The frequency and distribution of canine leishmaniosis diagnosed byveterinary practitioners in EuropeMJ Mattin a L Solano-Gallego b S Dhollander c A Afonso c DC Brodbelt a

a Department of Production and Population Health The Royal Veterinary College University of London Hawkshead Lane North Mymms HatfieldHertfordshire AL9 7TA UKb Departament de Medicina i Cirurgia Animal Facultat de Veterinagraveria Universitat Autogravenoma de Barcelona Edifici V 08193 Bellaterra Spainc European Food Safety Authority Via Carlo Magno 1deg 43126 Parma Italy

A R T I C L E I N F O

Article historyAccepted 31 March 2014

KeywordsCanineDogEpidemiologyLeishmaniosisPrevalence

A B S T R A C T

This study aimed to evaluate the frequency and spatial distribution of canine leishmaniosis (CanL) in FranceGreece Italy Portugal and Spain An online questionnaire investigated the location and frequency of CanLcases diagnosed by veterinary practitioners Further data from the practice management systems of vet-erinary clinics in France were provided by a financial benchmarking company in relation to all treat-ment and test invoice data from participating practices The geographical and temporal web interest inleishmaniosis was explored using Google Trends

Veterinary practitioners from France Greece Italy Portugal and Spain completed 1231 question-naires The percentage of practice-attending dogs with a veterinary diagnosis of CanL ranged from 071in France to 780 in Greece However due to regional differences in response rates particularly in Francethe mean regional estimates may better reflect the disease burden Benchmarking data relating to ap-proximately 180000 dogs estimated that 005 of dogs attending veterinary clinics were treated for CanLor euthanased with suspected CanL in France The regional frequency of Google web queries for leish-maniosis generally reflected the spatial patterns of disease identified from the other data sources In con-clusion CanL was a relatively common diagnosis in veterinary clinics in many regions of the countriesstudied Knowledge of CanL in endemic areas can direct the use of preventative measures and help es-timate the likelihood of infection in dogs visiting or inhabiting these countries

copy 2014 Published by Elsevier Ltd

Introduction

Leishmaniosis is endemic in parts of Europe where the causalagent is almost exclusively Leishmania infantum (Ready 2010) andthe main reservoir host is the domestic dog (Alvar et al 2004 Banethet al 2008 Quinnell and Courtenay 2009) The parasite can causesevere potentially fatal disease in humans (Desjeux 2004) and dogs(Solano-Gallego et al 2009) presenting both public health andanimal welfare concerns

In recent years a northward spread of leishmaniosis in Italy hasbeen documented (Maroli et al 2008 Baldelli et al 2011) This hasbeen attributed to changes in vector distributions possibly as a resultof climate change Increased travel and movement of infected dogsmay also contribute to the changing epidemiology of the diseasewithin and between countries (Teske et al 2002 Menn et al 2010)Shaw et al (2009) identified a number of clinically apparent canineleishmaniosis (CanL) cases in the United Kingdom (UK) which had

been imported from or travelled to CanL endemic countries Anumber of these dogs were re-homed shelter dogs which may beat a higher risk of developing seropositivity to L infantum than owneddogs in endemic countries (Paradies et al 2006 Schallig et al 2013)

However clinically apparent cases represent the minority of in-fected dogs in endemic regions (Moreno and Alvar 2002Solano-Gallego et al 2009 Schallig et al 2013) so dogs with sub-clinical infection that appear healthy may also be imported fromendemic regions Further an association between the area a dogoriginated from and the course of infection has been found in acohort of dogs exposed to natural L infantum infection (Quinnellet al 2003) suggesting that the likelihood of infection may be dif-ferent in dogs visiting and inhabiting endemic areas These issuesrelating to the spread of CanL make it particularly pertinent to eval-uate the current prevalence and distribution of the disease

Routine collection of veterinary data from companion animalsis limited and there have been few large scale epidemiological studieson clinically apparent CanL in the European Union (EU) Nationalsurveys of CanL in veterinary clinics across France estimated a diseaseprevalence of 041 and suggested that CanL was endemic along theMediterranean coast and in the South-East of the country (Bourdeau

Corresponding author Tel +44 1707 667168E-mail address maddylahotmailcom (MJ Mattin)

httpdxdoiorg101016jtvjl2014030331090-0233copy 2014 Published by Elsevier Ltd

The Veterinary Journal (2014) ndash

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Contents lists available at ScienceDirect

