Epidemiology of urban dog-related injuries requiring rabies post-exposure prophylaxis in Marseille, France

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Epidemiology of urban dog-related injuries requiring

rabies post-exposure prophylaxis in Marseille, France

Philippe Gautret, Sèverine Le Roux, Benoıt Faucher, Jean Gaudart, Philippe

Brouqui, Philippe Parola

To cite this version:

Philippe Gautret, Sèverine Le Roux, Benoıt Faucher, Jean Gaudart, Philippe Brouqui, et al..

Epi-demiology of urban dog-related injuries requiring rabies post-exposure prophylaxis in Marseille, France.

International Journal of Infectious Diseases, Elsevier, 2013, �10.1016/j.ijid.2012.09.011�. �hal-01307685�

Epidemiology

of

urban

dog-related

injuries

requiring

rabies

post-exposure

prophylaxis

in

Marseille,

France

Philippe

Gautret

*

,

Se´verine

Le

Roux

,

Benoıˆt

Faucher

,

Jean

Gaudart

,

Philippe

Brouqui

_,

_Philippe

_Parola

a

InstitutHospitalo-UniversitaireenMaladiesInfectieusesetTropicales,HoˆpitalNord,AP-HM,ChemindesBourrelys,13915Marseille,cedex20,France b

EquipeBiostatistiques,LERTIM,Faculte´ deMe´decine,Marseille,France

1. Introduction

Dogbitesareaseriouspublichealthconcern.Besidesinjuries and the adverse psychological impacts, dog bites can be complicatedbyinfectionsincludingrabies,whichhasthehighest case-fatality rate of all infectious diseases.1 _{The last case of}

humanrabiesacquiredinmainlandFrancewasreportedin1924 andthelastcaseoffoxrabiesin1998.However,rabiddogsare repeatedlyimportedintoFrancebytravelers,withthemajority originatingfromMoroccoafterhavingbeentransportedthrough Spainbycar.2–6

The decision to prescribe rabies vaccine and/or rabies immunoglobulin to patients injured by dogs depends on the originoftheanimal.Over-prescriptionofrabiespost-exposure prophylaxis(PEP)hasbeenquestionedinFrance.7_InMarseille,

efforts to minimize over-prescription of the vaccination for

rabies PEP has been conducted, by delaying the initiation of rabiestreatmentininjuriesinvolvinganapparentlyhealthydog that can be kept under observation.8 However, significant numbers of rabies PEP vaccinations are still given to injured patientsduetothehighproportionofdogsthatcannotbekept under observation. In this context, interventions aimed at reducingthenumberofdogbitesare critical.Thereductionof dog-related injuries by educational interventions has shown some success in children,9,10 _{although this has been}

contra-dicted.11_{Asafirststeptowardsthepossibleimplementationof}

suchastrategyinMarseille,weconductedapreliminarysurvey todescribe the epidemiologyof dog-relatedinjuries requiring rabiesPEPinthecity.

2. Materialsandmethods

From 2007 to 2010, epidemiological data on dog-related injuriesandassociatedrabiesPEPtreatmentwereprospectively collectedfrompatientsattendingtheMarseillerabiestreatment center (RTC) using standardized forms. At the Marseille RTC,

ARTICLE INFO

Articlehistory:

Received16January2012

Receivedinrevisedform20April2012 Accepted26September2012

CorrespondingEditor:WilliamCameron, Ottawa,Canada

Keywords: Dogbites

Rabiespost-exposureprophylaxis Epidemiology

Riskfactors Spatialdistribution

SUMMARY

Background:Dogbitesareaseriouspublichealthconcern.Besidesinjuriesandtheadversepsychological impacts,dogbitescanbecomplicatedbyinfectionsincludingrabies,whichhasthehighestcase-fatality rateofallinfectiousdiseases.

Methods:Dog-associatedinjuriesoccurringinthecityofMarseille,Francewereinvestigatedin245 individualsamongpatientspresentingtotherabiestreatmentcenterovera4-yearperiod.

