Study of the intra-prostatic arterial anatomy and implications for arterial embolization of benign prostatic hyperplasia

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ORIGINAL ARTICLE

Study of the intra-prostatic arterial anatomy and implications for arterial embolization of benign prostatic hyperplasia

Étude de la vascularisation intraprostatique appliquée à l’embolisation des artères prostatiques comme traitement de l’hyperplasie bénigne de prostate

J. Anract

, G. Amouyal

, M. Peyromaure

,

M. Zerbib

, M. Sapoval

, N. Barry Delongchamps

aServiced’urologie,hôpitalCochin,163,boulevarddePort-Royal,75014Paris,France

bServicederadiologieinterventionnelle,hôpitaleuropéenGeorges-Pompidou,20,rue Leblanc,75015Paris,France

Received7December2018;accepted14February2019 Availableonline1April2019

KEYWORDS Prostate;

Hyperplasia;

Embolization;

Adenoma;

Arterialanatomy

Summary

Introduction.—Prostaticarterialembolization(PAE)isanexperimentaltherapyforbenignpro- statichyperplasia.Itsfeasibilityisbasedontheknowledgeofthepelvicarterialanatomy,and more specificallythe prostate.The aimofthis study wasto describetheprostatic arterial supply:origins,distributionandvariability.

Materialandmethods.—Wereviewedretrospectively,withtworadiologists,40arteriographies ofpatientswhounderwentPAEinourcenter.Withtheseobservationsof80hemipelvics,we describedthenumberofprostaticarteries,theirorigins,theirdistributionsandeventuallytheir anastomoseswithotherpelvicarteries.

Results.—Therewasoneprostaticarteryin70%ofthecases.Itcamefromacommontrunk fortheprostateandthebladderin55%ofthecases,fromtheobturatorarteryin17.5%ofthe cases,fromthepudendalarteryin25%ofthecases,fromtheinterniliacarteryin1%ofthe cases,andfromthesuperiorglutealarteryin1%ofthecases.Theprostaticarterysplittedin twobranches(medialandlateral),withnoanastomosesin37%ofthecases.Anastomoseswith penileandrectalarterieswereobservedin29%ofthecases.

∗Correspondingauthor.

E-mailaddress:juanract@me.com(J.Anract).

https://doi.org/10.1016/j.purol.2019.02.007

1166-7087/©2019ElsevierMassonSAS.Allrightsreserved.

Conclusions.—Forour40patients,weobservedmanyvariationsofarterialprostaticanatomy.

WeproposedaclassificationinordertoincreasesecurityandefficacyofPAE,anditshouldbe validatedwithmorepatients.

Levelofevidence.—2.

©2019ElsevierMassonSAS.Allrightsreserved.

MOTSCLÉS Prostate; Hyperplasie; Embolisation; Adénome; Vascularisation

Résumé

Introduction.—L’embolisationdesartèresprostatiques(EAP)estuntraitementexpérimental del’hyperplasiebénignedelaprostate.Safaisabilitéreposesuruneconnaissanceprécisede lavascularisationprostatique.L’objectifprincipaldecetravailétaitdoncdedécrirelavascu- larisationartérielleintraprostatique,deprécisersesorigines,sadistributionetsavariabilité.

Matérieletméthodes.—Nousavonssélectionnérétrospectivementlesartériographiespelvi- ennesde40patientstraitésparEAPdansnotrecentrehospitalo-universitaire.Celles-ciontété reluespardeuxradiologues.Pourchacunedes80hémi-vascularisationsprostatiquesétudiées, nousavonsdécritlenombred’artèresprostatiques,leurorigine,leurmodededivisionetleurs anastomoseséventuellesavecd’autresartèresdupetitbassin.

Résultats.—L’artèreprostatiqueétaituniquedans70%descas.Sonorigineétaitobservéeau niveaudutroncantérieurdel’iliaqueinternedans55%descas,del’obturatricedans17,5% descas,del’artèrepudendaleinternedans25%descas,del’artèreiliaqueinternedans1% descas,etdelaglutéalesupérieuredans1%descas.L’artèreprostatiquesedivisaitenune branchemédialeetunebranchelatérale,sansanastomosedans37%descas.Desanastomoses avecdesartèresdupénisetdurectumontétéobservéesdans29%descas.

Conclusions.—Chezles40patientsétudiés,ladistributiondesartèresprostatiquesétaithaute- mentvariable.Notreclassificationapourambitiond’augmenterlasécuritéetlafaisabilitéde l’EAP,etdoitêtrevalidéesurunnombreplusimportantdepatients.

Niveaudepreuve.— 2.

©2019ElsevierMassonSAS.Tousdroitsr´eserv´es.

Introduction

Prostaticarterialembolization(PAE)iscurrentlyundereval- uation for the treatment of benign prostatic hyperplasia (BPH). The first feasibility study has been published by Carnevaleetal.in2010 [1].Sincethen, tworanbdomised controlled trials suggested that the functionnal improve- mentafterPAEwasnotinferiortotransurethralresectionof theprostate(TURP)[2,3].However,thisprocedureistech- nicallydifficultandabetterknowledgeofprostaticarterial vascularizationisrequiredforitsdevelopment.

Autopsy studiesshowed alarge variabilityof originsof theprostaticartery[4].Otherstudiesshowedseveralpedi- cles, and anastomotic plexus with other pelvic arteries [5]. Recently, Amouyal et al. analysed for the first time intra-prostaticarterialvascularizationanddescribedthree distributionmodesoftheprostaticartery[6].