The Veterinary Journal

journal homepage wwwelseviercom locate tv j l

et al 2004 2011) In 2009 the true prevalence of CanL infectionin dogs attending veterinary clinics across Portugal was estimatedto be 631 (Cortes et al 2012) The apparent prevalence of infec-tion was reported to be 194 in a study of clinically normal dogsattending veterinary clinics in mainland Greece (Athanasiou et al2012) Other CanL epidemiological studies were mostlyseroprevalence surveys conducted in limited geographical areas oftenin southern parts of Western European countries (Trotz-Williamsand Trees 2003)

Many factors will influence prevalence estimates of L infantuminfection and disease including the source population the charac-teristics of diagnostic tests used and the tissue sampled(Solano-Gallego et al 2001 Fernaacutendez-Bellon et al 2008Morales-Yuste et al 2012) Sampling techniques diagnostic test cut-off values and the time of year the study is conducted can also in-fluence estimates (Morales-Yuste et al 2012) making directcomparison of studies difficult

Recently disease surveillance techniques using search enginequery data have been developed to complement more convention-al methods (Eysenbach 2006 Carneiro and Mylonakis 2009) Googlean internet search engine has developed Google Trends (GT) (GoogleTrends 2013)1 a tool that captures data based on the number ofGoogle web searches for user-specified search terms This tool hasbeen used to track internet interest in several diseases including in-fluenza (Eysenbach 2006) West Nile virus Respiratory syncytialvirus (Carneiro and Mylonakis 2009) Lyme disease (Seifter et al2010) and otolaryngological conditions (Braun and Harreacuteus 2013)In addition to using English terms disease tracking with GT has beenexplored using French (Pelat et al 2009) and Spanish (Valdiviaand Monge-Corella 2010) search terms To our knowledge GT hasnot been used to explore trends in search terms relating toleishmaniosis

The objectives of this study were (1) to collect data on preva-lence and management of CanL as diagnosed by veterinary practi-tioners in France Greece Italy Portugal and Spain (2) to comparethe geographical distribution and frequency of the cases in Francewith data collected from a benchmarking company and (3) toexplore GT as a tool for monitoring CanL trends This work was doneas part of a project funded by EFSA (European Food Safety Author-ity) that evaluated the impact of CanL in the EU

Materials and methods

Three data sources were evaluated to estimate the frequency and spatial distri-bution of CanL in France Greece Italy Portugal and Spain an online question-naire benchmarking data and Google Trends The project received ethical approvalfrom the Royal Veterinary College Ethics and Welfare Committee (URN 2012 1188)

Online veterinary questionnaire

An online questionnaire for veterinarians asked respondents to estimate the totalnumber of confirmed CanL cases seen at their clinic within the last 12 months thenumber of new (incident) cases diagnosed within this period and their weekly caninecaseload (see Appendix A Supplementary material) The total annual number of casesincluded dogs with CanL that had attended the clinic within the previous 12 monthsirrespective of when the original diagnosis was made (both newly diagnosed inci-dent cases and pre-existing cases were included) CanL cases confirmed by any di-agnostic method were included Other questions related to the frequency with whichdifferent CanL preventative measures and treatments were used in respondentsrsquo clinicsand the perceived impact of the economic crisis on veterinary services relating toCanL The questionnaire was translated into the relevant languages and promotedto veterinary practitioners working in France Greece Italy Portugal and Spain Memberorganisations of the FVE (Federation of Veterinarians of Europe) and companion animalveterinary associations promoted the questionnaire to their members via email ortheir websites

Data collected from the online veterinary questionnaire were cleaned and analysedusing Microsoft Excel Period prevalence (the proportion of practice-attending dogs

with a confirmed veterinary diagnosis of CanL within a 12-month period) was cal-culated at the national and NUTS (Nomenclature of Territorial Units for Statistics)2

levels 2 (larger regions within a country) and 3 (smaller areas eg department orprovince within a region) using the following equation

Prevalence annual number of leishmaniosis cases existing a= ( nndnew cases annual number of dogs attending clinics)

The estimated number of dogs seen per week was multiplied by the average annualnumber of working weeks to derive the annual number of consultations involvingdogs The annual number of working weeks was calculated by subtracting the averagecollectively agreed paid annual leave for each country3 from the number of weeksper year To account for multiple visits per dog the annual number of consultationswas divided by the reported mean number of times a dog attends a clinic per year(P Mercader T Richard personal communication) Incidence risk was calculated bydividing the number of incident cases (newly diagnosed with CanL within the pre-vious year) by the number of dogs attending the clinics annually The mean and medianNUTS 2 level prevalence estimates and 95 confidence intervals (CI) were calculatedusing standard methods (Kirkwood et al 2003) The number of questionnaire re-sponses prevalence estimates and associated standard errors were presented as NUTS3 level choropleth maps in ArcGIS 9 (ESRI 2013) using shape-files downloaded froma database of global administrative areas (GADM 2013)4 In some instances NUTS 3regions were combined to become compatible for joining to shape-files

