Autochthonous liver cystic hydatid: Past or actual French shepherd's disease?

HAL Id: hal-02870087

https://hal-amu.archives-ouvertes.fr/hal-02870087

Submitted on 30 Jun 2020

HAL is a multi-disciplinary open access

archive for the deposit and dissemination of

sci-entific research documents, whether they are

pub-lished or not. The documents may come from

teaching and research institutions in France or

abroad, or from public or private research centers.

L’archive ouverte pluridisciplinaire HAL, est

destinée au dépôt et à la diffusion de documents

scientifiques de niveau recherche, publiés ou non,

émanant des établissements d’enseignement et de

recherche français ou étrangers, des laboratoires

publics ou privés.

Distributed under a Creative Commons Attribution| 4.0 International License

Autochthonous liver cystic hydatid: Past or actual

French shepherd’s disease?

Florent Darriet, Nadim Cassir, David Birnbaum, Jérôme Soussan, Estelle

Menu, Stephane Ranque, Coralie L’ollivier

To cite this version:

Florent Darriet, Nadim Cassir, David Birnbaum, Jérôme Soussan, Estelle Menu, et al.. Autochthonous

liver cystic hydatid: Past or actual French shepherd’s disease?. IDCASES, 2020, 21, pp.e00843.

�10.1016/j.idcr.2020.e00843�. �hal-02870087�

Case

report

Autochthonous

liver

cystic

hydatid:

Past

or

actual

French

shepherd's

disease?

Florent

Darriet

,

Nadim

Cassir

,

David

J.

Birnbaum

,

Jérôme

Soussan

,

Estelle

Menu

,

Stéphane

Ranque

,

Coralie

L

_’Ollivier

*

a

IHU-MéditerranéeInfection,Marseille,France

b

Aix-MarseilleUniversitéUM63,InstitutdeRecherchepourleDéveloppementIRD198,AssistancePublique–HôpitauxdeMarseille(AP-HM),Microbes, Evolution,PhylogenyandInfection(MEFI),Marseille,France

c_{DepartmentofDigestiveSurgery,HôpitalNord,AssistancePublique-HôpitauxdeMarseille,Aix-MarseilleUniversity,Marseille,France} d

DepartmentofRadiology,NorthUniversityHospital,ChemindesBourrely,13015,Marseille,France

e

AixMarseilleUniv.,IRD,AP-HM,SSA,VITROME,IHU-MéditerranéeInfection,Marseille,France

ARTICLE INFO Articlehistory: Received9March2020

Receivedinrevisedform22May2020 Accepted22May2020 Keywords: Hydatidosis French Indigenous Shepherd ABSTRACT

AutochthonoushydatidosisinFranceandwesternEuropaareuncommonsincethebeginningofthe21st century.WereporthereanauthenticindigenouscysticechinococcosiscaseinaFrenchshepherd.Therisk ofremergingpathologyshouldnotbeneglectedandmeasurestointerruptparasitetransmissionarestill relevant.

©2020TheAuthor(s).PublishedbyElsevierLtd.ThisisanopenaccessarticleundertheCCBYlicense (http://creativecommons.org/licenses/by/4.0/).

Introduction

Echinococcus granulosus is a cestode of the Tæniidæ family which mainlyinfects domestic dogs asa permanent host. It is transmitted to a wide range of intermediate-host domestic ungulates(e.g.,sheep, goats,cattle, camels,and cervids)which harbor the hydatid cysts [1]. Cystic echinococcosis (CE) is an importantzoonoticparasiticinfectionthatcausesmorbidityand mortalityinhumans.Humansbecomeinfectedbyingestingeggs from contaminated food or water, or from direct contact by handling infected dogs or their egg-containing feces [2]. CE is usuallyasymptomatic: the developmentof thelarvae occurred most commonly in the liver (50–70 % of cases) [3], and less commonlyinthelungs(20–30%),spleen,kidneys,brainandheart [4].Nevertheless,theinfectionmaybecomesymptomaticifthe cystseitherbreakorexertamass-effect.

