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Emerging zoonoses and vector-borne infections affecting humans in Europe

Published online by Cambridge University Press:  20 April 2007

R. M. VOROU*
Affiliation:
Hellenic Center for Disease Control and Prevention, Athens, Greece
V. G. PAPAVASSILIOU
Affiliation:
Hellenic Center for Disease Control and Prevention, Athens, Greece
S. TSIODRAS
Affiliation:
Hellenic Center for Disease Control and Prevention, Athens, Greece Fourth University Department of Internal Medicine, University of Athens Medical School, Athens, Greece
*
*Author for correspondence: Dr R. M. Vorou, 34 Ipirou Str, Halandri, 15231, Athens, Greece. (Email: vorou@keelpno.gr)
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Summary

The purpose of this study was to assess and describe the current spectrum of emerging zoonoses between 2000 and 2006 in European countries. A computerized search of the Medline database from January 1966 to August 2006 for all zoonotic agents in European countries was performed using specific criteria for emergence. Fifteen pathogens were identified as emerging in Europe from 2000 to August 2006: Rickettsiae spp., Anaplasma phagocytophilum, Borrelia burgdorferi, Bartonella spp., Francisella tularensis, Crimean Congo Haemorrhagic Fever Virus, Hantavirus, Toscana virus, Tick-borne encephalitis virus group, West Nile virus, Sindbis virus, Highly Pathogenic Avian influenza, variant Creutzfeldt–Jakob disease, Trichinella spp., and Echinococus multilocularis. Main risk factors included climatic variations, certain human activities as well as movements of animals, people or goods. Multi-disciplinary preventive strategies addressing these pathogens are of public health importance. Uniform harmonized case definitions should be introduced throughout Europe as true prevalence and incidence estimates are otherwise impossible.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2007

INTRODUCTION

The ability of infectious agents to cross the species barrier explains why numerous zoonotic and vector-borne agents affect humans. Of the growing list of human pathogens, 1415 according to one report [Reference Cunningham1], 61% are zoonotic [Reference Cunningham1]. Among emerging infectious diseases, 75% are zoonotic, originating principally from wildlife [Reference Blancou2]. The latter is a reservoir of microorganisms that, once transferred to humans, may emerge as public health threats [Reference Blancou2]. Other factors that might be important in the emergence and spread of zoonotic and vector-borne diseases include the increasing proximity of human and animal populations caused by growth of the human population, their mobility for recreational, cultural and socioeconomic purposes, and the efforts to keep them well nourished [Reference Cunningham1, Reference Blancou2]. Air transportation and air travel may facilitate the global spread of emerging infectious diseases as occurred with the SARS epidemic [Reference Cunningham1].

Detecting a rise in incidence of a specific disease remains the cornerstone of containment of an emerging communicable threat. However, as the emergence of an infectious disease appears to be the end result of a multi-factorial complex process, there is difficulty in predicting it, and also in responding quickly. This review attempts to identify zoonoses and vector-borne diseases that had an increasing impact on humans in Europe in the period from 2000 to August 2006. In addition, it discusses the social, ecological, technological and microbial factors that have affected emergence of such infections. Monitoring changes in these factors will be of paramount importance in the strategies against these infections.

METHODS

Search strategy and selection criteria

A computerized search of the Medline database from January 1966 to January 2006 was conducted. Articles reporting original data and original articles on emerging or re-emerging zoonoses in European countries were the sources used for this review. The terms used in the search included ‘emerging zoonoses’, ‘Europe’, ‘European countries’, and all the 46 European countries separately. In addition cross-checking of the results was performed with additional searches using all zoonoses from a formal recent combined WHO/FAO/OIE European Region Report [3]. The specific criteria used for each country were [3, Reference Hughes4]: (a) the detection of a new zoonotic or vector-borne species associated with human disease, (b) an increase in the incidence of a known zoonotic or vector-borne disease in humans, (c) spread of a pathogen to a new vector or animal reservoir and change in transmission dynamics, and (d) novel geographical locations for hosts or vectors of these pathogens. Each individual type of emergence is indicative of a separate dimension of the public health impact of each pathogen.

Exclusion criteria

Emerging zoonoses or vector-borne infections that could be potentially imported into Europe from other continents were excluded from this review.

RESULTS

Fifteen emerging zoonotic or vector-borne infections with increasing impact on humans in Europe during the last 7 years were identified (Table 1). Table 2 lists a description of the identified agents together with their factors affecting emergence.

