Veterinary Parasitology 163 (2009) 298–305

Emerging arthropod-borne diseases of companion animals in Europe

Frederic Beugnet a,*, Jean-Lou Marie b

a Meria Animal Health, 29 Av T.Garnier, 69007, Lyon, Franceb Direction du Service de Sante des Armees, BP 80, 83800 Toulon armees, France

A R T I C L E I N F O

Keywords:

Arthropod-Borne Diseases

Cats

Dogs

Epidemiology

Ticks

A B S T R A C T

Vector-borne diseases are caused by parasites, bacteria or viruses transmitted by the bite

of hematophagous arthropods (mainly ticks and mosquitoes). The past few years have

seen the emergence of new diseases, or re-emergence of existing ones, usually with

changes in their epidemiology (i.e. geographical distribution, prevalence, and pathogeni-

city). The frequency of some vector-borne diseases of pets is increasing in Europe, i.e.

canine babesiosis, granulocytic anaplasmosis, canine monocytic ehrlichiosis, thrombo-

cytic anaplasmosis, and leishmaniosis. Except for the last, these diseases are transmitted

by ticks. Both the distribution and abundance of the three main tick species, Rhipicephalus

sanguineus, Dermacentor reticulatus and Ixodes ricinus are changing. The conditions for such

changes involve primarily human factors, such as travel with pets, changes in human

habitats, social and leisure activities, but climate changes also have a direct impact on

arthropod vectors (abundance, geographical distribution, and vectorial capacity). Besides

the most known diseases, attention should be kept on tick-borne encephalitis, which

seems to be increasing in western Europe, as well as flea-borne diseases like the flea-

transmitted rickettsiosis. Here, after consideration of the main reasons for changes in tick

vector ecology, an overview of each ‘‘emerging’’ vector-borne diseases of pets is presented.

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1. Introduction

Vector-borne diseases are caused by parasites, bacteriaor viruses transmitted by the bite of hematophagousarthropods (mainly ticks and mosquitoes). Their manage-ment requires a multidisciplinary approach, especially asthe majority of these diseases are zoonotic (Parola et al.,2005). The past few years have seen the emergence of newdiseases, or re-emergence of existing ones, sometimeswith changes in their epidemiology (i.e. geographicaldistribution, prevalence, and pathogenicity) (Shaw et al.,2001). It appears that the frequency of some vector-bornediseases is increasing in Europe, and that pathogens arecirculating more easily. This is driven largely by humanfactors. Climate change, especially global warming, can

* Corresponding author. Tel.: +33 4 72 72 55 60; fax: +33 4 72 72 32 98.

E-mail address: frederic.beugnet@merial.com (F. Beugnet).

0304-4017/$ – see front matter � 2009 Elsevier B.V. All rights reserved.

doi:10.1016/j.vetpar.2009.03.028

also affect arthropod vector density, geographical dis-tribution and vectorial capacity. In the last 10 years, ‘‘new’’diseases have been reported in horses and carnivores, e.g.babesiosis in northern Germany and The Netherlands,canine monocytic ehrlichiosis (CME) in southern Europe,Anaplasma platys anaplasmosis in France, and A. phagocy-

tophilum anaplasmosis in cattle, horses, dogs and cats innorthern Europe.

Various factors have been linked to the changingepidemiology of vector-borne disease. Transport by air,sea, train, and road has dramatically increased over the lasttwo decades, with intense movements of productionanimals but also sport and companion animals. Thesemovements provide ideal conditions for the circulation ofpathogens. Increasing holiday entitlement and travel toever more distant locations promote pathogen exchanges,especially when pets are travelling with their owner. Forinstance, more northern Europeans go to Spain, Italy, andFrance during the summer, and their pets then return with

Table 1

Importation of pathogens into the UK through the Pet Travel Scheme

(PETS) or quarantine (from Shaw et al., 2003).

Blood samples from 67 dogs were submitted for PCR testing; 53 dogs

had entered the UK under PETS and 14 dogs were currently in

quarantine between April 2001 and July 2002.

