp. remain endemic mainly in Southern Europe, although both D. immitis and D. repens have spread northward and in eastern European countries in the past years, as a result of climate changes and animal movements (Genchi et al, 2011; Capelli et al, 2018). Therefore, pets visiting or travelling to these regions may become infected and bring back the parasite when they come back home to the UK, and there is also the risk of introducing Dirofilaria spp. with rescued or adopted animals. Thus, there is a potential threat that epizootiological drivers may facilitate the establishment of dirofilarial foci at least in more suitable southern regions of UK in the near future.
Southern parts of the UK are already warm enough to allow the development of Dirofilaria spp. L1 larvae to infectious L3s in the mosquitoes at least for a short period in the summer. This could be even more true for D. repens, which is able to complete its biological cycle at lower temperatures than are required by D. immitis.
Important factors for vector/pathogen importation
Travelling animals are the major source of various VBDs, although infected vectors may enter areas that were previously free of the pathogen (pathogen-free) mechanically on goods (e.g. vehicles, clothes).
At present, there is a substantial risk of importation of VBDs from mainland Europe to UK, considering the number of companion animals travelling into and out of the country; their arrival from rescue charities; frequent adoptions; and the possibility of illegal importations. In everyday scenarios, animals can bring with them bacteria, nematodes or protozoa when returning home after a holiday, or when they are rescued or adopted from an endemic region. Also, animals may bring various ectoparasites that pose a risk when they are infected by pathogens that infect pets and people in free regions.
As an example, this could be the case of the importation of ‘exotic’ ticks (e.g. R. sanguineus) that could be infected by pathogens causing unexpected diseases. Under suitable conditions, these ticks may continue their biological cycle. Animals and people may pick up arthropods that may be carrying pathogens or, alternatively, imported ticks may acquire pathogens from wild or domestic reservoirs and facilitate their spread. In the presence of suitable conditions, the arrival of exotic vectors and/or transmitted pathogens may lead to the spread and establishment of new foci in territories that were previously free. For instance, cats and dogs with eyeworms may act as source of infection for local drosophilids, or dogs with Dirofilaria spp. infection may infect autochthonous mosquitoes that, in some climatic scenarios, may establish a local biological cycle. As for L. infantum, the possibility of animal-to-animal infections shows that if a pathogen enters a previously pathogen-free region, the presence of their vectors is not essential for disease transmission.
Extrinsic factors may also promote the dissemination of imported vectors or diseases in given areas. Spreading of autochthonous (Ixodes spp.) or imported (R. sanguineus) ticks may be favoured by current global warming, which has the potential to enable these arthropods to be active for longer than in the past or to reproduce in regions that were previously unhospitable, thereby increasing the risk of disease transmission. At the same time, climate changes may allow the biological cycle (that is strictly temperature-dependent) of Dirofilaria spp. in mosquito intermediate hosts. Urbanisation and loss of habitat may bring wild animals to environments closer to human and pet activities, thus favouring bridging infections (e.g. of Hepatozoon spp. and Cytauxzoon spp.) between wild and domestic animals. Also, wild animals could serve as reservoirs of some VBDs of companion animals (e.g. leishmaniosis, thelaziosis) or harbour ectoparasites that may infect also dogs and cats (e.g. host-generalist fleas, Ixodes spp. ticks).
Role of veterinary professionals
Veterinary surgeons and veterinary nurses in the UK have a crucial role in vigilance, surveillance and control of exotic and unexpected diseases of companion animals. At the same time, it is of key importance to appropriately educate pet owners regarding the risks of importing and spreading diseases when they take dogs and cats abroad, or when they wish to import them. Pet owners need to be aware that preventative measures are crucial not only for the single animal that they take care of, but also for the health and welfare of pet populations living in the same areas and, in the case of zoonoses (e.g. TBE, rickettsiosis, leishmaniosis), of people. Therefore, appropriate measures should be taken.
Awareness of veterinary and medical risks needs to be raised among the general public, pet owners and people who want to adopt a pet from abroad. This should be conducted by veterinary professionals using a scientific rationale and without fear-mongering. Preventative measures are crucial for all dogs and cats travelling outside the UK to endemic countries, to avoid their returning home with undesired souvenirs. Depending on the epizootiological scenario of each visited country, these preventative measures may include the use of repellents for ticks and/or sand flies, or macrocyclic lactones for chemopropylaxis against dirofilarioses or thelaziosis. Visits to a veterinary surgeon on their return is also of importance, for example to identify ectoparasites on the animal or to perform diagnostic tests. Routine ocular examinations are advisable in those animals coming from areas endemic for T. callipaeda, and periodic serological tests for leishmaniosis, tick-borne diseases and dirofilariosis could be useful for those animals that come back from endemic regions. At the same time, rescued and adopted animals should be appropriately treated (e.g. against ticks or fleas) and subjected to diagnostic procedures, to identify infections that could be missed when subclinical. Local surveillance and vigilance should also be constant. For example, owners should frequently check their pets for ticks, as under certain circumstances acaricidal products may have less than 100% efficacy, and ticks that could be found on a pet when abroad or after travel should be appropriately identified, making veterinary surgeons aware of what pathogens the animals might have been exposed to.
Last but not least, the risk of importation of vectors and diseases from outside Europe should not be underestimated, for the UK but also for mainland Europe. For instance, attention should remain high for ticks arriving from Africa or the Americas that could bring severe and life-threatening zoonoses (e.g. Rocky Mountain spotted fever caused by Rickettsia rickettsii) or rare and/or exotic illnesses (e.g. haemoprotozan infections caused by Rangelia vitalii or Babesia rossi). As examples, in 2015 a dog imported from the USA was found infested by Dermacentor variabilis, one of the vectors of R. rickettsii, while in 2016 a dog from South Africa was found to harbour Haemaphysalis elliptica, a vector of the life-threatening B. rossi (Abdullah et al, 2016; Hansford et al, 2018).
Conclusions
Many drivers (e.g. increases in pet ownership; travels; rescued and adopted animals; globalisation and trade of goods; and global warming) have the potential to influence the endemicity and prevalence of VBDs, with a significant impact on disease dynamics and transmission patterns. Continuous epizootiological monitoring and surveillance are crucial to broaden our knowledge about the spreading of endemic VBDs and the risk of importation of ‘exotic’ diseases. This relies on a continuing and high-level of education of veterinary surgeons, veterinary nurses, physicians and public health workers, to ensure development and implementation of effective control programmes.
KEY POINTS
- The geographical ranges of a variety of vector-borne diseases (VBDs)in Europe are changing.
- Diseases may be seen in dos and cats in the UK that previously were considered to be exotic, with the UK being free of the causative pathogen.
- Many of these diseases are more likely to be seen in dogs than in cats, but infection may still occur in cats.
- Veterinary professionals have a crucial role in detecting, treating and controlling unexpected diseases in companion animals, and in educating pet owners regarding travel-associated risks to their pets and appropriate preventative measures.