Benchmarking data

Data were requested from a French benchmarking company (Panelvet)5 whichextracts clinical and financial data from the practice management systems (account-ing and clinical record computer systems) of primary-care veterinary clinics in FrancePrevalence was defined as the proportion of benchmarking company subscribingpractice-attending dogs invoicing treatment for or euthanasia with CanL annuallyData at the NUTS 3 (department) level were available including the number of vet-erinary clinics and the number of dogs attending clinics in each department thatcontributed data The latter figure was used as the denominator population for theprevalence estimates

CanL cases were defined as dogs whose electronic patient records contained in-voices for treatment specific for CanL (allopurinol meglumine antimoniatemiltefosine Solano-Gallego et al 2009) or dogs which were tested or treated (butnot vaccinated) and euthanased within 60 days of the last test or treatment pre-scribed Duplicate records of the same animal were excluded Data were analysedusing Microsoft Excel and exported to ArcGIS 9 (ESRI 2013) to create maps as de-scribed for the online questionnaire

Google Trends

Temporal trends for Google queries for lsquoleishmaniosisrsquo lsquocanine leishmaniosisrsquolsquorabiesrsquo and lsquobabesiosisrsquo between April 2007 and April 2013 were compared withineach studied country when possible Each search term was translated into the rel-evant language and entered into GT on 18 April 2013 to explore the relative web in-terest in the different veterinary diseases The results of the queries were displayedas search volume index graphs generated by GT News headlines relating to the searchterms were also indicated on the graphs whenever Google detected a peak in GoogleNews stories relating to a search term (Carneiro and Mylonakis 2009) Queries forlsquoleishmaniosisrsquo and lsquodogrsquo were entered into GT to generate maps showing the geo-graphical differences in web interest for these terms The latter term was includedto account for regional differences relating to interest in dogs or caninepopulations

Results

Online veterinary questionnaire

In total 1231 questionnaires were completed by veterinary prac-titioners between January and May 2013 625 came from France369 from Spain 57 from Portugal 67 from Italy and 113 from GreeceThirteen questionnaires were not analysed as they were com-pleted by veterinary practitioners working outside the studied coun-tries or not currently in employment The number of responses per

1 See httpwwwgooglecouktrendsexplore

2 See httpeppeurostateceuropaeuportalpageportalnuts_nomenclatureintroduction

3 See httpwwweurofoundeuropaeueirostudiestn1106010stn1106010shtmfig7

4 See httpwwwgadmorg5 See httpwwwpanelvetfr

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area varied within countries especially in France where more re-sponses were received from Southern departments (Fig 1)

The national prevalence estimates of veterinary-diagnosed CanL(percentage of practice-attending dogs with a confirmed veterinary-diagnosis of CanL) ranged from 071 in France to 780 in Greece(Table 1) This represented a median of one CanL case seen by theresponding veterinarian over the previous year in France and amedian of 25 cases seen by each veterinarian in Greece Veteri-nary practitioners in Spain Portugal and Italy saw a median of eightcases annually Generally prevalence estimates were highest in theMediterranean regions (Fig 2) and standard errors of these esti-mates were smaller in parts of France and Spain where number ofrespondents were higher compared with the other countries (Fig 3)Differences between the national and average regional (NUTS 2) prev-alence estimates were particularly marked for France (Tables 1and 2)

The most common CanL preventative measures used in practice-attending dogs were repellents and insecticides applied to the dog(Fig 4) In addition to the preventative measures specified in thequestionnaire some veterinarians recommended keeping dogsindoors overnight using environmental insecticides and using drugstypically used to treat CanL as prophylaxes (allopurinol meglumineantimoniate and miltefosine) Allopurinol was the most frequentlyprescribed treatment for CanL although meglumine antimoniate andmiltefosine were used relatively frequently in some countries (Fig 5)In addition some veterinarians used treatments not specified in thequestionnaire including antibiotics corticosteroids levamisole com-plementary therapies immunotherapy neutraceuticals ACE inhibi-tors anthelmintics and autovaccination

