Q J Med 1999; 92: 683-687
© 1999 Association of Physicians
Editorial |
Risk of importation of diseases exotic to Great Britain following the relaxation of quarantine regulations
Department of Infectious Diseases, University Hospital of Wales, Cardiff
PHLS Communicable Disease Surveillance Centre, (Wales), Cardiff
Quarantine has successfully prevented the introduction of rabies into Great Britain since its inception nearly 100 years ago. However, improved rabies control throughout Europe and the availability of an effective vaccine have led the government to consider whether quarantine is still necessary. The current system is inconvenient to those wishing to travel abroad with their pets and has greatly reduced the number of domestic animals travelling to and from Britain. The 6 months spent in isolation under veterinary supervision allows the detection and treatment of other diseases, and sick animals may die before coming into contact with other animals. Quarantine may therefore have unintentionally prevented the introduction of several animal pathogens exotic to Britain. We consider the potential risk of new diseases being introduced following the relaxation of quarantine regulations.
On 26 March 1999, the government announced its plans to replace quarantine with a Pet Travel Scheme (PETS), for dogs and cats returning from Europe, rabies-free Islands and possibly North America. This followed the publication of the report of the Advisory Group on Quarantine (AGQ) in September 1998 (the Kennedy report),1 which recommended that quarantine could be replaced by a system in which animals are: identified by the insertion of a subcutaneous microchip; vaccinated against rabies with inactivated vaccine; tested for antibodies by an approved laboratory; treated for exotic infections; and issued with an official health certificate (details available at http://www.maff.gov.uk/animalh/quarantine/movement/movement.html). The AGC believes that these measures will give protection against rabies importation equivalent to the current system of quarantine. The government stated that it was considering the proposals and invited opinions from the public and organizations with an interest in the proposed changes. They received over 3700 replies, the majority of which favoured the relaxation of quarantine. The government now intends to implement the Kennedy Report proposals and hopes to have the new arrangements in place by April 2001 and a pilot scheme in operation a year earlier. Domestic pets from outside the regions covered by PETS would still be subject to quarantine regulations.
When quarantine restrictions in Norway and Sweden were discontinued in 1994, there was a substantial increase in the movement of domestic pets between these countries and the European Union. The magnitude of the increase in animal movements which will occur between Britain and Europe is difficult to predict, but it is likely that many owners will take their pets with them on continental holidays. At present around 7000 domestic pets enter Britain each year and it is not unreasonable to believe that there may be a 30 to 70-fold increase.1 This animal movement and the loss of veterinary supervision and isolation provided by quarantine will increase the risk of exotic infections and their vectors being introduced to Britain. Many of these infections are principally of veterinary importance, but others, such as alveolar echinococcosis and the rickettsioses, could be a threat to human health. The Kennedy Report considered the risk of introduction of five zoonoses exotic to Britain and two diseases that do not affect humans.1 We discuss the risks from these and other organisms.
Echinococcus multilocularis, the fox tapeworm, has a two-host life cycle involving canids (predominantly foxes and coyotes but occasionally domestic dogs and cats) as definitive hosts and rodents as intermediate hosts. Humans are at risk of accidental infection by ingestion of eggs contaminating soil or unwashed fruit and vegetables. Multiple hydatid cysts develop in the liver and metastasise to other organs.2,3 Common symptoms include abdominal pain, jaundice, fever, anaemia, weight loss and hepatomegaly.2 Patients may have had symptoms for several years before diagnosis, and mortality can be very high, over 90% for advanced disease.4 Early diagnosis is essential. as prognosis depends on the stage at which the disease is treated.3 The prevalence of E. multilocularis is highest in the tundra regions of North America, Russia, northern Japan, central and northwest China and the central Asian Republics.5 It has also been recorded in ten European countries, including Belgium, France, Luxembourg, Germany, Switzerland, Liechtenstein, Austria, Poland, Czech Republic and Turkey, and its prevalence may be increasing with rising fox population densities.6–9 Domestic dogs and cats could acquire this tapeworm by ingesting small rodents during a European visit, and return with the infection. Fox tapeworm could then become established in Britain and may prove more difficult to control than the native dog tapeworm, E. granulosus, because of its sylvatic lifecycle. Although quarantine does not guarantee prevention of the introduction of the fox tapeworm, the widespread use of routine worming treatments provided substantial protection. The Kennedy Report recognized that every effort must be made to prevent this serious disease becoming established in Britain, and suggested that all imported cats and dogs should be treated with praziquantel within 24 h of import.1 This treatment is virtually 100% effective against immature and mature stages of E. multilocularis, but because it is not ovicidal, a repeat course of treatment would be required.9 Prevention of the introduction of E. multilocularis into Britain will depend upon adequate controls to ensure that all cats and dogs receive praziquantel at the correct time and correct dose before entering the country.