Table 1. Emerging zoonoses and vector-borne diseases in Europe: pathogens, main modes of transmission, and recent data on human cases or outbreaks in European countries from 2000 to August 2006

Table 2. Risk factors for the emergence of zoonoses and vector-borne diseases in Europe from 2000 to August 2006

The emergence of several of these infections is related to multiple factors (e.g. movement of animals and climatic changes affecting vectors) and the degree of importance of one over the other is not always easy to determine. Emergence of vector-borne diseases is predominantly affected by climatic variations and changes, and certain human activities and behaviour. On the other hand emergence of Hantaviruses, highly pathogenic avian influenza A/H5N1, trichinellosis, echinococcosis and prion disease is associated predominantly with other factors such as movements of animals, people or goods (Table 3). A detailed description of individual agents is given below.

Table 3. Criteria for emergence of the identified zoonoses and vector-borne diseases in Europe from 2000 to August 2006

BACTERIAL AND RICKETTSIAL INFECTIONS

Borrelia burgdorferi

Borrelia burgdorferi sensu lato is a complex of the following species: B. burgdorferi sensu stricto, B. afzelii, B. garinii, B. bissettii and B. lusitaniae that have been implicated as a cause of human Lyme disease mostly in central and Northern European countries [Reference Mehnert and Krause5Reference Nygard, Brantsaeter and Mehl7] including Scandinavia, Austria, Germany, and Switzerland (Table 1). Iceland is reportedly free of the disease, and Ireland has a very low incidence. An increase in incidence of 33%, from 17·8 cases/100 000 population in 2002 to 23·3 cases/100 000 in 2003 has been noted in eastern German states recently [Reference Mehnert and Krause5]. In Norway the highest number of Lyme cases, 253 in total, was noted as recently as 2004 [Reference Nygard, Brantsaeter and Mehl7].

The factors behind the increase in incidence are not clear (Table 2). Rodents serve as important hosts in the enzootic cycle of the disease and their population expansion may be a factor. A high proportion of rodents in Central Europe are seropositive for B. burgdorferi [Reference Stefancikova8]. Along with a substantial role in the maintenance of Lyme's disease in enzootic foci, migratory birds transfer infected ticks across national and intercontinental borders establishing new endemic foci of disease. Since ticks may attach to a host for 24–48 h, sufficient time is provided for some birds to travel hundreds or even a few thousand miles along migration routes before ticks complete feeding and drop off [Reference Reed9]. Even transhemispheric transfer by seabirds has been proven [Reference Olsen10]. A novel genospecies causing Lyme disease, B. spielmanii, has been recently detected in Hungary, The Netherlands and Czech Republic [Reference Foldvari, Farkas and Lakos11] and in several French and German sites where garden dormice have been identified as a new reservoir host [Reference Richter12] (Table 3).

Along with the emergence of Lyme borreliosis in the temperate northern hemisphere, there is an increased awareness of the potential for emergence of human babesiosis in Europe due to its transmission by the same tick vectors [Reference Piccolin13].

Bartonella spp

New Bartonella spp., an extended animal host range, and new endemic locations have been recognized since 2000 (Table 1). Advanced molecular diagnostics have greatly enhanced our ability to detect Bartonella spp. infections and have assisted in defining their mammalian reservoirs. Serology is mostly useful for the Cat Scratch Disease (CSD) agent Bartonella henselae.

Novel species have been recognized and may pose a threat to humans, e.g. the rodent-borne B. elizabethae, B. grahamii, and the feline B. koehlerae [Reference Avidor14, Reference Boulouis15].

Novel vectors and an extended range of mammal reservoirs have been identified including rodent and cat fleas for the rodent-borne and feline-borne Bartonella spp. respectively [Reference Boulouis15, Reference Tea16].

Expansion of the range of vectors and mammal reservoirs has been noted for B. henselae and other Bartonella spp. in recent years [Reference Tea16]; B. henselae, the CSD agent has been identified in the tick Ixodes ricinus, in long-tailed field mice and in domestic cats in novel geographical areas in Europe [Reference Engbaek and Lawson17, Reference Melter18]. B. quintana which causes the body-lice-mediated trench fever in humans and had no known animal reservoir, was shown to infect a domestic cat. This could explain B. quintana infections identified in humans who maintain high hygiene standards, are not infested with body lice, but have close contact with cats (Tables 2 and 3) [Reference La19].

Francisella tularensis

Tularemia caused by Francisella tularensis, a Gram-negative coccobacillus, is a widely dispersed disease throughout the Northern Hemisphere including Europe where only F. tularensis subsp. holarctica, also known as type B is endemic [Reference Cross, Penn, Mandell, Bennett and Dolin20Reference Perez-Castrillon24]. The terrestrial and aquatic cycles of the infection include a wide variety of rodent reservoirs, e.g. hares, squirrels, bank voles, beavers, muskrats, as well as a spectrum of diverse arthropod vectors such as ticks, midges and mosquitoes. In each geographical location diverse numbers of vectors and vertebrate hosts may be involved, e.g. tabanids, voles, hamsters, mice, and hares in Russia, mosquitoes in Sweden, Finland, Russia, and ticks in Central Europe [Reference Cross, Penn, Mandell, Bennett and Dolin20Reference Perez-Castrillon24] (Table 1).