Results:Malepatientsweremorelikelytoreportdogbitescomparedtofemalepatients(66.5%vs.33.5%; oddsratio2.25,95%confidenceinterval1.72–2.93).Themeanageofinjuredpatientswas32years(range 1–85years).Childrenandyoungadultsunder30yearsofageweremorethanfourtimesmorelikelyto reportdogbitescomparedtoothers.Mostcasesoccurredoutdoors(73.0%)–inpublicareas(38.0%)–and involvedanimalsofunknownownersin 56.3%ofthecases.Only28.2%ofdogswereavailablefor observation.Mostpatients(63.7%)receivedcompleterabiespost-exposureprophylaxis.Thedistribution ofdogbitesinthecitywasnothomogeneousandtheincidenceofbiteswassignificantlyhigherinsome areas.Elevenpercentofpatientsdeclaredhavingbeenbittenbydogswhoseownerwasastreetbeggar, andaclustereddistributionwasevidencedforthesecasesinoneareaofthecity.

Conclusions: Programsofferinglow-costrabiesvaccinationandveterinarycaretopetsbelongingtothe groupofstreetbeggarsshouldbeconsidered.Suchprogramsmaybeimplementedinotherlargecitiesin FranceandEuropewherestreetbeggarsarefrequentlyseen.

ß2012InternationalSocietyforInfectiousDiseases.PublishedbyElsevierLtd.Allrightsreserved.

*Correspondingauthor.Tel.:+33(0)491963535/36;fax:+33(0)491968938. E-mailaddress:philippe.gautret@club-internet.fr(P.Gautret).

ContentslistsavailableatSciVerseScienceDirect

International

Journal

of

Infectious

Diseases

j o urn a l hom e pa ge : ww w. e l s e v i e r. c om/ l o ca t e / i j i d

1201-9712/$36.00–seefrontmatterß2012InternationalSocietyforInfectiousDiseases.PublishedbyElsevierLtd.Allrightsreserved.

mostpatientsarescreenedbytelephonecallwithaspecialized physiciansothatthosepatientsinjuredbydogsthatcanbekept under surveillanceare screened-outanddonot receiverabies PEP.Thesepatientswerenotincludedinoursurvey.Onlythose who were advised to visit the center when the responsible animal was not available for surveillance were included. Additionalpatientswhospontaneouslypresentedtothecenter werealsoincluded.Onlypatientswhohadbeeninjuredwithin the boundaries of the city of Marseille were selected. Demo-graphic and clinical data and rabies prophylaxis details are routinelydocumentedattheRTC.Additionaldatawereobtained retrospectively by telephone, when possible, regarding the detailed circumstances of the dog attack: characteristics of thedog’sowner,placeofexposurewithinthecity,environment, andreasonfor thebite.Interviewswere allconducted byone person.ThecityofMarseilleislocatedinthesouthofFranceand comprises16districts.Humandemographicdata(total popula-tion and distribution according to sex and age range) were extractedfromthe2007officialcensus(http://www.insee.fr).At thattime,thepopulationtotaled852396inhabitants.Climatic data wereobtainedfrom the Wundergrounddatabase(http://

www.wunderground.com).

Placeofexposureandplaceofresidenceweremappedusing QuantumGIS 1.6.0 software(OpenSource Geospatial Founda-tion).Thespatialdistributionofcasesaccordingtotheseason, the day of the week (weekend vs. working days), and thecategoryofowner(streetbeggars ornot)wasinvestigated using SaTScan software. To detect clusters, this software systematicallymovesacircularscanningwindowofincreasing diameter over the studied region and compares observed numbers inside the window to the numbers that would be expectedunderthenullhypothesis(randomdistributionofthe studied features). The maximum allowed cluster size corre-sponded to 50% of the study population. The statistical significanceforeachclusterwasobtainedthroughMonteCarlo hypothesistesting, i.e.,results ofthe likelihood functionwere comparedwith999randomreplicationsofthedatasetgenerated underthenullhypothesis.

Differencesinproportions(categoricalvariables)weretested byPearsontestsusingSPSS(SPSS,Inc.)softwarepackage.Ap-value of <0.05 was considered significant. Odds ratios (ORs) were estimated by logistic regression. All statistical tests were two-sided.ComparisonsofpercentagesandORswith95%confidence intervals (95% CI) were carried out using R2.8.1 environment (www.r-project.org).

