Rabies in Europe: what are the risks?

Abstract

Rabies remains a serious endemic disease in animal populations in many European countries. Oral vaccination by use of rabies vaccine baits has proved to be durably efficient for controlling and eliminating terrestrial rabies. However, the recurrence of rabies in some countries highlights the fragility of rabies-free country status and the need for continuous surveillance. In Eastern and Southern countries, the rabies control programmes for foxes should be accompanied by stray dog management measures in view of the high populations of strays in certain areas. Alerts of rabies in pets imported from enzootic countries are regularly reported in Europe, threatening the rabies-free status of terrestrial animals. New variants of rabies virus have been recently discovered in autochthonous bats, implying research studies to assess the efficacy of the current vaccines against those strains and the possible crossing of the species barrier in terrestrial mammals. The incidence of the disease in humans is very low, with cases contracted in Europe or in enzootic countries. Sustainable strategies of vaccination programmes in animals and improvement of public awareness, particularly for travelers, regarding rabies risks and legislation for pet movements would render accessible the elimination of rabies in Europe.

Keywords::

• importation
• pet
• rabies
• rabies risk
• vaccination

Rabies is a fatal viral encephalitic disease that is caused by a rhabdovirus of the genus Lyssavirus which can affect all warm-blooded mammals. The disease is maintained in a wide range of wild and domestic animals. The virus is excreted in the saliva of infected animals and is usually transmitted to a susceptible host through biting [1]. The annual rabies burden is around 60,000 deaths annually [2], with 99% of them occurring in Africa and Asia through dog transmission [3], but the true incidence of this neglected disease is greatly underestimated due to a lack of systematic surveillance and reporting by most developing countries [4].

Rabies in wildlife

In Europe, rabies was historically reported in dogs and was progressively eliminated at the turn of the twentieth century in most European countries through dog control measures (destruction, movement restriction and muzzling) [5]. From the 1940s, the virus became adapted to the red fox (Vulpes vulpes) and spread westwards and southwards from the Russian–Polish border to the rest of Europe with a 20–60 km/year advance. Rabies is a notifiable disease in most of Europe.

Oral rabies vaccination (ORV) of foxes with live vaccines has been shown to be the most effective method for the control and elimination of terrestrial rabies in Western and Central Europe [6]. Vaccine baits containing a capsule or plastic sachet filled with a liquid antirabies vaccine are dispersed throughout fox habitats. Since 1989, the EU has become the driving force for supporting disease eradication programs and has been co-financing ORV programs in Member States (75% of funding since 2010) [7]. Since 2007, the EU has been providing financial support to both candidate and non-candidate countries [8]. As a result, the total number of reported rabies cases in Europe has significantly decreased, with 21,023 cases in 1990, 9834 in 2002 and 6186 in 2012 [9]. In 2012, the proportion of rabid domestic animals (3088 cases) was approximately similar to that diagnosed in wildlife, with domestic cases mainly reported in Ukraine (1161 cases) and in the Russian Federation (893 cases) [9]. These data suggest that rabies surveillance may be more focused on domestic species.

To date, several European countries have become rabies-free of terrestrial rabies (Austria, Belgium, Czech Republic, Estonia, Finland, France, Germany, Italy, Luxembourg, Switzerland and the Netherlands), and there is reasonable hope that this list will increase in the near future. However, rabies is a trans-boundary disease, and re-infections may occur. The recurrence of rabies in Italy (2008), Greece (2012) and Slovakia (2013) from bordering infected areas highlights the fragility of rabies-free country status and the need for continuous surveillance of the epidemiological situation, both in wildlife and in domestic animals [10]. In most infected countries, vaccination of pets is recommended or compulsory [11] as a preventive measure for animal and human health.

Rabies in humans

The incidence of human rabies in Europe is very low, both for cases contracted in Europe and imported from endemic countries. It should be noted that a number of travel-related and autochthonous rabies cases are neither reported nor published [3,12]. From 1990 to 2012, a total of 210 human fatalities due to rabies were reported in Europe [9] with around 10 cases per year. Contrary to the animal data, the global trend of reported human data over time suggests a relative stability in the number of cases reported. Indigenous cases were mostly reported from Eastern Europe, corresponding to patients bitten by stray or aggressive domestic dogs or foxes. In certain countries of southeastern Europe, stray dog populations are very high and their management difficult. This poses a threat to human health and animal welfare. Dog population management should be considered an integral part of rabies programs [13].

From 1990 to 2012, a total of 31 human deaths [12,14] were caused by infection acquired during a visit to an endemic area, usually in Africa or Asia. In 28 of the 30 cases where the cause of animal rabies was identified, the patient had been exposed to a dog. Histories of the reported cases showed that many travelers and healthcare workers ignore the WHO recommendations when exposed to rabies [12], consisting of local wound care, vaccination and, if indicated, passive immunization with immunoglobulins. The main risk factors identified were the country of destination, age and the reason for traveling, with the highest risks found in southeast Asia, India and North Africa, young people and those traveling to visit friends and relatives, respectively [15]. The risk of a traveler contracting rabies is considered low, although data may be underreported, since for example in 2012 over 52 and 233 million international travelers visited Africa and Asia, respectively, 52% of whom were tourists [12,16]. The last imported human case of rabies occurred in May 2012 in a British woman who died in the UK after having contracted the disease through a dog bite while traveling in India.