Generally veterinary practitioners responding to the online ques-tionnaire thought that the economic crisis was most likely to havea moderate to high impact on the use of prophylactic measures and

Fig 1 Number of responses to a veterinary questionnaire which aimed to estimate the percentage of practice-attending dogs diagnosed with canine leishmaniosis in FranceGreece Italy Portugal and Spain over a 12-month period (2012ndash2013)

Table 1Estimated frequency of confirmed veterinary diagnosis of canine leishmaniosis in dogs attending veterinary clinics over a 12-month period (2012ndash2013) in France GreeceItaly Portugal and Spain

Cases per veterinarianMedian (range)

Dogs per veterinarianMedian (range)

National prevalence b

(95 CI)National incidence per 1000

(95 CI)

Incidenta All cases Dogs per week Consults per year Dogs seen per year

CountryFrance 1 (0ndash150) 1 (0ndash190) 50 (0ndash600) 2350

(0ndash28200)783

(0ndash9400)071

(069ndash073)46

(45ndash48)Greece 20 (0ndash200) 25 (1ndash350) 30 (2ndash250) 1422

(95ndash11850)474

(32ndash3950)780

(758ndash803)563

(543ndash582)Italy 5 (0ndash100) 8 (0ndash250) 25 (3ndash150) 1160

(139ndash6960)387

(46ndash2320)433

(416ndash450)226

(210ndash243)Portugal 55 (0ndash80) 8 (0ndash80) 20 (1ndash100) 938

(47ndash4688)313

(16ndash1563)292

(271ndash313)231

(213ndash250)Spain 6 (0ndash220) 8 (0ndash220) 30 (0ndash209) 1406

(0ndash9798)469

(0ndash3266)371

(363ndash379)252

(245ndash259)

a Incident new canine leishmaniosis cases diagnosed within the last 12 monthsb Prevalence percentage of practice-attending dogs with a confirmed veterinary diagnosis of canine leishmaniosis

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Fig 2 Veterinary estimates of the percentage of practice-attending dogs diagnosed with canine leishmaniosis (pre-existing and incident cases) in France Greece Italy Por-tugal and Spain over a 12-month period (2012minus2013)

Fig 3 Standard errors of the estimated percentage of practice-attending dogs diagnosed with canine leishmaniosis (pre-existing and incident cases) in France Greece ItalyPortugal and Spain over a 12-month period (2012minus2013)

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the diagnosis and treatment of dogs with CanL (Fig 6) The re-sponses relating to the impact of the economic crisis on euthana-sia decisions were more diverse

Benchmarking data

In total 97 clinics located in 52 French departments contrib-uted data relating to approximately 180000 dogs each year betweenAugust 2010ndashAugust 2011 and August 2011ndashAugust 2012 Up to sevenpractices per department contributed data (Fig 7) A mean of 844dogs were under the care of each full-time veterinary practitionerannually

Table 2Regional estimates of the percentage of practice-attending dogs with a confirmedveterinary diagnosis of canine leishmaniosis attending veterinary clinics over a 12-month period (2012ndash2013) in France Greece Italy Portugal and Spain

Regional (NUTS 2) prevalence estimates ()

Mean Median Range

CountryFrance 043 005 001ndash351Greece 905 741 380ndash2157Italy 361 285 000ndash1118Portugal 278 312 097ndash366Spain 287 295 031ndash615

NUTS Nomenclature of Territorial Units for Statistics

Fig 4 Veterinary estimates of the proportions of all dogs attending their clinic that receive preventative measures for canine leishmaniosis in France Greece Italy Portu-gal and Spain The Y axis represents the percentage of respondents per country indicating that level of measure use

Fig 5 Frequency of treatments used for canine leishmaniosis in veterinary clinics France Greece Italy Portugal and Spain The Y axis represents the percentage of respon-dents per country indicating that level of treatment use

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During the first and second 12 months of the study period 415(023) and 735 (041) dogs attending these clinics were tested forLeishmania infection The majority of invoices (593) did not specifythe type of test used Of the specified tests the most commonly usedwere serological rapid tests (396) Less than 1 of Leishmania testswere specified as PCR tests Ninety-four and 83 dogs were treatedfor CanL or euthanased with CanL between August 2010ndashAugust 2011and August 2011ndashAugust 2012 respectively The vast majority relatedto invoice data for treatment (910) with only 16 (90) euthanasedThis equated to 0052 (95 CI 0047ndash0057) and 0046 (95 CI0041ndash0051) of practice-attending dogs being treated for oreuthanased with CanL in each 12-month period The apparent prev-alence at the department-level ranged from 0 to 083 (Fig 8) with

higher levels of disease generally found in the South-Eastern de-partments

A total of 565 (031) dogs were vaccinated against Leishmaniainfection between August 2011 and August 2012 The median pro-portion of dogs receiving the vaccine per department was 001 andranged from 0 to 953 The pattern of vaccination administrationlargely reflected the disease distribution