In Finland and Sweden outbreaks were recorded at least once every decade [Reference Payne25, Reference Eliasson26], but as a human disease it has re-emerged causing increasing numbers of cases in Bulgaria in the last decade [Reference Kantardjiev27], Sweden in 2000 and 2003 [Reference Payne25, Reference Eliasson26] and more recently in France [Reference Siret23].

In other areas outbreaks occur only occasionally except in times of socio-ecological change and disruption of the public health system such as has occurred recently from armed conflict in Kosovo (Table 2) [Reference Reintjes28]. Contact with animal products through wounds and abrasions, consumption of contaminated food or water [Reference Reintjes28], and inhalation [Reference Siret23] are the main modes of transmission in endemic areas [Reference Tarnvik, Priebe and Grunow21]. The most recent outbreak was reported from Germany among hare hunters in January 2006 [Reference Hofstetter29] (Table 3).

Anaplasma phagocytophilum

Human granulocytic anaplasmosis (also known as human granulocytic ehrlichiosis), is a tick-borne zoonosis caused by the pathogen Anaplasma phagocytophilum (formerly named Ehrlichia phagocytophila and Ehrlichia equi). It was associated with tick-borne fever in cattle, sheep, and goats in Europe for several decades.

Human cases emerged in Europe in 1996 [Reference Petrovec30] and have been reported in several European countries since then (Table 1) [Reference Blanco and Oteo31]. Co-infection with Borrelia burgdorferi is attributed to their common vectors [Reference Piccolin13, Reference Parola, Davoust and Raoult32, Reference Stanczak33], I. ricinus ticks (throughout Europe), and I. persulcatus ticks (Eastern parts of Europe) [Reference Santos34, Reference Parola35].

Transmission and propagation of A. phagocytophilum occurs in large mammals such as horses, cattle, sheep, goats, dogs, cats in Europe. Small mammals and not ticks are the reservoirs of anaplasmoses. Several rodent and other animal species contribute in various European countries [Reference Petrovec36Reference Oporto40], e.g. roe deer have a principal role in the life-cycle of I. ricinus in Spain [Reference Oporto40].

Roe deer are the main reservoir for A. phagocytophilum in Central Europe and Scandinavia with a high seroprevalence of about 95% and a variable rate of PCR-proven infection ranging from 12·5% in the Czech Republic to 85·6% in Slovenia [Reference Skarphedinsson, Jensen and Kristiansen41].

Expansion of vectors and reservoirs into novel geographical locations has been noted in several countries, e.g. Spain [Reference Oporto40], Austria [Reference Petrovec36], Czech Republic [Reference Petrovec36] and Denmark [Reference Skarphedinsson, Jensen and Kristiansen41]. The role of migrating birds in long-range tick transfer may be important since the same A. phagocytophilum gene sequences were detected in infected ticks on migrating birds and in humans and domestic animals in Sweden [Reference Bjoersdorff39] (Tables 2 and 3).

Rickettsiae spp

Spotted fever group (SFG) rickettsioses caused by novel species such as R. slovaca [Reference Cazorla42Reference Punda-Polic44], R. helvetica [Reference Nielsen45Reference Fournier47], R. aeschlimannii [Reference Punda-Polic44, Reference Raoult48, Reference Fernandez-Soto, Encinas-Grandes and Perez-Sanchez49] and others such as R. sibirica sensu stricto [Reference Shpynov50, Reference de Sousa51], R. heilongjiangensis [Reference Shpynov50], and R. mongolotimonae [Reference de Sousa51, Reference Psaroulaki52] are emerging (Table 1). This emergence may only be an artefact reflecting the wide application of molecular diagnostic techniques which have facilitated identification and characterization. There is evidence that SFG rickettsioses were initially misidentified by serology as R. conorii, the common pathogen of Mediterranean spotted fever [Reference Fernandez-Soto, Encinas-Grandes and Perez-Sanchez49, Reference Beninati53]. Ticks may serve as vectors, reservoirs and/or amplifiers for most of these new species. Vertebrates are bacteraemic for short periods and whether they can serve as reservoirs is still under discussion [Reference Fernandez-Soto, Encinas-Grandes and Perez-Sanchez49, Reference Sreter-Lancz54].