Rhipicephalus sanguineous, the brown dog tick, is the usual vector for Rickettsia conorii, the causative agent of Mediterranean spotted fever (also known as Boutonneuse fever) and is transmitted to a vertebrate host from tick salivary glands during feeding. R. conorii occurs throughout the Mediterranean, including Italy, Spain, Portugal, Greece, Turkey, Cyprus, Palestine, Romania, Bulgaria, Tunisia, Algeria, Morocco, Libya and Egypt.10 It is also widespread in Central and Southern Africa and Asia.10 Mediterranean spotted fever is often a mild disease in humans, but severe forms occur in 6% of cases and overall mortality is up to 2.5%.10,11 Features include an eschar at the bite site (`tache noir'), maculopapular or purpuric rash, fever (>39 °C), headache, myalgia, arthralgia, elevated hepatic transaminases and a low platelet count. In severe cases, neurological, renal and cardiac problems occur.11 R. sanguineous is currently not found in Britain. Other tick species belonging to the genera Amblyomma, Haemophysalis and Ixodes can also transmit the disease, but with reduced efficacy. Therefore R. conorii probably would not become widespread in Britain unless the brown dog tick also became prevalent. Dogs have been considered as a reservoir for R. conorii as they are the main host for R. sanguineous.10 However although dogs seroconvert after being bitten by infected ticks, they do not develop disease, and R. conorii has not been isolated from dogs in Southern Europe.10 Dogs are therefore unlikely to be a significant reservoir host. R. conorii multiply in almost all organs of their tick host and can be transmitted transovarially.12 It has been suggested that rickettsiae may also be transmitted between ticks feeding in close proximity on the host's skin.10 Therefore R.-conorii-infected brown dog ticks probably pose a greater threat to the introduction of Mediterranean spotted fever into Britain than infected pets. Tick infestations have been detected in quarantined dogs allowing treatment before contact with other animals.1 Therefore quarantine may have been important in preventing the introduction of Mediterranean spotted fever and other tick-borne infections into Britain. The Kennedy Report suggested that all imported cats and dogs should be treated with an anti-tick wash or spray within 24 h prior to entry. Whether this will be adequate to prevent infected ticks entering Britain is not certain. R. sanguineous ticks have been found in a household in Hull, the authors concluding that they were transmitted accidentally by car from Brittany, even though the owner's dog had remained in Hull. The ticks probably came from a neighbour's dogs which travelled in the car in France.13 As ticks which have engorged on pets during a trip abroad could remain in a car for some time before feeding again, many more ticks could enter Britain in this way, despite anti-tick treatment of the animals themselves.
Although several species of Leishmania cause leishmaniasis, Leishmania infantum is the predominant cause of both visceral and cutaneous leishmaniasis in Europe. The predominant reservoir host is the domestic dog and infection reflects the distribution of the vector, the Phlebotomus sandfly. L. infantum transmission is concentrated in suburbs and villages close to the sea throughout the Mediterranean region including southern France, Portugal, Spain, Italy, Greece, Turkey and North Africa.14 The visceral form of the disease was previously largely restricted to young children under 2 years, adults generally only developing cutaneous disease.14 However there has been a recent dramatic increase in adult visceral leishmaniasis due to cases in HIV patients, particularly among injecting drug users in Spain.14,15 Typical features of visceral leishmaniasis include fever, weight loss, malaise, anaemia and hepatosplenomegaly. Dogs may also develop severe disease eventually causing death. Quarantine is not effective in preventing the introduction of leishmaniasis because of its long incubation period. Dogs travelling to Mediterranean regions are at risk of acquiring leishmaniasis, but they are unlikely to spread the infection in Britain as the sandfly Phlebotomus is not present here. However, it is possible that Phlebotomus species could become established in southern Britain, particularly if global climate changes produce significant warming of air temperatures. Surveillance for the vector will be important to provide an early warning of risk of L. infantum being introduced.