Google Trends

G generated graphs and maps reflecting web search volumes forlsquoleishmaniosisrsquo in France Italy Portugal and Spain There were in-sufficient numbers of web queries for this term for analysis in Greece

Fig 6 Veterinary opinion of the likely impact of the current economic crisis on the veterinary care of dogs affected by leishmaniosis in France Greece Italy Portugal andSpain

Fig 7 Number of Panelvet practices contributing financial and clinical veterinary data per department in France August 2011ndashAugust 2012

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Generally web searches for leishmaniosis were more frequent thansearches for babesiosis but less frequent than for rabies (Fig 9) Re-gional web searches for lsquodogrsquo were generally more homogenouslydistributed than for lsquoleishmaniosisrsquo especially in France and Spain(Fig 10) where searches for lsquoleishmaniosisrsquo broadly followed thedisease distribution identified from the veterinary questionnaire(Fig 2)

Discussion

This study highlights the greatest estimates of veterinary-diagnosed CanL in the Mediterranean in Greece whereas France hadthe lowest perceived burden of disease and Italy Portugal and Spainhad intermediate estimates The geographical distribution of diseasebased on the questionnaire data was broadly consistent with thepatterns identified from two novel data sources namely veteri-nary benchmarking data and GT

The national prevalence of disease seen in France was 071 (pro-portion of practice-attending dogs with a diagnosis of CanL over a12-month period 95 CI 069ndash073) whereas the mean region-al prevalence was 043 The national prevalence in the current studywas higher than that observed by Bourdeau et al (2004) (041)The difference in national prevalence estimates may be due to dif-fering methodologies temporal changes in diagnostic test avail-ability or accuracy an increased awareness of CanL or a true increasein CanL prevalence over time In both studies greater numbers ofresponses were received from departments in South-East Francewhere CanL was observed to be most prevalent Consequently thenational estimate of 071 may be an overestimate and the meanregional estimate was likely to represent a better estimate of theburden of disease Furthermore the large difference betweenthe regional median and mean prevalence estimates reflects that

the regional prevalence estimates of CanL were highly skewedwith the majority of regions in France experiencing very low levelsof disease

The benchmarking data estimated that 005 of practice-attendingdogs were treated for or euthanased with CanL in France This wasbased on invoice data relating to CanL treatments or euthanasia fol-lowing testing and was much lower than the estimates calculatedfrom the online questionnaire This case-finding method would nothave detected CanL cases prescribed treatments other than allopu-rinol meglumine antimoniate and miltefosine or therapies sold anddispensed that were not entered onto the clinicsrsquo practice manage-ment systems Moreover dogs receiving treatment purchased fromhuman or online pharmacies that were not invoiced via the par-ticipating practice would not have been included as cases Despitethis limited sensitivity the geographical distribution of cases fol-lowed a similar pattern to the questionnaire data

Veterinary-diagnosed CanL was observed to have a relatively highprevalence in dogs attending practices in all responding regions inGreece However there were low numbers of responses from regionsoutside of Athens resulting in imprecise estimates In Italy the regionsof Sicily Piedmont and Liguria had the highest prevalence of CanLwhereas the North-East regions had low levels of disease Previ-ous studies on owned dogs in coastal and Southern Italy generallyreported higher CanL seroprevalence estimates (Zaffaroni et al 1999Cringoli et al 2002 Rossi et al 2008) compared with a study con-ducted in Northern continental regions (Maroli et al 2008) In con-trast to the results in the current study Ferroglio et al (2005)detected a low prevalence of CanL infection in the region of Pied-mont The prevalence of CanL in Portugal appeared to be highestin parts of Central Portugal and lowest in the north consistent withthe results of a recent national survey (Cortes et al 2012) The fre-quency of CanL cases was highest in the South-East and lowest in

Fig 8 Percentage of practice-attending dogs treated for or euthanased with canine leishmaniosis in France between August 2010ndashAugust 2011 (Fig 8a) and August 2011ndashAugust 2012 (Fig 8b) and standard error maps of these estimates (Figs 8c and d)