Novel geographical locations have been noted for vectors and hosts of rickettsial species. R. slovaca, originally isolated from ticks in Slovakia, is now recognized as a human pathogen in France [Reference Fournier47, Reference Di rique Gouriet, Rolain and Raoult55]. More recently R. slovaca and R. helvetica were the first recognized rickettsioses in Scandinavia [Reference Nielsen45]. Although the reasons for this geographical expansion are unclear, the role of both migrating birds and tick-infested dogs imported into Northern European areas cannot be underestimated [Reference Jaenson56]. Recently rare rickettsial species such as R. mongolotimonae have been associated with human disease in the Mediterranean area [Reference de Sousa51, Reference Psaroulaki52]. The burden of tick infestation with SFG rickettsiae is rising and this, together with the currently observed expansion of the tick vectors' range and geographical distribution in Europe [Reference Punda-Polic44Reference Fournier46Reference Punda-Polic44Reference Fournier46, Reference Fernandez-Soto, Encinas-Grandes and Perez-Sanchez49, Reference Shpynov50, Reference Beninati53] suggests an increased risk for human infection (Tables 2 and 3).

VIRAL INFECTIONS

Crimean-Congo Haemorrhagic Fever (CCHF) virus

CCHF infection, genus Nairovirus, family Bunyaviridae, is widespread in Africa, Asia, Middle East and East Europe. CCHF has a fatality rate up to 17%, which can be even greater in nosocomial outbreaks. The infection is transmitted by ixodid ticks, e.g. Hyalomma marginatum, Rhipicephalus rossicus, Dermacentor marginatus or by body fluids from viraemic hosts, e.g. humans or livestock [Reference Papa57Reference Yashina62] (Table 1).

Outbreaks of CCHF have been reported between 2000 and 2006 from South-Eastern Europe – in Bulgaria in 2002 and 2003 [Reference Papa57], in Albania and in Kosovo in 2001 [Reference Papa58, Reference Papa59] with still undefined reservoirs. Social disruption, conflict, or war were major factors [Reference Papa57Reference Papa59].

An outbreak in Turkey began as increased activity of the infection in 2002. Up to until 2005 about 500 cases were reported to the Turkish Ministry of Health. Twenty-six of these cases died. The virus was transmitted via tick bite or contact with blood or other infected tissues from viraemic livestock [Reference Ergonul60]. This CCHF outbreak in Turkey may be attributed to the milder climate reported during April in the year preceding the outbreak [Reference Ergonul60] (Tables 2 and 3).

In genetic analyses, strains from Bulgaria were similar to others from Albania, Kosovo, European (South West) Russia and Turkey. However, a great divergence was seen between these virus strains and the non-pathogenic AP 92 strain from Greece, and strains from Asia and Africa [Reference Papa57, Reference Ergonul60Reference Yashina62].

Hantavirus

The main Hantaviruses, genus Hantavirus, family Bunyaviridae, seen in Europe, are Dobrava-Belgrade and Puumala. They are associated with haemorrhagic fever with renal syndrome (HFRS) whereas Seoul virus causes a mild HFRS, with worldwide distribution, but without reported clinical disease in Europe thus far. The main mode of transmission is via inhalation of aerosols from excreta of persistently infected rodents. High-risk groups include farmers, forestry workers, and individuals in close contact with wildlife [Reference Lundkvist63Reference Olsson65] (Table 1).

Dobrava-Belgrade virus has been reported as a cause of severe HFRS in the Balkans [Reference Markotic64, Reference Pal, Strle and Avsic-Zupanc66] and Russia [Reference Lundkvist63]. Puumala virus on the other hand causes a milder disease, called nephropathia epidemica, and has been described in Western Russia [Reference Alexeyev67], Scandinavia [Reference Olsson65], Western Europe, including France [Reference Sauvage68] Germany [Reference Mailles69], and the Balkans (excluding the Mediterranean region) [Reference Cvetko70]. The coexistence of the two viruses in the Balkans [Reference Markotic64, Reference Cvetko70] might lead to exchange of genetic material and emergence of new viral subtypes.

An increased incidence has been recently seen in Central and Northern European countries, including Belgium, France, Germany [Reference Mailles69], Finland [Reference Rose71], and Luxembourg [Reference Schneider and Mossong72]. During the first quarter of 2005 the incidence in parts of Belgium and France rose to 5·5 and 13·8/100 000 population respectively [Reference Mailles69]. The first human case in Austria was reported in February 2006 [Reference Hoier73]. A large outbreak of more than 10 000 cases of Puumala virus-induced HFRS was identified in 2004 in the European region of Russia with an annual incidence of 124/100 000 in the Udmutria Republic and a case-fatality rate of about 1% [Reference Garanina74].