Although very rare, rabies can also be transmitted through organ transplantation. In February 2005, six German patients received organs or tissues from a donor with rabies. Three patients who received lung, kidney and combined kidney and pancreas organs died [17].

Importation of rabid pets

Infected and rabies-free European countries regularly report imported rabies cases in cats and dogs. In most of these cases, the animals are non-vaccinated puppies or young dogs. From 2000 to 2013, a total of 22 imported pets incubating rabies were recorded (21 dogs and one cat) [18]. The risk associated with importing pets depends upon the geographical location as well as upon the patterns of tourism. In France, for example, rabid dogs have frequently been imported from Morocco, a country highly appreciated by tourists traveling by car through Spain. In 2013, two imported cases occurred in France and in Spain, both originating in Morocco [18]. Such illegal importations generally result in the administration of high numbers of post-exposure treatments [3]. Moreover, such imported cases pose a threat of rabies reintroduction into rabies-free areas. In 2008, France lost its rabies-free status for 2 years due to secondary cases after the illegal importation of a rabid dog [19].

Rabies in bats

European countries occasionally record rabies cases in bats (469 cases reported since 2001 mainly in The Netherlands, Germany, Poland and France). Two main lyssavirus species are the causative agents of rabies in European bats, that is, European Bat lyssavirus type 1 and 2 (EBLV-1 and EBLV-2). Four more Eurasian lyssaviruses have been described, generally from single isolates taken from different bat species [20]. More recently, two novel lyssavirus species – Bokeloh Bat Lyssavirus (two cases in Germany in 2010 and 2012, two cases in France in 2012 and 2013) and Lleida virus in 2011 (one case in Spain) – have been discovered [21,22]. Both EBLV-1 and EBLV-2 have caused four human fatalities in Europe [20], and low levels of spill-over infections of EBLV-1 have been documented in non-flying mammals. Exposure to bats or their secretions should be considered as a potential rabies risk regardless of the world region in which the exposure occurs. Studies in animal models suggest that current human rabies vaccines have variable efficacy against some of these new lyssaviruses and that more cross-reactive vaccines may be necessary [20].

Discussion & conclusion

While the threat from rabies in Europe has decreased mainly as a result of successful ORV programs, fox rabies in Eastern and Southern Europe continues to pose a risk. In such areas, the populations of stray dogs are high and measures to control dog population, which should be part of rabies control programs, have been relatively unsuccessful. EU animal welfare legislation could help in implementing efficient control practices to replace the mass killing of strays, a measure which is not durably efficient. Reliable data are needed from all European countries for more accurate surveillance and reporting of rabies cases in people and animals, including bats, demonstrating the need for a single health approach [23] for improving coordination in the fight against rabies. Furthermore, rabies eradication programs need to be continuously evaluated by the competent national authorities in order to be able to improve the strategy of vaccination in the field, with a view to enhancing their cost efficiency.

The WHO has established a worldwide map for rabies risks [1], from no-risk countries to countries or areas of low, medium and high risk. Western and Central European countries belong to the low-risk category in which pre-exposure immunization is recommended for people likely to be in contact with bats. This part of Europe is bordered by the countries of Southern and Eastern Europe as well as those of Africa, which are classified in a high-risk category. Pre-exposure immunization is recommended for travelers/people likely to be in contact with domestic animals, particularly dogs and other rabies vectors.

The persistence of rabies in the developing world and increased travel to exotic destinations means that the disease is still of public health concern to Europe. Therefore, rabies should be suspected, even when a history of animal bites is lacking, in patients with encephalitis or paralysis who come from a rabies-enzootic country or who are returning from a trip to one of these countries. As the disease is invariably fatal after the onset of neurological symptoms, timely prophylaxis in cases of exposure to a potentially infected animal is of utmost importance [2], and knowledge of the epidemiological situation is vital to making decisions with regard to appropriate post-exposure measures.

Tourists are generally unaware of the risks of being infected through bites from animals that may have normal behavior at the early stage of infection, of the danger of importing potentially rabid animals and of the rules governing the movements of pets [15]. EU Regulation (EC) No. 998/2003 applicable to the non-commercial movements of pets between Member States and from third countries requires that animals be identified and that they possess a passport indicating a valid anti-rabies vaccination. Pets must be serologically tested with a positive result at least 30 days following vaccination and 3 months before being moved from certain third countries to the European Union. Experience shows that pet owners, veterinarians as well as the officials in charge of checks at entry are insufficiently aware of this rule.

Continued vigilance is needed to ensure that animals entering the EU are properly vaccinated and, whenever required by legislation, tested for their immune response. Policy should focus on reducing the incidence of exposure to rabies mainly by promoting both awareness of the danger of rabies and behaviors which can help to prevent the disease. European countries not already involved in eradication programs should rapidly initiate ORV which is the only cost–effective and sustainable strategy for controlling and eliminating wildlife rabies in Europe.

Financial & competing interests disclosure

The authors have no relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript. This includes employment, consultancies, honoraria, stock ownership or options, expert testimony, grants or patents received or pending, or royalties.

No writing assistance was utilized in the production of this manuscript.