An aspiration of the EU is free movement of people between member states, and since many people travel with their pets, this includes companion animals. However, it is recognized that in some cases such movement can increase risks of spreading harmful parasites and other diseases to areas from which they are currently absent. Therefore, since 2000, certain EU countries have been permitted to keep in place legal requirements spe-cifically designed to exclude rabies, the tapeworm Echinococcus multilocularis, and exotic ticks and tick-borne diseases. In the UK, these were essentially vaccination against rabies, with entry delayed at least 6 months after proof of seroconversion, plus treatment against ticks and tapeworms between 24 and 48 hours before entry. From 1st January 2012, owners have to wait only 21 days after rabies vaccination, with no need for a blood test, before being allowed entry to the UK from another EU or approved third country, and there is no requirement to treat against ticks before entry, whatever the country of origin. Dogs (but not cats) still must be treated against tapeworms, but the window has expanded to 1 to 5 days before entry. Further changes are envisaged in future, at least in principle, to react to the latest evidence on the disease status of the UK, and the risks of disease spread through pet movement. Further information can be viewed on www.defra.gov.uk/wildlife-pets/pets/travel/
Current ticks and tick-borne diseases in dogs in the UK
The dog population in the UK already encounters several species of tick. A recent large-scale national study conducted from the University of Bristol showed that ticks are much more commonly attached to dogs than owners realize. Of 3534 dogs presenting to veterinary practices between March and October for a wide range of reasons unrelated to parasitism, 14.9% were found on close inspection to be carrying one or more ticks (Smith et al, 2011). Most of the ticks were not yet fully engorged and were therefore difficult to find. Roughly three-quarters of the ticks were Ixodes ricinus, the common sheep or deer tick (Figure 1), with the other species I. hexagonus, I. canisuga and Dermacentor reticula-tus found less often. The Ixodes species were widely distributed across Great Britain, while D. reticulatus was found in small numbers in west Wales and the Welsh borders, and south-east England. The high prevalence of attached ticks emphasizes that dogs carrying ticks could easily be imported, along with the diseases carried by these vectors, without the owner's knowledge.
The most important tick-borne disease of public health importance in the UK is Lyme borreliosis. This is caused by a bacterium, Borrelia burgdorferi, and can present with a rash, and a wide range of other symptoms especially affecting the joints and the nervous system. Dogs can also be infected. The vector, I. rici-nus, is already widespread and common, and increases in Lyme disease in recent years could be the result of further increases in these tick populations with changes in climate, land use, and deer abundance (Randolph, 2004; Pietzsch et al, 2005; Gilbert, 2010). Anaplasma phagocytophilum, causing granulocytic anaplasmosis in a number of species including dogs and probably humans, is also already present in the UK and transmitted by I. ricinus. Therefore tick control should already be a routine consideration for pet dogs, even if they do not travel outside the UK.
Ticks and tick-borne diseases in the rest of Europe
Ticks
Although D. reticulatus (Figure 2) is already present in Great Britain, it is more common in continental Europe, and UK populations could be augmented by ticks newly imported on dogs. The European tick species of most concern, however, is Rhipicepha-lus sanguineus, since this species can carry several very pathogenic diseases not presently recorded in the UK, such as babesiosis caused by Babesia vogeli, monocytic ehrlichiosis and hepatozoonosis in dogs, and Mediterranean spotted fever in humans. R. san-guineus, in contrast to Ixodes spp., is associated with the kennel environment, and large populations of ticks can build up in such environments. This species is more successful in Mediterranean than in more temperate climates (Beugnet et al, 2011); however, indoor environments could perhaps provide suitable conditions for establishment and population expansion in the UK.
Tick-borne diseases of dogs
Canine babesiosis can be caused by several differ-ent species of Babesia in Europe. The large Babesia spp. include B. canis, carried by D. reticulatus, and B. vogeli, carried by R. sanguineus. Infection causes haemolytic anaemia, with subsequent complications including tissue hypoxia and multiple organ failure manifesting as neurological, renal and muscular signs. Diagnosis is by blood smear, which reveals the parasite cells within the red blood cells. PCR is more sensitive than microscopic examination of a blood smear, but the clinical interpretation of a PCR positive test result is not always straightforward (Otranto et al, 2010). Although both of the large Babesia species are pathogenic, B. vogeli appears to be more common as a cause of severe disease, possibly for epide-miological reasons rather than any inherently more severe pathology. This species is transmitted by R. sanguineus, the brown dog or kennel tick, which can reach very high densities in its core range, especially in kennels and other buildings. The infective challenge to dogs can therefore be high, leading to severe disease. This disease is likely to be even more dangerous in visiting dogs, which do not have immunity (Otranto et al, 2010).
Canine monocytic ehrlichosis is a rickettsial disease infecting the monocytes and leading to fever, lymphadenopathy and splenomegaly. Infected dogs can experience anaemia, thrombocytopenia, bleeding disorders, immune-mediated disease and bone marrow hypoplasia. Diagnosis is by Giemsa-stained peripheral blood smears, supplemented by PCR. Hepatozoonosis in Europe tends to infect haemo-lymphatic tissues, and its role in disease is difficult to determine due to the fact that infected dogs usually present with vague signs and are commonly co-infected with one or more other tick-borne infections (Otranto et al, 2010). Comparison with hepatozoono-sis in North America is complicated by the likelihood that parasite species differ between continents. Both of these diseases, along with Babesia vogeli, are found in the home range of R. sanguineus, which is currently southern Europe, especially the Mediterranean (Beugnet at al, 2011).