Novel endemic areas were recognized in Croatia during the 2002 Puumala virus outbreak that followed war conflicts, abandonment of human settlements and uncontrolled rodent population expansion (Table 3) [Reference Cvetko70].

The emergence of these viruses has been attributed to ecological changes of the rodent reservoir habitats, the milder climate in Northern Hemisphere and altered human behaviour patterns (Table 1) [Reference Olsson65, Reference Cvetko70, Reference Rose71, Reference Lindgren and Gustafson75]. However, increased awareness among physicians and better access to Hantavirus testing may account for the increase in registered Hantavirus infections in Europe [Reference Mailles69].

Sandfly fever viruses (Toscana, Naples, Sicilian)

Sandfly fever viruses belong to genus Phlebovirus, family Bunyaviridae. They are transmitted in the Mediterranean area by the sandflies Phlebotomus perniciosus and P. perfiliewi. Naples and Sicilian sandfly fever viruses cause mild self-limiting disease of unknown epidemiology. Toscana virus is the third most frequent cause of aseptic meningitis between May and October in Central Italy, where it was originally isolated from sandflies in 1971 (Table 1). Toscana virus has since been detected in France [Reference Peyrefitte76], Spain [Reference Sanbonmatsu-Gamez77], Slovenia, Greece, Cyprus, Turkey and other European countries [Reference Hemmersbach-Miller78, Reference Charrel79] (Table 3). In all Northern Mediterranean countries Toscana virus should be included in the differential diagnosis of viral meningitis during the warm season. Entomological studies may provide a better estimation of the variety of vectors, their geographic distribution, and the disease potential for further spread (Table 2) [Reference Sanbonmatsu-Gamez77, Reference Charrel79].

Tick-borne encephalitis virus (TBEV) group

The TBEV group, genus Flavivirus, family Flaviviridae, is a complex of closely related viruses affecting the central nervous system (Table 1). Importantly, several other viral species including those belonging to the genus Bunyaviridae and Togaviridae can be involved in the syndrome of tick-borne encephalitis (TBE). The TBEV group includes the European subtype, widely distributed in Europe and transmitted by I. ricinus ticks, and the Far-Eastern and Siberian subtypes, present from the Far East to Baltic countries and transmitted by I. persulcatus ticks [80]. Recently, foodborne outbreaks of TBE linked to consumption of unpasteurized goats' and cows' milk have been reported in Lithuania, Latvia and Estonia [80, Reference Kerbo, Donchenko and Kutsar81].

Cases of TBE have been recorded focally throughout Central and Eastern Europe and Scandinavia [80, Reference Beran82]. During the last 5 years an increasing incidence has not only been noted in most Central European countries [Reference Beran82, Reference Strauss83] but has also spread to European areas previously considered free of disease, e.g. Norway [Reference Csango84]. Latvia and neighbouring Finland (especially the Aland island area where annual incidence was 100/100 000 population in 2001) [Reference Strauss83], areas in Russia and the Czech Republic [80] show very high incidences whereas in Austria a significant decrease occurred after a specific immunization programme [80].

It could be speculated that recent climatic changes and global warming may change the transmission dynamics of the TBE viruses [Reference Csango84] and the TBE risk area may enlarge even more in landscape types suitable for leisure and recreational activities [Reference Daniel85]. The TBE viruses are maintained in nature in a cycle involving permanently infected ticks and wild vertebrate hosts. The viruses are transmitted horizontally between vectors and vertebrates especially from spring to autumn with small mammals serving as reservoirs of the virus [Reference Jaenson86]. I. ricinus, the principal tick vector involved in the transmission of the European subtype in Central Europe is found in microhabitats with high humidity and moderate temperatures. Temperature patterns during the year determine the altitude above sea level (a.s.l.) where there is high risk for a tick bite. A study of the popular resort area, Sumava Mountains in the Czech Republic (a region that borders the Czech Republic, Germany and Austria), revealed that I. ricinus habitats have reached 1000–1100 m a.s.l. compared to 700 m a.s.l. during the previous decade (Table 3). Human cases have already been reported from the Sumava Mountains area at altitudes as high as 900 m a.s.l. [Reference Daniel85, Reference Daniel87] (Table 3). TBE is a growing concern in Europe but case definition and notification schemes are not yet uniform and may affect the estimated prevalence of the disease focally (Table 2) [Reference Stefanoff88, Reference Gunther and Lindquist89].

West Nile virus (WNV)

WNV is a member of the genus Flavivirus, family Flaviviridae (Table 1). The virus is transmitted mainly by mosquito bites [Reference Murgue90]. Before 2000, it was enzootic in Africa, Europe, and Asia where it was maintained in natural cycles between birds and mosquitoes [Reference Murgue90]. Large outbreaks occurred in the European countries of Romania in 1996 [Reference Hubalek and Halouzka91] and Russia in 1999 [Reference Platonov92]. Human and equine WNV infections have recently been described in France [Reference Del Giudice93, Reference Zeller and Schuffenecker94] and Portugal [Reference Connell95].