In dogs entering under PETS 32% were carrying at least

one pathogen

29% had babesiosis

2.3% had monocytic ehrlichiosis

11% had leishmaniosis

Of the dogs released

from quarantine

50% were carrying at least

one pathogen

20% had babesiosis

36% had monocytic ehrlichiosis

9% had leishmaniosis

F. Beugnet, J.-L. Marie / Veterinary Parasitology 163 (2009) 298–305 299

leishmaniosis, ehrlichiosis, babesiosis, or heartworm. Theimportation of new diseases has been documented in theUK following introduction of the Pet Travel Scheme, whichallows pet owners to travel to continental Europe withtheir dogs or cats (Table 1). Landscape changes such as thecreation of recreational parks facilitates the establishmentof tick populations close to human habitation and,potentially, exposure to diseases such as Lyme borreliosis.Open-air activities such as trekking, mountain biking orjogging also increase the risk of being bitten, while thedevelopment of large suburban areas with private gardensalso provides a niche for arthropod vectors (e.g. ticks,mosquitoes, and biting flies) and peri-domestic hosts(rodents). In other parts of the world, dams and artificial

Table 2

Summary of surveys for ticks, fleas and arthropod-borne diseases in France fro

Pathogen Percentage PCR positiv

Dogs (n = 632)

(a)

Babesia 4%

Borrelia burdorferi sl 0%

Haemoplasma (anc. Haemobartonella)

Ehrlichia or Anaplasma 0.15%

Pathogen Percentage PCR positive

Ixodes Derma

(b)

Babesia canis 0% 6%

Babesia vogeli 0% 0%

Babesia odocoilei 8% 0%

Borrelia burgdorferi sl 2.8% 0%

Anaplasma phagocytophilum 4% 0%

Ehrlichia canis 0% 0%

Rickettsia 23% including non-pathogenic species 20% in

(a) Results from PCR survey of dogs and cats for vector-borne diseases in the Prov

in 2001–2002 (Beugnet et al., 2003; Clement-Sailhac, 2003; Savary de Beaureg

infection by vector-borne pathogen based on febrile syndrome. (b) The percentag

(n = 51) in veterinary clinics in East and Central France (Rhone-Alpes and Auver

(Halos et al., 2005; Marotel, 2006; Vayssier-Taussat et al., 2005).

lakes can create conditions favourable for disease vectors.Measures to protect wild fauna, combined with landrehabilitation and management practices, particularly inforestry, have contributed to the proliferation of red androe deer, wild boar and foxes, which are all hosts forhematophagous arthropods acting as vectors of pathogens.

Variations in temperature and humidity can have rapideffects on arthropod populations including fleas, ticks,mosquitoes, sandflies, and Culicoides. Climatic changesbeyond simple increases in mean temperature can alsoaffect vector abundance and distribution. Global warmingis associated with unstable weather conditions and acutephenomena such as rain, floods, storms, etc., which canimprove local conditions for vector populations. Perhapsmost important is the change in seasons, with reduction ofthe classic winter period, allowing ticks, for example, to beactive all year round over an increasing area.

2. Changes in tick populations

Altered geographical distribution, as well as density andperiod of activity of ticks, could underlie changes in vector-borne disease. Two surveys in France (Table 2) showed thepresence of the three main tick species as well as theirpathogens, highlighting how tick distribution has changed.The data suggest that Rhipicephalus sanguineus has tendedto move north from its previously Mediterranean dis-tribution, probably being transported on carnivores. Thistick is now described all over France, in Belgium, Germanyand The Netherlands. Dermacentor reticulatus is recordedin almost all European countries but formerly was

m 2001 to 2004.

e

Cats (n = 243) Ticks (n = 214)

0% 24%

Ixodes: 6.9% (B. odocoilei)

Dermacentor: 13.3% (B. canis)

Rhipicephalus: 6.33% (B. vogeli)