3. Results

Atotalof245patientsinjuredbydogsinsidethecitypresented totheRTCbetween2007and2010.Themeanannualincidence was 0.71 per 1000 inhabitants, with no significant annual variation.

3.1. Demographics

The male to female sex ratio was 1.98 in the injured population compared to 0.88 in the whole population. Malepatients weremorethantwotimesmorelikelytoreport dog bites compared to female patients (66.5% vs. 33.5%; OR 2.25, 95% CI 1.72–2.93). The mean age of injured patients was32years(median29years,range1–85years).Individuals aged 0–29 years were over-represented among injured individuals(53.5%)comparedtothewholepopulation(38.7%), while those aged 30 years and over were under-represented

(Table 1); 75.9% of injured patients were over 15 years of

age.

3.2. Circumstances

In 44.9% of the cases, the dog’s owner was not identified becausetheanimalwasafree-roamingdog,orbecausetheowner refusedtoprovidetheir identityand address.No case ofa dog travelinginfromarabiesendemicareawasrecordedamongthose dogswhoseownerwasidentified.Oftheinjuredpatients,11.4% mentionedthatthedog’sownerwasastreetbeggar.Mostcases occurredoutdoors(73.0%)–inpublicareas(38.0%)–and29.8%of respondents thoughtthe dog attackedthem intentionallyafter they had interacted withtheanimal, out of thedog’s territory (Table2).

3.3. Spatialdistributionandtemporalandclimaticfactors

Themeanannualincidencevariedsignificantlyaccordingtothe place of exposure within the city, with 0.19 cases per 1000

Table1

PatientswithdogbiteinjuriespresentingtotheMarseillerabiestreatmentcenter, byagecategory,comparedtotheMarseillepopulation

Age (years) Injured patients % Inhabitants % OR 95%CI 0–14 59 24.1 154704 18.2 4.35 1.99–9.52 15–29 72 29.4 175000 20.5 4.69 2.16–10.20 30–44 46 18.8 173819 20.4 3.02 1.36–6.69 45–59 31 12.7 158051 18.5 2.24 0.98–5.08 60–74 29 11.8 111002 13.0 2.98 1.31–6.80 75 7 2.8 79820 9.4 1 0–0 Unknown 1 0.4 Total 245 100 852396 100 Table2

Detailsof245dogbiteincidentsinMarseille

Detailsofincidents n(%) Identificationofthedog’sowner

Identified 107(43.7)

Un-identified(free-roamingdogsandownersrefusingto providetheiridentityandaddress)

110(44.9)

Streetbeggars(individualssittingonthesidewalkand askingformoneyfrompeoplepassingby)

28(11.4)

Environment

Publicareas(streets) 93(38.0) Statefinancedapartmentcomplexarea(outdoors) 28(11.4) Victim’sorotherhome 21(8.6) Publicgardenordogpark 7(2.9) Naturereservearea 2(0.8)

Notdocumenteda _94(38.4)

Reasonforbiteasmentionedbythevictim

Intentionalbitefollowingvolunteerinteractionwithadog outofitsterritoryb

73(29.8)

Attackedbyadogwhilerunning 41(16.7) Unprovokedattack 29(11.8) Involvedinafightbetweendogs 20(8.2) Attackedbyadogwhileenteringthedog’sterritoryb _2(0.8)

Notdocumenteda _80(32.7)

Distancebetweenplaceofresidenceandhospital(km)

4 35(14.3)

5–9 70(28.6)

10–14 74(30.2)

15 50(20.4)

Notdocumented 16(6.5)

Bodysiteofinjury

Lowerlimbs 99(40.4)

Upperlimbs 89(36.3)

Multiple 24(9.8)

Headandneck 17(6.9)

Trunk 10(4.1)

Notdocumented 6(2.4)

a

Dataweremostlyobtainedbytelephoneinterview.Wewereunabletoreacha numberofpatientsandthereforetodocumenttheenvironmentandreasonforthe biteinthosecases.

b

Dogterritory=homeorgardenofthedogowner.

inhabitantsinthe9th_{district(southernpartofthecity)and2.43}

per1000inhabitantsinthe16thdistrict(northeastpartofthecity) (OR12.47,95%CI4.91–31.64).Themajorityofthoseinjuredinthe 16th_{districtwereresidentsofthatarea(Figure1;Supplementary}