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the North and West of Spain largely compatible with existingseroprevalence studies (Morillas et al 1996 Amusategui et al 2004Alonso et al 2010)

The online questionnaire estimates were based on veterinary-diagnosed cases of CanL seen at private veterinary clinics Due to

different clinical approaches specific criteria for the case defini-tion (eg specific clinical signs serology results exceeding a certaintitre) were not specified in the questionnaire The local prevalenceestimates would have depended on factors including the clinicalacumen of the veterinary practitioners the proportion of sus-

Fig 9 Temporal patterns of Google web searches for leishmaniosis and other selected veterinary diseases in France (Fig 9a) Italy (Fig 9b) Portugal (Fig 9c) and Spain(Fig 9d) April 2007ndashApril 2013 The number 100 on the Y axis represents the relative peak in web search interest for any search term

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pected cases that underwent investigations and the characteris-tics of the diagnostic techniques adopted

The travel history of the dogs with CanL was not collected so itwas not possible to speculate where the infections were acquiredFurther although it is likely that a high proportion of veterinary case-loads consist of client-owned dogs the living conditions of the dogswere not recorded the prevalence of CanL in client-owned dogs maydiffer to that of stray dog populations In order to calculate thenumber of dogs seen annually it was assumed that a dog at-tended a clinic three times per year based on data from bench-marking companies in France and Spain (P Mercader T Richardpersonal communication) It was assumed that this figure would besimilar for all the studied countries If the mean number of annualvisits per dog was under- or overestimated for a country this wouldhave impacted on the prevalence estimate Furthermore thegeneralisation of these estimates to the wider dog population willdepend on the proportion of the entire dog population that attendveterinary clinics in each country

Generally the impact of the economic crisis on the use of CanLprophylaxis diagnostics and treatments was considered to be higherin Spain Greece and Portugal than France and Italy consistent withthe reported magnitude of economic hardship of the respectivecountries6 If disease control measures were relaxed or treatmentplans were suboptimal this may have both animal welfare and publichealth implications

The frequency of Google searches for CanL followed the patternof searches for leishmaniosis Peaks in Italy appeared to corre-

spond to news headlines and follow a seasonal pattern The termlsquoleishmaniosisrsquo rather than lsquocanine leishmaniosisrsquo was selected togenerate maps showing the spatial distribution of web interest asa greater number of searches were performed for the more generalterm than for the canine-specific term Although a proportion ofthese searches may have been relating to the human form of thedisease the levels of web interest in the two search terms ap-peared to be correlated The geographical distribution of web searchinterest in France Italy and Spain broadly followed the patterns iden-tified by the online questionnaire and the benchmarking data Al-though GT normalises the data to compensate for differences inpopulation size to be effective a large population of Google usersis necessary (Carneiro and Mylonakis 2009) The relativelysmall populations in Portugal and Greece7 may explain why limitedand no regional results were generated for these countriesrespectively

Conclusions

CanL was a relatively common clinical diagnosis in veterinaryclinics in many regions of France Greece Italy Portugal and SpainCanL had a heterogeneous spatial distribution as evidenced fromveterinary questionnaire data French benchmarking data and in-ternet web interest The current economic climate may have anadverse impact on the prevention and treatment of CanL whichcould subsequently influence the future epidemiology of the diseaseThere is therefore a major need for the routine collection of epide-

6 Eurostat National accounts and GDP ndash Statistics explained httpeppeurostateceuropaeustatistics_explainedindexphpNational_accounts_and_GDP (ac-cessed 30 April 2013)

7 Eurostat Population statistics at regional level ndash Statistics Explained httpeppeurostateceuropaeustatistics_explainedindexphpPopulation_statistics_at_regional_level (accessed 9 August 2013)

Fig 10 Regional Google web search volumes for lsquodogrsquo in France (Fig 10a) Italy (Fig 10b) Portugal (Fig 10c) and Spain (Fig 10d) and for lsquoleishmaniosisrsquo in France (Fig 10e)Italy (Fig 10f) Portugal (Fig 10g) and Spain (Fig 10h) April 2007ndashApril 2013

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9MJ Mattin et alThe Veterinary Journal (2014) ndash

miological data from companion animals in the EU to be able tomeasure and respond to changes in disease frequency

Conflict of interest statement

None of the authors of this paper has a financial or personal re-lationship with other people or organisations that could inappro-priately influence or bias the content of the paper