0% 0%

26.4%

0% 16.5%

Ixodes: 25.9%

Dermacentor: 0%

Rhipicephalus: 19%

centor Rhipicephalus

0%

4%

0%

0%

0%

0%

cluding non-pathogenic species 17% including non-pathogenic species

ence-Cote d’Azur and Languedoc Roussillon regions of the south of France

ard, 2003), at least half the animals were included because of suspected

e of 520 ticks collected in 2003–2004 in a survey of dogs (n = 377) and cats

gne regions) that were positive for a range of pathogens in a PCR survey

F. Beugnet, J.-L. Marie / Veterinary Parasitology 163 (2009) 298–305300

relatively rare in cold continental climates (central andnorthern Europe). It is believed to be spreading now inthese areas (Poland, northern Germany, The Netherlands,Denmark), enabling the establishment or increase ofcanine babesiosis. The spread of Dermacentor ticks isthought to be linked to importation and climate changes,notably the shortening of the winter period and increasingminimum temperatures. Ixodes ricinus is distributed allover Europe, except in the Mediterranean zone where it istoo warm and dry except at altitude. The density of Ixodes

ticks appears to have increased in some areas, which couldlead to a higher risk of pathogen transmission. Changes intick density may be related to increases in host popula-tions, e.g. rodents, wild boars and wild ruminants, inEuropean forests.

3. Enzootic arthropod-borne diseases

Certain arthropod-borne diseases like canine monocyticehrlichiosis, leishmaniosis and dirofilariosis are enzootic insouthern Europe. With the exception of imported cases,dirofilariosis appears to have remained epidemiologicallystableinmostofEurope.Nevertheless,aclear extensionof itsgeographical distribution has been demonstrated in Italyand new models indicate an increase of the possibility oftransmission by mosquitoes in northern Europe (Rinaldiet al.,2006;Mortarino etal.,2008).Leishmaniosis has tendedto move north, an extension that could be related to humanactivities especially the rehabilitation of old houses andstone walls in villages in France, Spain and Italy, creatingfavourable areas for the sandfly vector. Regarding CME, dueto the geographical extension of R. sanguineus all overcontinental Europe, there is a trend for extension towardsnorthern countries, e.g. northern France and Belgium. Thefirst autochtonous cases have been identified in TheNetherlands in spring 2008 (F. Jongejan, Utrecht University,pers. com., June 2008). For the same reason, the thrombo-cytic ‘‘ehrlichiosis’’ due to A. platys, transmitted by R.

sanguineus, appears to be more frequently diagnosed. Afew cases have been described recently in France in the areaof Lyon (L. Chabanne, Veterinary School of Lyon, pers. com.,July 2008).

The presence of the European dog tick D. reticulatus allover continental Europe allows transmission of caninebabesiosis (Babesia canis canis) in most countries. Babesiosis(piroplasmosis) is highly endemic in France, Switzerland,Hungary, Serbia, Croatia, northern Italy and northern Spainbut it was traditionally less common in Belgium, Germany,Poland and The Netherlands. Since 2000, there has been aclear extension in those countries, with establishment inThe Netherlands in 2005 and a clear movement from thesouth (Bavaria) to the north in Germany. Babesiosis causedby Babesia canis vogeli, transmitted by Rhipicephalus,remains less common. Babesiosis caused by small Babe-

sia/Theileria has been described in southern countries(Spain, Italy, Greece) but seems to remain sporadic.

4. Emerging tick-borne diseases

In terms of emerging diseases of pets, recent attentionhas focused on some other tick-borne diseases (anaplas-

mosis and tick-borne encephalitis) and some flea-bornediseases (bartonellosis, haemoplasmosis and rickettsiosis).

4.1. Tick-borne encephalitis virus

Tick-borne encephalitis (TBE) is, like yellow fever ordengue, caused by a flavivirus, and is an importantinfectious disease in many parts of Europe, the formerSoviet Union, and Asia. Initially described in humans inAustria, TBE has rapidly become a growing public healthproblem in Europe (Haglund, 2002). Two subtypes of TBEvirus are usually recognized, the western variant inoccidental and central Europe and the eastern variant, inthe Far East, which is much more virulent. I. ricinus isresponsible for the spread of TBE western subtype virus inoccidental and central Europe, but fortunately the geo-graphical distribution of TBE is more restricted than that ofits vector. Recent foci of human TBE have been reported innorth and central Italy, Greece, Denmark, Norway, and thesouthern part of Sweden (reviewed in Pugliese et al., 2007).In addition, the incidence of human TBE rose dramaticallyin a number of countries. For example, between 1974 and2003, incidence increased by 1033% in Lithuania and 574%in Germany (Suss et al., 2006). In Sweden, the increase inTBE incidence since the mid-1980s was related to milderwinters and early arrival of spring, responsible for anorthward extension of I. ricinus and a general increase intick density (Lindgren and Gustafson, 2001). Trans-ovarialand trans-stadial transmission have been proven in Ixodes

spp. ticks, therefore ticks act as both vector and reservoirfor the virus (Suss, 2003).