Bartonella henselae, the causative agent of cat scratch disease, is common among cats in the USA and has been described in several European countries.16,17 Cats are the natural reservoir of B. henselae and direct transmission to humans occurs via a cat scratch, bite or lick.18 B. henselae was considered in the Kennedy Report because it was previously uncertain whether it occurs in Britain. However it is now known that B. henselae infections are common in this country,19 and therefore changes in the quarantine regulations are not relevant to the risk of this disease.
Dirofilaria immitis is a common filarial parasite of dogs in southern Europe, the USA, Australia, Asia, Africa and South America.20 The disease in humans is very rare and generally mild, so this disease is principally of veterinary importance. In dogs, the adult worms inhabit the right side of the heart and pulmonary arteries. Heavy infestations can lead to cardiac insufficiency, pulmonary thrombosis, myocardial infarcts and frequently early death. In humans the infection is often asymptomatic, although it may present with chronic cough, chest pain, fever and haemoptyssis. The finding of a coin-shaped lesion on chest radiography sometimes leads to unnecessary surgical resection in the belief the lesion is malignant.21 The vectors of D. immitis are Aedes, Anopheles and Myzorhynchus mosquitoes, several species of which occur in Britain. However the parasite may not survive Britain's climate, as it has been suggested that temperatures below 17°C kill the immature forms of the parasite in the mosquito.20 Ivermectin kills D. immitis larvae22 and could be used as prophylaxis for dogs returning from short holidays in Europe. Treatment of adult worms is less satisfactory and very toxic, and could not be routinely given to all dogs entering Britain after prolonged periods spent abroad. Quarantine does not prevent the disease due to its long asymptomatic period. Vets will need to become increasingly aware of the possibility of heartworm infection in dogs which have travelled abroad.
Tick-borne encephalitis (TBE) virus is a flavivirus spread by Ixodes ricinus and I. persulcatus ticks. Reservoir hosts are believed to include rodents such as field mice and bank voles.23 In humans, TBE has a typically biphasic course. In the initial viraemic phase there is fever, headache, myalgia and general malaise lasting up to 8 days. In the second stage, meningoencephalitis occurs causing neurological deficits in 20% of patients. The disease is more severe in adults, with overall mortality of 1–5% of cases.24 TBE is geographically widespread in Europe, but has not been described in Britain. Prevalence varies geographically with low rates of virus isolation (<10 cases per year) in France, Italy and Greece, intermediate rates (80 to 300 cases per year) in Austria, Hungary, former Yugoslavia, Czech Republic and Germany and very high rates (>5000 cases per year) in parts of the former USSR.23 The prevalence of infected ticks has been found to vary between 0.05% in Italy and 40% in parts of the former USSR.23 As I. ricinus occurs in Britain, TBE could potentially become established here. Although TBE virus can infect dogs, it is more likely that the disease would be established due to importation of infected ticks than infected humans or domestic animals. Nymphs are the most likely vector, because they are less host-specific than adult ticks and due to their size, much more difficult to detect. Dogs are more likely to introduce infected ticks than humans, as ticks are more visible on human skin. The use of topical anti-tick treatment suggested by the Kennedy report will help prevent the introduction of ticks, although this may not be fully effective for the reasons discussed previously.
R. rickettsii, the agent of Rocky Mountain spotted fever (RMSF), occurs throughout the US and Southern Canada, and could be introduced to Britain if relaxation of the quarantine regulations is applied to these countries. The vectors include Dermacentor species and the brown dog tick R. sanguineous.24 The clinical severity of RMSF in humans is highly variable, from a mild febrile illness to profound shock and multi-organ failure.25 Small mammals such as field mice, rabbits and hares are believed to be the principal reservoirs of infection. Dogs can also be infected, but they are unlikely to be a significant reservoir of the disease, because only 1% of ticks feeding on rickettsaemic dogs become infected.26 Several other spotted fever group rickettsiae occur in Europe including R. sibirica (European parts of former USSR), R. slovaca (Czechoslovakia, Switzerland, France and Portugal), R. helvetica (Switzerland), R. rhipicephali (France), R. massiliae (France, Greece, Portugal), Mtu 5, Bar 29, PoTiR 1 and PoTiR8 strains (France, Spain, Portugal), Astrakhan SFG rickettsia (Astrakhan) and R. akari (former USSR).24 These infections are spread by several vectors including R. sanguineous and Dermacentor species. Infected ticks provide the greatest risk of introduction of R. rickettsii or other rickettsiae to Britain. Treatment of animals with a topical anti-tick agent prior to importation will be the most important control measure.