Acknowledgements

The authors would like to acknowledge the European Food SafetyAuthority (EFSA) for funding this work and EFSA scientific staff ClaireWylie Solenne Costard Luis Espejo and Francisco Zagmutt for theirvaluable input The authors would like to thank Nancy De Briynefor her help distributing the online veterinary questionnaire to FVEmember associations The authors are grateful to the following vet-erinary associations for promoting the questionnaire to theirmembers SNVL and AFVAC (France) HCAVS and HVA (Greece)FNOVI and SCIVAC (Italy) OMV and APMVEAC (Portugal) and CGCVEand AMVAC (Spain) The authors would also like to thank all the vet-erinary practitioners who responded to the survey and the follow-ing people who translated the questionnaires into the locallanguages Aris Polyviou Maria Ferrara Alex Mattin Ana PascualLuiacutes Cardoso and Joatildeo Sucena Afonso The authors also acknowl-edge Thibault Richards for providing the benchmarking data and PereMercador for information relating to trends in Spanish practice at-tending animals This manuscript has been approved by the RoyalVeterinary Collegersquos publications approval system in order to complywith Good Research Practice Policy on Publications (manuscriptnumber PPH_00629) Dr Laia Solano-Gallego holds a Ramoacuten y Cajalsenior researcher contract awarded by the Spanish Ministerio deEconomia y Competitividad and the European Social Fund

Appendix A Supplementary material

Supplementary data associated with this article can be found inthe online version at doi101016jtvjl201403033

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Alvar J Canavate C Molina R Moreno J Nieto J 2004 Canine leishmaniasisAdvances in Parasitology 57 1ndash88

Amusategui I Sainz A Aguirre E Tesouro MA 2004 Seroprevalence of Leishmaniainfantum in Northwestern Spain an area traditionally considered free ofleishmaniasis Annals of the New York Academy of Sciences 1026 154ndash157

Athanasiou LV Kontos VI Saridomichelakis MN Rallis TS Diakou A 2012 Across-sectional sero-epidemiological study of canine leishmaniasis in Greekmainland Acta Tropica 122 291ndash295

Baldelli R Piva S Salvatore D Parigi M Melloni O Tamba M Bellini R PoglayenG 2011 Canine leishmaniasis surveillance in a northern Italy kennel VeterinaryParasitology 179 57ndash61

Baneth G Koutinas AF Solano-Gallego L Bourdeau P Ferrer L 2008 Canineleishmaniosis ndash new concepts and insights on an expanding zoonosis part oneTrends in Parasitology 24 324ndash330

Bourdeau P Mallet M Marchand A 2004 Canine Leishmaniosis in France anational survey on distribution and prevalence In European Multicolloquiumof Parasitology Valencia Spain

Bourdeau P Doval A Roussel A 2011 Canine Leishmaniosis in France Results ofa National Survey with 1345 clinics In European Veterinary Parasitology CollegeAnnual Conference 2011 Zagreb

Braun T Harreacuteus U 2013 Medical nowcasting using Google Trends applicationin otolaryngology European Archives of Oto-Rhino-Laryngology 270 2157ndash2160

Carneiro HA Mylonakis E 2009 Google Trends a web-based tool for real-timesurveillance of disease outbreaks Clinical Infectious Diseases 49 1557ndash1564

Cortes S Vaz Y Neves R Maia C Cardoso L Campino L 2012 Risk factors forcanine leishmaniasis in an endemic Mediterranean region Veterinary Parasitology189 189ndash196

Cringoli G Rinaldi L Capuano F Baldi L Veneziano V Capelli G 2002 Serologicalsurvey of Neospora caninum and Leishmania infantum co-infection in dogsVeterinary Parasitology 106 307ndash313

Desjeux P 2004 Leishmaniasis current situation and new perspectives ComparativeImmunology Microbiology and Infectious Diseases 27 305ndash318

ESRI 2013 Environmental Systems Resource Institute ArcMap 93 ESRI RedlandsCalifornia

Eysenbach G 2006 Infodemiology tracking flu-related searches on the web forsyndromic surveillance In AMIA Annual Symposium Proceedings pp 244ndash248

Fernaacutendez-Bellon H Solano-Gallego L Rodriacuteguez-Corteacutes A Ferrer L Gallego MAlberola J Ramis A 2008 Little evidence of seasonal variation of naturalinfection by Leishmania infantum in dogs in Spain Veterinary Parasitology 15532ndash36

Ferroglio E Maroli M Gastaldo S Mignone W Rossi L 2005 Canine leishmaniasisItaly Emerging Infectious Diseases 11 1618ndash1620