Human cases of TBE tend to occur during the highestperiod of tick activity, mainly between April and Novem-ber. After an incubation period of 7–14 days, the typicalclinical picture is characterized by a non-specific influ-enza-like syndrome followed by an asymptomatic intervaland a second stage of the disease with at least four clinicalmanifestations of different severity: meningitis, menin-goencephalitis, meningoencephalomyelitis, meningoradi-culoneuritis (Haglund and Gunther, 2003). In Germany,during the period 1991–2000, 1500 patients were diag-nosed with symptomatic infection of TBE and neurologicmanifestations were described in 47% of the cases with anestimated mortality rate of 1% (Pugliese et al., 2007).

In dogs, TBE may induce febrile syndrome andencephalitis as in humans. The infection can be peracuteand lethal, as well as subacute and chronic (Leschnik et al.,2002). In the Czech Republic, 5 dogs out of 151 sampled inan endemic focus were found seropositive (IFA) for TBE andshowed symptoms of meningoencephalitis or encephalitis(Klimes et al., 2001). In a study performed on horse serafrom a German area endemic for TBE, 2.9% (7/240) werefound positive, using a seroneutralization technique(Muller et al., 2006). Given the increase of TBE cases inhuman, we can predict that TBE will be more frequentlydiagnosed in dogs as well as in horses in the future.

4.2. A. phagocytophilum

This Ehrlichia-like organism has been known since the1930s as the agent of tick-borne fever in Scottish sheep and

F. Beugnet, J.-L. Marie / Veterinary Parasitology 163 (2009) 298–305 301

recognized since the 1950s as the agent of pasture fever incattle in England. The disease was later identified in mostEuropean countries where it contributes to considerableproductivity losses in dairy cattle. A. phagocytophilum wasreported in dogs from Switzerland and Sweden in the late1980s. The first case of human granulocytic ehrlichiosiswas described in the USA in 1994 (Chen et al., 1994) andthe disease emerged in Europe in 1997. Thanks tomolecular phylogenetic studies, all these agents, as wellas Ehrlichia equi in horses, have been unified within a singlespecies named A. phagocytophilum (reviewed in Parolaet al., 2005), which includes genetic variants. The pathogenis transmitted to humans and animals through the bite ofIxodes spp. and induces a febrile syndrome associated withmyalgia, thrombocytopenia, leucopenia, and headache. InEurope, I. ricinus is the recognized vector of A. phagocy-

tophilum. It is prevalent from western Europe (with theexception of the Mediterranean area, except at altitude)through to central Asia, more particularly in a humidmicrohabitat in forests, forest edges, and pastures. InEurope, several studies have detected A. phagocytophilum

DNA in ticks. Prevalence in ticks in Germany, Switzerland,Austria, Scotland, Hungary, Estonia, and northeast Polandranged from 1.2% to 8.7% (Jensen et al., 2007).

In addition to the classic hosts (ruminants and rodents),other animals have been found to be infected, includingdogs and cats (Tozon et al., 2003). In Switzerland and in theUnited Kingdom, different rodent species have been shownto harbour A. phagocytophilum, and have been suggested aspotential reservoirs (Bown et al., 2003; Liz et al., 2000).Nevertheless, PCR analysis suggested that rodent infec-tions are generally short-lived and that ticks rather thanrodents may maintain the infection over the winter. Roedeer are thought to be competent reservoirs for A.