Francisella tularensis causes a plague-like disease in humans and animals, between the latitudes of 30°N and 71°N.27 F. tularensis subspecies holarctica is widespread in northern Europe, but does not currently occur in Britain. Subspecies tularensis occurs in North America27 but has also recently been described in Europe.28 The epidemiology of F. tularensis is very complex, with natural infections demonstrated in at least 14 species of ticks, six flea species, several species of mosquito and over 100 mammals.27 Transmission of tularaemia can occur due to the bites of ticks and mosquitoes, drinking infected water or by inhalation. Widespread dissemination can occur if an infected animal falls into a river or by air if rodent-contaminated hay is moved. Many different forms of human disease are recognized including the ulceroglandular, oculoglandular and oral-tonsillar-glandular forms of primary localized infection; the influenzal, pulmonary and abdominal forms of primary generalized infection, and several forms of secondary generalized infection, including generalized glandular swelling, multiple lung infiltrations, typhoidal illness and central nervous system involvement.27 Due to the large number of potential animal reservoirs of infection and vectors capable of transmitting the disease, it is difficult to evaluate the risk of F. tularensis becoming established in Britain. Potentially it could become widely disseminated and be a threat to wildlife, domestic animals and humans. Topical anti-tick treatment of animals entering Britain will help reduce the risk of introduction but infected animals could still pose a risk. A high degree of awareness of the disease among doctors, vets and those working with wildlife will be needed to provide early warning of any potential outbreak.
Ehrlichia chaffeensis, the causative agent of human monocytic ehrlichiosis, is predominantly found in North America but cases in Europe have been described.29,30 White-tailed deer are probably the principal animal reservoir though this remains uncertain.31 The vector is probably Ixodes ticks.31 Features of human infection include malaise, nausea, vomiting, myalgia, bone marrow suppression and in severe cases renal failure, encephalopathy and death.32 The risk of this disease being introduced to Britain by dogs carrying E. chaffeensis-infected ticks is difficult to assess until more is known about the epidemiology of this organism.
Ehrlichia canis and Babesia canis were considered by the Kennedy report because they are important canine pathogens, although they are not known to cause disease in humans. E. canis can cause a wide range of symptoms in dogs including, fever, lymphadenopathy, weight loss, jaundice, anaemia and haemorrhage. The disease may present as a chronic or acute illness and can be fatal. Treatment of dogs with a topical anti-tick agent will only partly reduce the risk of introduction to Britain, because healthy dogs can be carriers of infection.31 B. canis is a protozoan parasite which can cause serious disease in dogs including fever, jaundice, anaemia and haemolyis. Transmission occurs via ticks, and preventing disease entering Britain will depend on effective use of topical anti-tick treatment.
A large number of diseases exotic to Britain have the potential to infect dogs and cats and could theoretically be transmitted to humans. We have focused on some of the most important diseases, but due to the likely enormous increase in animal movements, it is difficult to anticipate all of the infectious disease problems which could arise. Two important treatments have been highlighted by the Kennedy Report, praziquantel and topical anti-tick agents. Praziquantel is important to prevent the fox tapeworm being introduced and anti-tick treatment to prevent several vector-borne diseases. The safeguards which are set in place to ensure that these treatments have been correctly applied to all imported cats and dogs will be important determinants of whether new diseases are introduced to Britain. As discussed previously treatment of animals alone may not be sufficient to prevent the importation of infected ticks and it may be necessary to apply anti-tick spray to cars and other vehicles.
The government has suggested a one-year pilot programme before complete implementation of the PETS scheme. During this period, and after PETS becomes fully operational, it will be necessary to set up surveillance mechanisms for infectious diseases in dogs and cats entering Britain. A sample of the returning animals could be screened for several of the infections highlighted in this review (e.g. by serology or stool examination). Any exotic infectious diseases diagnosed in these animals will need to be reported and diagnostic specimens submitted to Veterinary Laboratories Agency facilities. Medical practitioners will need to have awareness of potential unusual zoonoses which could affect their patients and report them to their local Consultant in Communicable Disease Control to instigate further investigation. The public wishes the current quarantine regulations to be relaxed. The likelihood of exotic diseases other than rabies being introduced is uncertain. It is vitally important that any diseases which do occur are detected early and met with an appropriate response.
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