HydatidosishasaworldwidedistributionfromtropicaltoArtic areas[5]. It typically occursin poor pastoral regions,in which sheeporotherlivestockareraisedandinwhichdogsarekept,for herdingorpropertyguarding,incloseproximitytohouseholds.In

Europe,publisheddatasuggestthattheprevalenceisratherhighin someregionsinItaly,SpainandeasternEuropa[6].InFrance,the annualincidenceofhumanCEcasesofhasbeenestimatedat260 hospitalizedpatients[7].Thesoutheastarea,especially Provence-Alpes-Cote d’Azur and Corsica regions, is the historically CE endemicareaknowninFrance.Becausenomandatorymonitoring program of human CE infections exists in France, the relative proportionofimportedorindigenouscasesisimpossibletoasses. Indeed,thisareaisrelativelyclosefrom3hyperendemicCEareas, namely Spain, Italy and Northern Africa. Apparently, French autochthonouscasesamongshepherdsbecameclearlyuncommon withoutreportsincetheendofthe20thcentury,sothatlocalCE seemed tohavedisappeared.Here, wereportanindigenousCE caseinaFrenchshepherd.

Casereport

In June 2017, a78-year-old Frenchman,was hospitalized for episodic pain in the right hypochondrium for one month. His medicalhistoryincludedprostatelocalresectionin2013,inguinal herniaanddailybothalcoholdrinkingandtobaccosmoking.The patientwasatraditionalshepherdwhonevertraveledoutsidethe South-EastofFrance.Hehaddailycontactwithsheep,sheepdogs, donkeys,horsesandcats.Physicalexaminationrevealedapainful mass in the right hypochondrium. Computed tomography and

* Correspondingauthorat:IHU–MéditerranéeInfection,19-21BoulevardJean Moulin,13005,Marseille,France.

E-mailaddress:coralie.lollivier@ap-hm.fr(C.L’Ollivier).

https://doi.org/10.1016/j.idcr.2020.e00843

2214-2509/©2020TheAuthor(s).PublishedbyElsevierLtd.ThisisanopenaccessarticleundertheCCBYlicense(http://creativecommons.org/licenses/by/4.0/).

IDCases21(2020)e00843

ContentslistsavailableatScienceDirect

IDCases

magneticresonanceimagingscanshowedthreelivercysts,located insegmentsIV,VandVI(Fig.1),thatwereclassifiedfollowingthe WHOstandardizedUSclassificationsintwoCE5cystsized5cm and a bi-vesicular CE3b cyst sized 10cm, respectively. No remarkablebiologicalparameterswerefound,withtheexception of a 78mg/L C-reactive protein level (N<5mg/L). Hydatidosis serologywasnegative.

BasedonCT-scanimages,adiagnosisofliverhydatidcystwas retained.Thepatientreceivedalbendazole(ABZ)400mgtwiceper dayforsixmonths.ABZwasstoppedtemporarilyduringacourse of 2 monthsbecause oflymphopenia. Thefollow-up showed a suspectedpre-ruptureofthelargestcyst:theserologyswitchedto positive,thusprecipitatingthedecisionofsurgicaltreatmentby resectionoftheprotrudingdomeinMarch2018.Thepostoperative biologicalexaminationofthepuncturefluidrevealedscolexand typicalhooklets(Fig.2).MoleculartestbasedonthecytochromeC oxidase subunit1 nucleotidesequence hasmade it possibleto identifyEchinococcusgranulosussensustrictogenotypeG1(99%on genebank:HF947568.1).ABZtreatmentwascontinueduptoMay 2018. At 2 months of follow-up, the patient had no pain and CT-scanimagesshowedonlythe4cmcalcifiedcystinsegmentIV. Discussion

In western Europe, helminthiasis are usually diagnosed in migrantsortravelers[8]asindigenouscasesarescarce.HumanCE casesinFrancearenotanexceptiontotherule.Umhangetal.[9] found low prevalence of E. granulosus (4/100,000 sheep and 3/100,000cattle)atslaughterhousesinsouthernFrance.Despite thisfact,onlyonehumancase[10]hasbeenreportedfromthis majorhistoricalendemicareawithinoverthepasttwodecades. Also, humanCE areusuallyimportedcases; mainlyfromSpain, ItalyandNorthernAfrica.Thispresentreporthighlightsthefact thatautochthonousCEisstillpresent,especiallyamongshepherds who practice transhumance in the mountain pastures that is, movinglivestock ina seasonalcycletypically tolowland inthe winterandhighlandsinthesummer.Thecarcassesofsheepthat dieonthewaycanbeavailableforthesheepdogs.