phagocytophilum and high seroprevalence was found inDenmark (95.6%), Norway (96%) and Slovenia (94%). Largervariations have been encountered in the number of PCR-positive roe deer, from 12.5% in Czech Republic to 85.6% inSlovenia. The proportion of roe deer being rickettsaemicalso varies seasonally (Skarphedinsson et al., 2005).Human granulocytic anaplasmosis (HGA) has beenincreasingly recorded: in the USA between 1997 and2001, 654 confirmed, 434 probable, and 3 suspect/unknown cases were reported (Parola et al., 2005). InEurope, the first documented case of HGA was reported inSlovenia in 1997 and by 2006, only 22 confirmed cases hadbeen described (Kowalski et al., 2006), in Slovenia, TheNetherlands, Spain, Sweden, Norway, Croatia, Poland, Italy,Austria and France. The majority of the cases occurredbetween June and August, coinciding with peak tickactivity as well as human activity in tick habitats.

Dogs are susceptible to infection. In an experimentalinfection of seven beagles in Sweden, the main clinicalfeatures appeared after 4–11 days of incubation and werehigh fever for 2–5 days and depression. All the dogsdeveloped an intensive thrombocytopenia, moderateleukopenia and a strong antibody response. Ehrlichialinclusions were detected in blood neutrophils from 4 to 14days after inoculation, for 4–8 days. Ehrlichial DNA couldbe detected by PCR during the parasitaemic stage (Egenvallet al., 1998). In addition to high fever, A. phagocytophilum

also includes apathy, anorexia, reluctance to move,lameness, diarrhoea or nervous symptoms. However, mildor subclinical infections are supposedly common. Thedisease in dogs is probably underdiagnosed, as the clinicalsigns may suggest Lyme borreliosis, thrombocytic ehrli-chiosis, canine monocytic ehrlichiosis or even babesiosis.Recently, the first clinical cases of A. phagocytophilum indogs were identified in France (unpublished data). Clinicalcases have also been described in dogs in Italy (Tarello,2005). In a study in Germany, 41.9% (26/62) of healthy dogswere found to be seropositive for A. phagocytophilum. Dogswith high tick infestation were significantly more seror-eactive than those with no or low tick infestation. Amonganother group of dogs with clinical signs compatible withthe infection, the seroprevalence level was not signifi-cantly different (44.9%, 22/49). In this later group, six dogs(12.2%) were also positive by PCR (Jensen et al., 2007).

The first case of feline granulocytic anaplasmosis wasreported in Sweden in 1999 (Bjoersdorff et al., 1999). Theanimal was presented for a 2-day history of lethargy,anorexia and tachypnoea. Clinical examination andlaboratory investigations revealed fever, dehydration,neutrophilia, lymphopenia, hyperglycaemia and intracy-toplasmic neutrophilic Ehrlichia inclusions, and the pre-sence of ticks. The diagnosis was confirmed by serology,PCR and DNA sequencing. Treatment based on doxycyclineled to complete recovery. In a large survey throughout theUSA, 4.3% (20/460) of cats were seropositive to A.

phagocytophilum (IFA) (Breitschwerdt et al., 2002). Inanother study carried out in the northeastern UnitedStates, where the agent is naturally more common, 30% ofcats were positive for A. phagocytophilum antibodies by IFA(Magnarelli et al., 2005).

The clinical signs of A. phagocytophilum infection inhorses include high fever, depression, partial anorexia,limb oedema, petechiae, icterus, ataxia and a reluctance tomove (Madigan and Gribble, 1987). The first case ofEhrlichia equi infection in an adult horse in France,confirmed by both serology and PCR, was reported in2002 (Bermann et al., 2002). In a recent survey in thenorth-west of France, 31% (45/144) of horses wereseropositive using an indirect immunofluorescence testbut in all cases PCR performed on whole blood from thesame animals was negative (J.L. Marie and B. Davoust,2008, unpublished data).

5. Emerging flea-borne diseases

Fleas are competent vectors for numerous microbialpathogens of medical and veterinary importance. Plague,murine typhus and cat-scratch disease are examples ofwell-known flea-transmitted diseases. Despite regularantiparasitic treatment of domestic carnivores, cat anddog fleas remain their most common ectoparasite (Table 3)(Gracia et al., 2008). There is an abundant literatureconcerning cat-scratch disease and other Bartonella infec-tions and there is some indication that these bacterialinfections are emerging in Europe or that their epidemiologyis changing (Rolain et al., 2003; Shaw et al., 2004; Boulouiset al., 2005). Similarly, there are publications worldwideconcerning infection of cats by Haemobartonella, now called

Table 3

Prevalence of flea infestation on pets in Europe.