Phylogenetic analyses have shown that WNV strains from France 2000 (horse), Tunisia 1997 (human) and Kenya 1998 (mosquito) belong to same genetic lineage possibly indicating the circulation of the virus along migratory bird routes in Europe [Reference Reed9, Reference Charrel96]. Similarly, it is thought that a strain closely related to the Israel strain first identified in 1951 [Reference Murgue90] was transferred by migratory birds to New York, where it triggered a human outbreak of WNV encephalitis in late 1999. This was the first documented occurrence of this virus in the Western Hemisphere [Reference Hayes97].

New European areas are affected by expanding vector and vertebrate hosts [Reference Charrel96Reference Autorino98]. Moreover, novel viral strains closely related to WNV (initially identified as WNV), and characterized with molecular techniques [Reference Bakonyi99], are now present in Central Europe and southern Russia [Reference Bakonyi99]. As the genetic evolution of WNV continues to be observed this virus remains an important public health threat (2 and 3) [Reference Beasley100].

Sindbis virus

Sindbis virus, genus Alphavirus, family Togaviridae, was first isolated in 1952 [Reference Kurkela101] causing a rash and fever-related arthritis called Pogosta disease in Finland, Ockelbo disease in Sweden and Karelian fever in European Russia (Table 1). A higher than expected seroprevalence (including children) has been recently shown in Finland [Reference Laine102] (Table 3). The disease is mild or asymptomatic in children causing underestimation of the problem. Northern European strains are genetically similar to each other [Reference Kurkela101] and to African strains [Reference Laine102], indicating transfer by migratory birds (Table 2) [Reference Laine102].

Highly pathogenic avian influenza A/H5N1 (HPAI)

The recent wide geographical spread of the virus [Reference Editorial103] is attributed to its apparent carriage by migratory birds [Reference Reed9, Reference Liu104] from Asia to Europe and now to Africa [Reference Ducatez105], the expansion of host range in other mammals as well as the increased risk for human infection especially for persons involved in commercial poultry farming [Reference Coulombier and Ekdahl106]. Suspected human cases were identified in Europe based on epidemiological criteria [Reference Quoilin107] and confirmatory testing was positive in Turkey without evidence of human-to-human transmission (Table 1) [108]. In Turkey severe weather conditions forced people into closer contact with their domestic birds with subsequent increased human exposure to the virus [Reference Giesecke109].

The conditions for zoonotic transmission of avian influenza will probably not be found in most other parts of Europe (excluding the influenza pandemic). HPAI is a global threat and its presence has increased awareness about a potential influenza pandemic [Reference Coulombier and Ekdahl106] (Table 3). Pre-pandemic planning and response activities are necessary for all countries around the world especially those with poor resources (Table 2).

New variant Creutzfeldt–Jakob disease (vCJD)

vCJD was initially recognized in 1995–1996 in several patients from the United Kingdom and one from France [Reference Will110Reference Chazot112] (Table 1). There are questions regarding its pathogenesis [Reference Colchester and Colchester113]. It is primarily considered as foodborne and is associated with the zoonotic epidemic of bovine spongiform encephalopathy (BSE). Any patient that has had a cumulative residence of 6 months or more in the United Kingdom during the period from 1980 to 1996 is considered at risk [Reference Collinge114, Reference Ward115]. Several controversial issues regarding vCJD exist, e.g. the percentage of the population exposed to BSE-contaminated beef during that period and the contribution of the still unknown co-factors in the pathogenesis of the disease [Reference Ward115].

An international network reports surveillance data for vCJD cases (Table 2). Current data (up to 17 November 2006) of patients with vCJD that have died include 156 cases in Britain, 19 in France, three in Ireland, two in The Netherlands, and one each in Italy and Spain; extending the list of affected countries [116] (Table 3).

Future predictions about at-risk populations are difficult to make. In the United Kingdom where the vCJD epidemic was first recognized, annual incidence is not increasing and it is thought that only a few cases will occur during the next years [116, 117]. However, it cannot be excluded that the limited outbreak experienced from 1996 to today may be followed by another. The emergence of transfusion-associated vCJD, i.e. two cases from the United Kingdom, caused the initiation of stricter measures for the reduction of risk associated with blood transfusions [Reference Llewelyn118Reference Ludlam and Turner121].