GADM 2013 GADM database of Global Administrative Areas Available fromlthttpwwwgadmorg2013gt

Kirkwood BR Sterne JAC Kirkwood BREOMS 2003 Kirkwood BR SterneJAC (Eds) Essential medical statistics second ed Blackwell Science MaldenMass Oxford

Maroli M Rossi L Baldelli R Capelli G Ferroglio E Genchi C Gramiccia MMortarino M Pietrobelli M Gradoni L 2008 The northward spread ofleishmaniasis in Italy evidence from retrospective and ongoing studies on thecanine reservoir and phlebotomine vectors Tropical Medicine and InternationalHealth 13 256ndash264

Menn B Lorentz S Naucke TJ 2010 Imported and travelling dogs as carriers ofcanine vector-borne pathogens in Germany Parasites and Vectors 3 34

Morales-Yuste M Morillas-Maacuterquez F Diacuteaz-Saacuteez V Baroacuten-Loacutepez S Acedo-SaacutenchezC Martiacuten-Saacutenchez J 2012 Epidemiological implications of the use of variousmethods for the diagnosis of canine leishmaniasis in dogs with differentcharacteristics and in differing prevalence scenarios Parasitology Research 111155ndash164

Moreno J Alvar J 2002 Canine leishmaniasis epidemiological risk and theexperimental model Trends in Parasitology 18 399ndash405

Morillas F Sanchez Rabasco F Ocana J Martin-Sanchez J Ocana-Wihelmi J AcedoC Sanchiz-Marin MC 1996 Leishmaniosis in the focus of the Axarquia regionMalaga province southern Spain a survey of the human dog and vectorParasitology Research 82 569ndash570

Paradies P Capelli G Cafarchia C de Caprariis D Sasanelli M Otranto D 2006Incidences of canine leishmaniasis in an endemic area of southern Italy Journalof Veterinary Medicine Series B- Infectious Diseases and Veterinary Public Health53 295ndash298

Pelat C Turbelin C Bar-Hen A Flahault A Valleron A 2009 More diseases trackedby using Google Trends Emerging Infectious Diseases 15 1327ndash1328

Quinnell RJ Courtenay O 2009 Transmission reservoir hosts and control ofzoonotic visceral leishmaniasis Parasitology 136 1915ndash1934

Quinnell RJ Kennedy LJ Barnes A Courtenay O Dye C Garcez LM Shaw MACarter SD Thomson W Ollier WE 2003 Susceptibility to visceral leishmaniasisin the domestic dog is associated with MHC class II polymorphismImmunogenetics 55 23ndash28

Ready PD 2010 Leishmaniasis emergence in Europe Euro Surveillance 15 19505Rossi E Bongiorno G Ciolli E Di Muccio T Scalone A Gramiccia M Gradoni

L Maroli M 2008 Seasonal phenology host-blood feeding preferences andnatural Leishmania infection of Phlebotomus perniciosus (Diptera Psychodidae)in a high-endemic focus of canine leishmaniasis in Rome province Italy ActaTropica 105 158ndash165

Schallig HD Cardoso L Semiao-Santos SJ 2013 Seroepidemiology of canineleishmaniosis in Evora (southern Portugal) 20-year trends Parasites and Vectors6 100

Seifter A Schwarzwalder A Geis K Aucott J 2010 The utility of lsquoGoogle Trendsrsquofor epidemiological research lyme disease as an example Geospatial Health 4135ndash137

Shaw SE Langton DA Hillman TJ 2009 Canine leishmaniosis in the UnitedKingdom a zoonotic disease waiting for a vector Veterinary Parasitology 163281ndash285

Solano-Gallego L Morell P Arboix M Alberola J Ferrer L 2001 Prevalence ofLeishmania infantum infection in dogs living in an area of canine leishmaniasisendemicity using PCR on several tissues and serology Journal of ClinicalMicrobiology 39 560ndash563

Solano-Gallego L Koutinas A Miroacute G Cardoso L Pennisi MG Ferrer L BourdeauP Oliva G Baneth G 2009 Directions for the diagnosis clinical stagingtreatment and prevention of canine leishmaniosis Veterinary Parasitology 1651ndash18

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ARTICLE IN PRESS

Please cite this article in press as MJ Mattin L Solano-Gallego S Dhollander A Afonso DC Brodbelt The frequency and distribution of canine leishmaniosis di-agnosed by veterinary practitioners in Europe The Veterinary Journal (2014) doi 101016jtvjl201403033

10 MJ Mattin et alThe Veterinary Journal (2014) ndash