Country Author Period Dogs Cats

Germany Beck et al. (2006) Annual average 5% 14.3%

Winter and Spring 3% 12%

Summer and Fall 8% 21%

UK Bond et al. (2005) July–August 7% 21%

Hungary Farkas et al. (2009) Annual average 16%a 22%

Winter 11.5% 18.8%

Summer 22% 33%

a 59% of the fleas infesting dogs were Ctenocephalides canis.

F. Beugnet, J.-L. Marie / Veterinary Parasitology 163 (2009) 298–305302

Mycoplasma (Haemoplasma) haemominutum or M. haemo-

felis, and of dogs by M. haemocanis. Prevalence of infection isusually high, from 20% to 40% or more (Tasker et al., 2003;Kenny et al., 2004). Pathogenicity is considered to be lowexcept in the case of co-infections, e.g. with FIV-FeLV in cats(Messik, 2004; Harrus et al., 2002). There are no dataregarding any recent changes in epidemiology.

5.1. Rickettsia felis

Recently, R. felis has emerged as a new pathogen inhumans, causing flea-borne spotted fever, also called catflea typhus. The bacterium was first detected in the cat flea,Ctenocephalides felis in 1990 by molecular techniques(Adams et al., 1990). Later, in 1994, DNA fragments of thisagent were detected in blood samples obtained from the

Fig. 1. The worldwide prevalence of Rickettsia felis (countries with positive report

star and the number reported cases given in red text). (For interpretation of the

version of the article.)

first human patient in Texas (Schriefer et al., 1994).Analysis of the 16S rRNA and citrate synthase genespositioned R. felis within the spotted fever group, in thesame clade as R. akari, R. australis, and R. helvetica (Azadet al., 1997). Based on the detection of DNA in fleas in anincreasing number of countries around the world, themajority of authors consider its distribution as wide as itsmain and cosmopolitan vector, Ctenocephalides felis (Fig. 1).R. felis has been detected in fleas in Europe including Spain,France, and the United Kingdom (Bitam et al., 2006; Gilleset al., 2008) (Table 4). In fleas, the prevalence can be veryhigh and varies according to the ecological environmentand season. Although C. felis is the main biological vectorfor R. felis, this bacterium has also been detected in C. canis,Pulex irritans, the human flea, and Archeopsylla erinacei

(reviewed in Bitam et al., 2006). Recently, R. felis was also

s indicated in blue text and countries with human cases indicated by a red

references to color in this figure legend, the reader is referred to the web

Table 4

Prevalence of Rickettsia felis in fleas using PCR in different countries.

Country/author Animal host Prevalence of R. felis in fleas

USA (Texas, Alabama, Maryland) Cats 67.4% (62/92)

Hawley et al. (2007) Analysis of pools of 1–14 fleas

United Kingdom Dogs and cats 23.3% (21/90) in cats

Shaw et al. (2004) 12.9% (4/31) in dogs

Analysis of pools of 1–20 fleas

France Cats 8.1% (25/309)

Rolain et al. (2003) Individual analysis

France Cats 29.2% (14/48)

J.L. Marie and Davoust (2003) Individual analysis

Spain Dogs and cats 54.2% (39/72)

(Southeast: Andalusia) Analysis of pools of 1–11 fleas

Marquez et al. (2006)

F. Beugnet, J.-L. Marie / Veterinary Parasitology 163 (2009) 298–305 303

found in Xenopsylla cheopis, the Oriental rat flea (Schlo-derer et al., 2006). The role of mammals, including cats,dogs, rodents and hedgehogs, in the life cycle andcirculation of R. felis remains unclear.

Although disease caused by R. felis is probablyubiquitous, up to now few clinical cases have beenreported worldwide. The disease may be misdiagnosedas a tick-borne rickettsiosis. Classical symptoms reportedare fever, maculo-papular rash and eschar (Brouqui et al.,2007). According to previous reports, headache, abdominalpain, nausea, vomiting, and diarrhoea, as well as centralnervous system involvement (photophobia, hearing loss,and/or meningitis), have also been described. Recently, inthe Canary Islands, five cases of flea-borne spotted feverwere diagnosed by serology (western blot) among 44patients with clinically suspected rickettsiosis (Perez-Arellano et al., 2005).