PARASITIC INFECTIONS

Trichinellosis

Most trichinella infections worldwide are attributed to Trichinella spiralis which parasitizes domestic animals. Rarely can they be associated with other parasite species such as T. britovi and T. nativa that mainly infest wildlife (Table 1).

Trichinella spp. are transmitted directly by ingestion of infective larvae through consumption of undercooked meat. Only thoroughly cooked meat is safe for consumption, whereas smoking, salting and drying are unreliable as meat processing techniques. Industrialized pig farming and meat inspection have prevented endemic trichinellosis caused by T. spiralis in Western Europe. However inadequate inspection is implicated in outbreaks after 2000 in Lithuania and Latvia where the annual incidence is 0·6 and 0·7–1/100 000 population respectively (Table 2) [Reference Perevoscikovs122, Reference Bartuliene, Jasulaitiene and Malakauskas123].

Horse meat consumption was implicated in T. spiralis outbreaks in France and Italy [Reference Pozio124]. Socioeconomic changes are well known to be associated with peaks in the incidence of the disease [Reference Ozeretskovskaya125] – as recently in Serbia [Reference Djordjevic126]. T. britovi is an emerging pathogen in free-range domestic pigs which may feed on rodents infected with the parasite. The parasite's presence is maintained in sylvatic cycles involving wild pigs, foxes and rodents of the same habitat as is the case in Spain [Reference Cortes-Blanco127] and France [Reference Gomez-Garcia, Hernandez-Quero and Rodriguez-Osorio128]. Infection originating from wildlife is emerging, as hunting and consumption of raw meat are becoming more popular, e.g. in France (Table 2) [Reference Gari-Toussaint129].

Recently another species, Trichinella pseudospiralis, a cosmopolitan non-encapsulated species has been detected in Sweden [Reference Pozio130] and in pigs, rats and a cat in a farm in Slovakia [Reference Hurnikova131] (Table 3). Raptorial migrating birds that are well-known hosts of T. pseudospiralis introduced the parasite into this area which serves as a crossing of Pan-European bird migration routes from Europe and northern Asia in autumn and spring (Table 2) [Reference Hurnikova131].

Alveolar echinococcosis

Alveolar echinococcosis (alveolar cyst disease), endemic in Northern Central Europe and the Arctic region, is caused by the small tapeworm Echinococcus multilocularis carried by its terminal hosts, e.g. foxes, dogs, wolves, that shed the parasite's eggs in their faeces (Table 1). It is transmitted through consumption of infected raw or undercooked food containing eggs of the parasite. Humans serve as inadvertent intermediate hosts. The water vole is the principal intermediate host in Central Europe along with more than 40 species of rodents. The prevalence of the parasite is increasing in rodents that spillover the organism to other animal species, e.g. beavers [Reference Janovsky132], wild boars [Reference Boucher133] or wolves [Reference Martinek134]. Parasite eggs have been detected in 47·3% of excreta from red foxes in the city and 66·7% from red foxes in the adjacent recreational areas, which also migrate eastwards as a result of their population expansion [Reference Hofer135Reference Deplazes138]. Interestingly the population of both water voles and red foxes is increasing as a result of ecological changes (voles) and institution of animal anti-rabies vaccination programmes (foxes) [Reference Sreter136Reference Deplazes138]. Furthermore, the infection has been now transmitted to domestic dogs and cats that comprise a permanent source of human infection near dwellings [Reference Deplazes138, Reference Deplazes and Eckert139] (Table 3).

In Europe up to 2000, 559 human cases were verified (Table 1) [Reference Kern140]. As the incubation time is thought to be anywhere from 5 to 15 years the limited number of sporadic human cases after 2000 is not a reassuring finding. The high annual incidence in particular regions [Reference Kern140], the spread of the parasite sylvatic cycle in other meadow ecosystems and the expansion to other animal hosts indicate a possible spread of the infection and underestimation of the problem (Table 2). Currently a surveillance scheme has been established with participation from 12 European countries, the European Echinococcosis Registry [Reference Kern140].

Other

Although not among the emerging zoonoses, brucellosis and visceral leishmaniasis had a significant impact on the endemic European countries.

Brucellosis is endemic in most Southern European countries, with sporadic outbreaks, but the impact on humans has not increased since 2000. The epidemiological trends vary slightly according to the strictness of the preventive measures especially the ones concerning dairy products [Reference Mendez Martinez141] and imported cases from endemic to non-endemic European countries offer a diagnostic challenge [Reference Al Dahouk142].