Material,file1).Injuriescausedbydogswhoseownerwasastreet beggarweresignificantlymorefrequentlyreportedfromanarea centered on the 1st _{district, as shown in Figure 1 (OR 13.5,}

p<0.0001).ThedistancefromtheplaceofresidencetotheRTC waslessthan14kminmostcases(73.1%)(Table2).Inaddition, therewasnodifferenceindistributionofcasesaccordingtothe season,dayoftheweek,schoolperiod,windspeed,temperature,or lunarcycle(SupplementaryMaterial,files2and3).Therewasno significantspatialdistributiondifferencebasedonseasonordayof theweekwhentheinjuryoccurred(datanotshown).

3.4. Typeofinjuryandrabiespost-exposureprophylaxis

Mostinjuries(88.3%)weretrans-dermalinjuriesandlocalized tothelowerandupperlimbs.Overall,63.7% ofinjured patients receivedcompleterabiespost-exposureprophylaxis.Of245dogs, only 55 (22.4%) were available for surveillance by veterinary personnel and only 14 (5.7%) for surveillance by their owner, allowingtheavoidanceorinterruptionofpost-exposure vaccina-tionfornearlyallofthepatientsinjuredbythesedogs.Bycontrast, nearlyall patients injured by dogs whoseobservation wasnot feasible(71.8%)werevaccinated.

4. Discussion

TheexactnumberofdogbitesoccurringannuallyinFranceis unknown.Theannualincidenceofdogbitesseenintheemergency departmentsinFrancehasbeenestimatedataround0.03–0.05per 1000individualsaged<15years,accountingfortwo-thirdsofall dogbiteinjuriesseenintheemergencydepartment.12_InMarseille,

around50%ofinjuredpatientsarescreened-outbytelephonecall when the animal responsible can be kept under surveillance.8

Therefore,theactualannualincidenceofpatientsinjuredbydogs inMarseillethatarenotifiedtotheRCTisapproximately1.4per 1000inhabitants.Itiswellknownthatpatientsseekingcarefor rabies PEP following animal-related injuries represent a small proportionoftheactualnumberofinjuredpatients.13_Therefore,

theannualincidenceinourstudyverylikelyunderestimatesthe trueincidenceofdogbitesinthecityofMarseilleandourresults cannotbeextrapolatedtotheentirepopulationofdogbitevictims. Nevertheless,itprovidesusefulinformationtobettercharacterize thecircumstancesofdogbiteincidentsthatareseenatourcenter. Comparedtofemales,malepatientshadahigherlikelihoodof beinginjuredbydogs,asalreadyobservedbynumerousauthors.14

Whilemoststudieshaveindicatedthatthemajorityofdogbites occurinchildren,usuallyintheirownhome,andareinflictedby theirownpet,15,16_{oursurveyshoweddistinctresultswithmost}

casesoccurringnotonlyinchildren,butalsoinyoungadultsaged 15–29years,mostlyoutsidetheirhomeandinvolvinganimalsof

Figure1.Mapsshowing(A)thelocationofexposureand(B)theplacesofresidenceofinjuredpatientspresentingtotheMarseillerabiestreatmentcenter,and(C)thecluster ofbitesduetodogsownedbystreetbeggars(C).ThenumbersindicatethedistrictsofMarseille.

unknownownersinmostinstances(56.3%).Thisprobablyresults froma selectionbias,aspatientsinjuredbytheir owndogsare usuallytoldbytelephonetopostponetherabiesPEPwhiletheir dog is under observation. This further illustrates that the identificationofriskfactorsfordog-relatedinjuriesby epidemio-logicalsurveyslargelydependsonthesourceofdataandthatcare needstobetakenincomparingtheresults.17_{Ourresultssuggest,}

as reported by others,18 _{that dog bite prevention strategies}

teachingpeople to interactbetterwithdogsare unlikelyto be enoughtopreventtheseattacks,asonly29.8%didinteractwith their aggressor. On those occasions where the humandid not interactwiththedogthat bitthem,thefocusshouldbeon the owners,whomustbemadeawarethattheirdogcaninflictdamage tootherpeople,tofeelaccountableforthebehavioroftheirpet, and tobewillingtotake the necessarymeasurestoprevent it causing harmtoothers. However, inourstudy, halfofthedog ownerswereunidentified.