Very few cases of animal disease due to R. felis infectionare reported in the literature. Interestingly, in Spain, DNAof R. felis was found in the serum of a dog living in a housewhere two people developed flea-borne spotted fever, asevidenced by PCR (Oteo et al., 2006). The dog did not showfever, but signs of fatigue, vomiting and diarrhoea werereported. Although no fleas were observed on the dog atthe time of the outbreak, the patients said fleas hadparasitized the dog in the past and they had been bitten byfleas (Oteo et al., 2006). In a similar situation in Germany,one dog from a family in which two people suffered fromflea-borne spotted fever was found to be infected by R. felis,but showed no signs (Richter et al., 2002). Previous studiesof naturally or experimentally infected cats have docu-mented antibody responses to R. felis, suggesting that atleast a transient infection occurs. There is no clinical case ofR. felis infection reported in cats, to the author’s knowledge.

6. Modelling tick and flea risk

As described above, the abundance and distribution ofmany species of tick and the prevalence of tick-bornedisease have increased considerably in Europe over the last10 years, with a clear increase in the human diseasestransmitted by forest ticks, such as rickettsiosis, anaplas-mosis, and encephalitis. It is therefore important todevelop epidemiological models linking three key ele-ments: biomathematics – to study the dynamics of vectorsand pathogens; satellite mapping – to monitor the

emergence and distribution of diseases related to vegeta-tion and human activities; and climatic modelling – tofollow parasite activity caused by meteorological trends.

The necessity of modelling and mapping to surveyveterinary patasitology and vector-borne diseases hasbeen raised recently by several teams (Rinaldi et al., 2006;Marechal et al., 2008). Modelling will also help to identifythe best control methods against arthropod-borne diseasesby assessing the impact of different measures (Otranto andWall, 2008).

A new model, called ‘‘FleaTickRisk’’ has been designedin collaboration between climatologists (from Climpact, astart-up between researchers from the CNRS and Paris VIUniversity), biomathematicians (from the research unit ofthe Lyon Veterinary School associated with the CNRS) andparasitologists (from Merial and the Maisons-AlfortVeterinary School) (Beugnet et al., 2008). After 2 yearsof development, the model known as ‘‘FleaTickRisk’’ cannow predict, on a weekly basis, the activity of three tickspecies across Europe as well as that of cat fleas in France(which was the pilot country in 2008). It can also predictthe abundance of parasites and the risk of diseasetransmission (i.e. animal and human infestations). It hasbeen made available for veterinarians on a dedicatedwebsite: http://www.fleatickrisk.com/. This model hasbeen extended to all of Europe in the autumn of 2008and made available in several languages. Scientificvalidation based on parasite collection has started andwill continue throughout 2008 and 2009. The model meansthat the impact of the climate on parasite burdens can bestudied, but it will also help veterinarians in their day-to-day activity of recommending suitable parasite treatmentand prevention.

7. Conclusion

For multifactorial reasons, the epidemiology of arthro-pod-borne diseases in Europe is changing. This makes itnecessity to put in place new measures to survey theirepidemiology as well as new alert and control strategies(Otranto and Wall, 2008). Amongst vector-borne diseases,tick transmitted infections appear to be less stable in termsof epidemiology and emergence. It is therefore crucial tocontinue and increase surveillance and to develop tools fortheir study, including epidemiological modelling. Becausethe majority of these diseases are zoonotic, involve wild

F. Beugnet, J.-L. Marie / Veterinary Parasitology 163 (2009) 298–305304

hosts, and may be affected by many ecological factors,future studies call for a multidisciplinary approachincluding veterinarians, physicians, ecologists, climatolo-gists, biomathematicians and others. Due to the closerelationships between humans and their pets, domesticcarnivores may act as a sentinel for their owners,reinforcing the role of veterinarians in the diagnosis ofsuch emerging diseases.

Conflict of interest

None.

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