Tick-borne diseases of humans
Lyme disease and anaplasmosis are widely distributed in Europe including the UK, and Lyme disease is recognized as an important and increasing public health issue in many countries. Recent surveys of dogs indicate that many are carrying ticks without their owner's knowledge (Smith et al, 2011), and many of these ticks are carrying the bacteria responsible for Lyme disease (Smith et al, 2012). Overall, 0.5% of pet dogs in a recent survey carried infected ticks (Smith et al, 2012). This indicates that the threat of human exposure to Lyme disease is high in endemic areas, since these pet dogs frequented the same environments as their owners. The frequency of infected ticks on dogs could therefore be a useful indicator of the level of this threat, i.e. dogs can act as sentinels for human infection. However, it is unlikely that dogs act as a source of infection for their owners, since most ticks on dogs are adults, and the rate of trans-ovarian transmission of Lyme disease is thought to be low. In Central Europe, a virus is also present in ticks, causing tick-borne encephalitis (TBE). TBE can cause anything from mild febrile illness to severe neurological disease and death, both in humans and more rarely in dogs (Lindgren et al, 2000; Lindgren and Gustafson, 2001). Although the vector, I. ricinus, is already common in the UK, importation of an infected tick on a dog is still in theory a possible route of spread to the UK. Vaccination against TBE is available for humans, although it is not available or used in all countries, while a vaccine does not yet exist for dogs.
The most important human infection carried by the exotic tick R. sanguineus is the bacterium Rick-ettsia conorii, causing Mediterranean spotted fever (MSF) or boutonneuse fever. Infection causes a rash followed by a wide range of symptoms secondary to multiple organ dysfunction, including renal and myocardial complications. MSF is quite rare and is reputed to be less pathogenic than related rickettsial illnesses in North America such as Rocky Mountain spotted fever (RMSF). However, high case fatality more recently in some European countries makes this questionable (de Sousa et al, 2003). Although the incidence of MSF in Italy and Portugal has been in decline since the mid 1990s, it is possible that this is part of a cyclical pattern and precedes an increase in future (Rovery et al, 2008). There is also perhaps some complacency regarding the level of risk to humans, since R. sanguineus is strongly associated with dogs and rarely bites humans. However, there is some indication that the biting behaviour and host preferences of this tick changes with climate, while cases of MSF outside the core range of R. sanguineus raise the possibility of alternative vectors. Overall, then, MSF remains a concern and its importation with R. sanguineus as a result of dog travel is a danger to be avoided.
A new approach to advising travelling dog owners
The Pet Travel Scheme controls were designed exclusively to protect public health from exotic infections that could be imported with dogs. The responsibility on the pet owner was to abide by the law, and their motivation was mainly the risk of delays, disruption and associated stress for the pet and themselves, should they not have the correct documentation at port. The pressure on the veterinary practice, therefore, was to ensure that the correct documents were in place, and that advice concerning the pre-entry parasite treatments was also clear and correct. Nowhere in this process was the health of the travelling pet given top priority: when considered, it was on the initiative of the veterinary surgeon or veterinary nurse giving pre-trav-el advice, and might have been less effective given that the owner was thinking about documents and the costs already invested in the obligatory procedures. Therefore, the changes in the rules provide an opportunity to shift the emphasis of pre-trav-el consultations, and focus more fully on canine health. This means that those providing travel advice should be much more fully aware of the risks to the travelling pet, and how to avoid them while abroad, as well as what to do on re-entry.
Previously, there was no requirement to treat against ticks while abroad. Nevertheless, this has always been important to prevent infections such as babesiosis from being contracted while on holiday. The risk of importing ticks and tick-borne diseases will also be substantially reduced if dogs are properly protected throughout their trip, not just treated on a one-off basis on re-entry. Therefore, core advice for owners of travelling pets should be to protect against ticks for the duration of their journey, using effective repellents and acaricides. Dogs should be groomed regularly and any ticks observed attached in spite of treatment should be carefully removed. Owners should also be made aware of other diseases such as leishmaniosis and how to prevent them, as well as the remaining requirement to treat against tapeworms before re-entry to the UK. In terms of geographic variation in risk, it is true that the ticks and diseases of concern have very different distributions, for example R. sanguineus and related infections in southern Europe, especially the Mediterranean, and D. reticula-tus along with B. canis, and tick-borne encephalitis in I. ricinus, further north and extending into Central and Eastern Europe. However, this all boils down to significant risks from ticks and tick-borne diseases in virtually all parts of Europe. Therefore the advice to prevent against tick attachment and feeding holds whatever the destination. Generally, the risk will increase with duration of the visit and the range of environments that are visited. A post-travel check up could be useful to remove any ticks that have escaped treatment, and to remind owners to be aware of the presenting signs of the important tick-borne diseases, if there has been risk of exposure.
Conclusions
Changes to the Pet Travel Scheme in terms of removal of the requirement to treat against ticks undoubtedly increase the risks that exotic ticks and tick-borne diseases will be imported into the UK with travelling dogs. This could have profound and long-term implications for the health of the canine population, and for human health. However, the risk can be minimized by adherence to good advice on preventive measures, especially application of effective aca-ricides and/or repellents during the whole duration of the visit abroad. Indeed, the change in the rules means that protection of pets’ health becomes the over-riding purpose of the pre-travel consultation, and this could make pet owners more receptive than in the past to such preventive measures. Advisors in veterinary practices should take note and make sure they are up to date on the risks and means of managing them.