ThenationalsurveyofUmhangetal.[9]demonstratedthatCEis endemicinlivestock. Furthermore,rarehumancaseshavebeen reportedinFrance[10,11]inrecentyears.Allthesedataconverge towardstheevidenceoftheparasite’sdevelopment atdifferent stagesofitslifecycleinFrenchruralarea.Nevertheless,thereisno largedataavailableonCEinsheepdog.Itisadmittedthatkeyto successofCEcontrolistheremovalofwormbiomassindog,by interruptingtheparasitelifecycleandreducinghumanexposure [12]. Praziquantel (5mg/kg), the anthelminthic agent used to dewormingdogshasneitheraresidualnoranovicidaleffect,and shouldthusbepreferablyadministeredeachsixweekstoprevent eggoutput.Ahealtheducationprogramonhygiene,deworming anddogscontacttargetingshepherdswouldalsobeofinterestin implementinginCEendemicareasinFrance.

The genotypesG1, G2 and G3 of E. granulosusstricto senso (recoveredfromsheep)areendemicinsouthofFrance.Inlinewith thesedata,thegenotypeG1wasinvolvedinthispatient’scyst.The standardizedclassificationofCEproposedbytheWHO-Informal WorkingGrouponEchinococcosis(WHO-IWGE)[13]definedsix cyst stages assigned to three clinical groups (Table 1). This classificationprovidesarationalbasisforchoosinganappropriate CE treatment schemeand follow-up,i. e.surgery,percutaneous treatmentsuchasPAIR(puncture,aspirate,injection,re-aspirate),

Table1

SimplifiedclassificationofliverhydaticcystsaccordingtotheWHOinformalworkinggroup[13]. Stagesofcysts Clinicalgroup Imaging(ultrasound)features

CL active Unilocularcyst,anechoïc,nowalldepicted

CE1 CLcharacteristics+“snowflake”signs

CE2 Multivesicular(daughter)cystsassociatedwith“wheel-like”“rosette-like”or“honeycomblike”structures CE3a

transitional Detachmentoflaminatedmembrane+“water-lilysign”

CE4 inactive Heterogenoushypoechoiccyst

CE5 CE4characteristics+athickcalcifiedwall

a_{CE3cystshavebeenfurtherdividedintoCE3a(activeorinactive)andCE3b(active).}

Fig.2.PuncturefluidwithtypicalhookletsofEchinococcusgranulosus. Fig. 1.Magnetic resonance imaging. Coronal section in T2-weighted pulse sequence.Cysticbilobatelesionwithexophyticpart.WHOClassification:CE3a: Liquidcystwithdetachedmembraneappearance.

albendazolechemotherapyor‘watch&wait’(WW).Ourpatient presented with 3 cysts, two classified CE5 and one CE3b. Conventionally, WW is appropriate for uncomplicated inactive CE5cyst [14], whereas management of transitional CE5cyst is unclear.Rinaldietal.showedthatseveralmonthsABZtreatment inducesCE3bcystsinactivation.Inthispresentcase,thepatient wastreatedbyABZduring6months.However,duringthe follow-up,evidenceofcyst’spre-rupture,includingtheseroconversionof bothELISAandimmune-blottingtests,posedathreatofsecondary hydatidosis and anaphylactic shock triggered by the release of viablecontentoftheCE3bcyst.Itisimportanttonotethatthis 10cm long cyst was at risk of rupture [14] and that the recommendationsaretopromotesurgicaltreatmentandtoavoid PAIR procedure [15]. Therefore, the patientstreated by a long courseofABZtherapyshouldberegularlyfollowed-uptoassess bothadverseevents(i.e.alopecia,livertoxicity,and agranulocyto-sis)andcystleakage.