Visceral leishmaniasis (VL) due to Leishmania infantum is a zoonotic disease, endemic in Southwest Europe where the predominant vector is the sandfly Phlebotomus perniciosus and the main reservoir of infection is dogs. HIV patients are more susceptible to the infection, but there was a fall in the proportion of cases of HIV/VL co-infection after 1996 following the introduction of highly active antiretroviral therapy [Reference Malik143, Reference Desjeux and Alvar144]. Eighty-five percent of these co-infections originate from Southwest Europe, 71% of them affecting intravenous drug users [Reference Malik143Reference Gabutti145]. In the last decade, the disease has been stable in Europe except for an increasing shift from rural areas to suburbs where dogs are present and small gardens offer refuge to the vector [146]. New zoonotic foci of canine leishmaniasis have been detected in the northwest of Italy, without an increase in the incidence of the human disease [Reference Ferroglio147, Reference Paradies148]. Climatic changes in the future could modify the geographical distribution, rendering surveillance for vector spread necessary even in the absence of established increasing impact for humans in Europe from 2000 to the present.

DISCUSSION

Several bacterial, viral and parasitic zoonoses affecting humans have emerged in the last 6 years in Europe by strictly defined criteria. The phenomenon may be associated with social, ecological, technological and microbial risk factors which act synergistically to facilitate emergence of such pathogens in Europe.

Social factors include human mobility especially with air travel, tourism and outdoor activities, permanent residence in rural areas, food habits, international commerce, war and political conflicts.

Concerning ecological factors it is probable that milder climate (global climatic change) may be followed by a northern shift in the distribution of major disease vectors, i.e. ticks and mosquitoes [Reference Lindgren and Gustafson75, Reference Lindgren, Talleklint and Polfeldt149]. A milder winter, earlier arrival of spring and/or late arrival of the following winter permit prolonged seasonal tick activity and hence pathogen transmission, a general increase in vector and mammal populations and changes in the migration patterns of animals and birds. However, more research is necessary to investigate and identify the effect of climate changes on emerging infectious diseases [Reference McMichael, Woodruff and Hales150]. The ecological changes may act in combination with social factors to increase the chance that a communicable disease emerges, e.g. recent emergence of arthropod-borne infections like TBEV group encephalitis, Lyme borreliosis and anaplasmoses [Reference Lindgren and Gustafson75, Reference Lindgren, Talleklint and Polfeldt149].

Microbiological factors contribute to disease spread and emergence into new territories, e.g. the evolution noted in WNV and Avian influenza A(H5N1).

Technological factors may contribute to the false sense of ‘emergence’ of such diseases. These include the enhanced diagnostic techniques including newer molecular methods that facilitate the isolation and characterization of emerging pathogens as well as the increased awareness of physicians with careful case-history recording and laboratory investigation leading to subsequent correct diagnosis and reporting. Tularemia historically could have remained unrecognized as it affected a limited number of humans. As a potential bioterrorist weapon it received increased awareness among physicians followed by increased research funding, enhanced diagnostics and vigilant surveillance systems. Furthermore, the surveillance of emerging zoonotic diseases in the European countries is not uniform. Uniform harmonized case definitions and laboratory assays should be introduced in all European countries; as an example the true prevalence estimates for TBE might be affected by case definition restrictions [Reference Stefanoff88]. Notification for the majority of these diseases is not mandatory, it is based on voluntary laboratory reporting schemes leading to underreporting. Consequently, it is possible that enhanced monitoring and optimized diagnostics may account for the observed emergence in certain geographic locations.

A potentially valuable tool in the accurate estimation of the prevalence and incidence of these pathogens might be the performance of virological investigation of their vectors and seroepidemiological surveys regarding their human reservoirs and their animal hosts. Animal serological data can be used to identify novel zoonotic foci and assist in predicting human outbreaks. Long-term surveillance of natural foci in endemic regions provides useful information on the activation of zoonoses and may provide a marker for future outbreaks. This permits timely epidemiological prognosis and institution of preventive measures. In that respect it is necessary to highlight the need to train young people in disciplines such as entomology and wildlife biology.

In conclusion, 15 zoonotic and vector-borne agents were identified as emerging threats with a public health impact for humans in Europe for the period from 2000 to August 2006. National and regional public health sectors should give priority to surveillance systems and enhanced diagnostics regarding these emerging pathogens. A broad collaboration among clinicians, public health workers, veterinary medicine and veterinary public health officials is necessary for prompt response strategies ensuring the prevention and management of such infections.

DECLARATION OF INTEREST

None.

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Figure 0

Table 1. Emerging zoonoses and vector-borne diseases in Europe: pathogens, main modes of transmission, and recent data on human cases or outbreaks in European countries from 2000 to August 2006

Figure 1

Table 2. Risk factors for the emergence of zoonoses and vector-borne diseases in Europe from 2000 to August 2006

Figure 2

Table 3. Criteria for emergence of the identified zoonoses and vector-borne diseases in Europe from 2000 to August 2006