Thedistributionofcaseswithinthecityinoursurveyshouldbe interpreted with caution. The higher prevalence of dog bites requiringrabiesPEPinnorthwestMarseillemaybeduetoahigher densityofdogsin thatarea. Thedogpopulation inMarseilleis estimated to be around 100 000 animals; however, their distribution in the city is unknown. Alternatively, the higher prevalence of bites in individuals injured and living in the northwestarea mayresultfromthelocation oftheRCTin this partofthecity.TheRCTistheonlyplacewhererabiesPEPcanbe obtainedinthecityandthesurroundingarea.Ofmajorconcern,a clearclusterofdogbitecaseslinkedtodogswhoseownerwasa streetbeggarwasobservedaroundthe1st_{districtofMarseille,in}

thewest-centralareaofthecity.Inthiscase,thelocalizationofthe RTCcannotaccountforthespecificdistributionofstreetbeggar dog-relatedinjuries.Thisareaisthecommercialcenterofthecity withaconcentrationofshops,restaurants,andbars,andbeggars areusuallylocatedinthiszonebecauseitiseasiertobeg.Theexact numbers of street beggars in Marseille and of their dogs are unknown.Thenumberofstreetbeggars inFranceisdifficultto assess and the evaluations usually considered as mostreliable providenumbersof100000to200000,representinglessthan0.4% oftheentirepopulation.Thefactthat11.4%ofbitesinvolvedstreet beggar dogs in our study strongly suggests that this specific populationof dogsmayberelativelylarge in Marseille,orthat victimsofsuchdogsperceivedthemtobehigh-riskinrelationto possiblerabiesinfection.Furtherinvestigationsshouldbemadeto bettercharacterizethisgroupandtoidentifytheoriginofthedogs andpotentialillegalimportationfromrabies-endemicareas.

We failedtofindany temporal orclimatic variationsin the incidence of dog bites in our survey, which is in contrast to theresultsofotherinvestigators.19–21_{Norelationshipbetweenthe}

lunarphase andbiteincidencewasevidencedin oursurvey,as previouslyshownbyothers.20,22

Themainfindingsofoursurveyarethatmorethanhalfofthe dogbitesoccurringinthecityofMarseillethatrequiredrabiesPEP involvedanimalsofunknownownersandthatmorethan11%of bitevictimshadbeenbittenbydogsbelongingtostreetbeggars. Also,aclustereddistributionwasevidencedfortheselattercases in one area of the city. Based on our results, educational interventionsinchildrenwouldnotbeveryefficientinreducing thenumber ofrabiesPEPtreatmentsinMarseille.Interventions targetingstreetbeggardogscouldbeofsomeinterest,although suchdogsonlyaccountforasmallpartofthebitesleadingtorabies PEP.Frenchlawrequiresthatdogsarekeptontheleadinpublic areas.Frenchregulationsalsorequirethatdogsimportedfroma rabiesendemic areaarevaccinated againstrabiesandlicensed;

however,itisnotmandatorytovaccinateandlicensedogsbornin mainland France with the exception of Staffordshire (pit bull) terriers, boerboels, the Japanese tosa, and rottweilers. Street beggarsmaynotbeabletoaffordtherabiesvaccinefortheirpets. Programsofferinglow-costrabiesvaccinationandveterinarycare topetsbelongingtothisgroup,aswellasemphasizingtheneedfor theownerstokeeptheirpetsontheleash,shouldbeconsidered. SuchprogramsmaybeimplementedinotherlargecitiesinFrance andEuropewherestreetbeggarsarefrequentlyseen.

Conflict of interest: None of theauthors of this paper hasa financialorpersonalrelationshipwithotherpeopleor organiza-tionsthatcouldinappropriatelyinfluenceorbiasthecontentofthe paper.

AppendixA. Supplementarydata

Supplementarydataassociatedwiththisarticlecanbefound,in theonlineversion,athttp://dx.doi.org/10.1016/j.ijid.2012.09.011. References

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