This patient’s case, associated with the other reported indigenouscasesinwesternEurope,highlightthatCEriskpersists intheseruralareas.Therefore,somerecommendedmeasuresto interrupt parasite transmission are still relevant, including: controllinglivestockslaughtering,properdisposalofoffal particu-larlyviscera,regulardeworming ofdogswith praziquanteland vaccinationofintermediatehosts[12].Autochthonousorimported hydatidosis in France should not be neglected. Indeed, the management of patients withCE requiresa skilledand expert medicalstaff.

CRediTauthorshipcontributionstatement

Florent Darriet: Writing - original draft. Nadim Cassir: Resources,Visualization.David J.Birnbaum:Resources.Jérôme Soussan:Resources.EstelleMenu:Resources.StéphaneRanque: Supervision.CoralieL’Ollivier:Writing-review&editing. DeclarationofCompetingInterest

Allauthorsdeclareanyconflictsofinterestorsourcesoffunding

Acknowledgement None.

References

[1]CarmenaD,CardonaGA.Canineechinococcosis:globalepidemiologyand genotypicdiversity.ActaTrop2013;128(December(3)):441–60.

[2]McManusDP,ZhangW,LiJ,BartleyPB.Echinococcosis.Lancet2003;362 (October(9392)):1295–304.

[3]BhutaniA,KajalP.Hepaticechinococcosis:areview.AnnMedSurg(Lond) 2018;36(November):99–105.

[4]FiengoL,BucciF,GiannottiD,PatriziG,RedlerA,KucukaksuDS.Giantcardiac hydatidcystinchildren:casereportandreviewoftheliterature.ClinMed InsightsCaseRep2014;7(September):111–6.

[5]DeplazesP,RinaldiL,AlvarezRojasCA,TorgersonPR,HarandiMF,RomigT, etal.Globaldistributionofalveolarandcysticechinococcosis.AdvParasitol 2017;95:315–493.

[6]Dakkak A. Echinococcosis/hydatidosis: a severe threat in Mediterranean countries.VetParasitol2010;174(November(1–2)):2–11.

[7]VanCauterenD,MillonL,DeValkH,GrenouilletF.Retrospectivestudyof humancysticechinococcosisoverthepastdecadeinFrance,usinga nationwidehospitalmedicalinformationdatabase.ParasitolRes2016;115 (November(11)):4261–5.

[8]Zammarchi L, VellereI, Stella L, BartalesiF,Strohmeyer M,Bartoloni A. Spectrumandburdenofneglectedtropicaldiseasesobservedinaninfectious andtropicaldiseasesunitinFlorence,Italy(2000–2015).InternEmergMed 2017;12(June(4)):467–77.

[9]UmhangG,RichommeC,BoucherJM,HormazV,BouéF.Prevalencesurveyand firstmolecularcharacterizationofEchinococcusgranulosusinFrance. ParasitolRes2013;112(April(4)):1809–12.

[10]TourneM,DupinC,MordantP,NeuvilleM,TailléC,DanelC.Kystehydatique pulmonaireautochtone.AnnPathol2019;39(February(1))47–53French. [11]BassetD,FrapierJM,DedetJP,GrolleauR.Autochthonouscardiachydatidcyst

offavorableoutcome.PresseMed2000;29(June(21))1175French. [12]CraigPS,HegglinD,LightowlersMW,TorgersonPR,WangQ.Echinococcosis:

controlandprevention.AdvParasitol2017;96:55–158.

[13]WHO Informal WorkingGroup. Internationalclassification of ultrasound imagesincysticechinococcosisforapplicationinclinicalandfield epidemiologicalsettings.ActaTrop2003;85(February(2)):253–61. [14]RinaldiF,DeSilvestriA,TamarozziF,CattaneoF,LissandrinR,etal.Medical

treatmentversus"WatchandWait"intheclinicalmanagementofCE3b echinococcalcystsoftheliver.BMCInfectDis2014;14(September):492. [15]Stojkovic M, Weber TF, Junghanss T. Clinical management of cystic

echinococcosis:stateoftheartandperspectives.CurrOpinInfectDis 2018;31(October(5)):383–92.