Theaimofourworkwastodescribethenumberofpro- static arteries, their origins, their distribution mode and anastomoticbounds.Ourobservationsweremadeusingret- rospective arteriographic analysis of patients treated by PAE.

Thesecondobjectivewastoproposeavalidation,based onour results, of the classification proposed by Amouyal etal.[6].

Patients and methods Population studied

Between December 2013and July 2014, 40male patients weretreatedbyPAEforBPHinourcenter.Inclusioncriteria were:malepatients>50yearsold,lowurinarytractsymp- toms(LUTS)duetoBPH,prostatevolume>40mL.Exclusion criteria were:bladder diverticula or bladder stone, renal failure,orsuspisionofprostatecancer.

PAE

PAE protocol was standardized. The right femoral artery was catheterized.Arterial prostaticcartography was per- formed usingcone-Beam CT-scan,aftercatheterisation of theinterniliacartery.Embolizationprocedurestartedwith selective catheterism of the left prostaticartery. In case of extra-prostatic anastomotic bound, targeted zone was protected by distal dropping of micro coils or resorbable gelatine. This technique allowed to protect anastomoses whilemaintainingopenprostaticfeedingvessels.Emboliza- tion of the prostatic artery was performed using the PErFectEDtechniquedescribedbyCarnevaleetal.[1]:prox- imalembolization withmicroTrisacryl spheresdroppedin

medial and lateral branches; second embolization in the distalpartofthemedialbranchwhenpossible.

Arteriographic analysis

Arteriographic images were saved on the intranet of our center.Weretrospectivelyreviewedimagesof40patients, previouslyanonymised,withtworadiologistswithmorethan twoyearsofPAEexperience.Theobjectivewastodescribe precisely,foreachpatientandeachside:

• theoriginoftheprostaticartery;

• numberofprostaticartery(ies);

• thedistributionmodeoftheprostaticartery;

• extra-prostaticanastomosisandtheanatomicregioncon- cerned.

Dataaboutthenecessityofadistalprotection(incaseof extra-prostaticanastomosis)andthepossibilityofasecond distaldropping(PErFectED)wereprospectivelycollected.

Statistical analysis

Qualitativedatawereshownwithabsolutevaluesandpro- portions.Quantitativedatawereshown inabsolutevalues andmeans.

Results

Allpatients were included in thefinal analysis. Meanage was69.5years(56;88).Meanprostaticvolumewas95.7mL (40;210).Prostaticarterialvascularizationbeingbilateral, 80vascularizationmodeswereanalysed.

Origins of the prostatic artery

The differentoriginsof theprostaticarteryweresumma- rizedinTable1.

Acommonarterialtrunkforprostateandbladder(ante- riortrunk)takingitsoriginfromtheinterniliacarterywas observedin44(55%)cases.Thisanteriortrunkdistributed onearteryforthebladderandonefortheprostate.Theone for theprostate, going obliquelydownwardly towards the medialline,gaveonitsproximalpartthehomolateralsemi- nalvesicleartery,andthebranchesfeedingthehomolateral hemi-prostate.

In20(25%)othercases,theprostaticarterytookitsorigin fromthe intern pudendal artery.In 14 (17.5%) cases, the prostaticarterytookitsoriginfromtheobturatorartery.It tookits origin fromthe commontrunk of the intern iliac

Table1 Originsoftheprostaticartery.

Originsofprostaticartery n %

Anteriortrunk 44 55

Obturatory 14 17.5

Internalpudendal 20 25

Internaliliac 1 1.25

Superiorgluteal l 1.25

Total 80 100

arteryin one (1.25%) case, andfrom the superiorgluteal arteryinoneothercase(Fig.1).

Number of prostatic arteries

In 58 (72.5%) cases, prostatic artery was unique. In 21 (26.25%)cases,weobservedanaccessoryprostaticartery.

Inonecase(1.25%),thereweretwoaccessoryarteriesasso- ciatedtothemainone.Theseaccessoryarteriestooktheir originfromtheintern pudendalarteryin 8(36.4%)cases, theobturatorarteryin7(31.8%)cases,andfromtheante- riortrunk (commontrunkdistributing theinferiorbladder arteryandtheprostaticone)in7(31.8%)cases.However, theaccessoryarterywasalwaysgoingobliquelydownwardly towardstheapex,afteradistalorigincomparedtothemain one.

Distribution modes

In 30 (37.5%) cases, prostatic artery distributed two branches.We observedthearterialdivisionatthe periph- eralandbasal partof the prostate. Afirst medialbranch wenthorizontallytotheprostaticurethra,alongthebasal part,underthebladderneck.Asecondlateralbranchwent obliquelydownwardlytowardstheapex,alongtheprostatic capsule,withnoanastomotic boundvisible witharteriog- raphy. This lateral branch gave a third one in 6 cases, goinghorizontallyalongthelowerpartofthemedialbranch towardsthetransitionalzoneoftheprostate.Inonecase, this third artery took its origin from the prostaticartery directly.

We observed extra-prostatic anastomoticbounds in 23 (28.7%)cases.Mostly,theboundstooktheiroriginsfromthe lateralbranchoftheprostaticartery(18ofthe23cases,so 78.2%).Rarely,theytooktheiroriginsfromtheproximalpart oftheprostaticartery,beforedistributingthemedialand lateralbranches(5of,so21.7%).Theseanastomoticbounds fedtwoareas: penisvia thecavernous artery(39.1%)and rectumviamiddlerectalartery(60.9%).

In16(20%)cases,weobservednodivisionoftheprostatic artery, but a unique artery going obliquely downwardly towardsthemedialline,tothemedianpartoftheprostate, and then distributing multiples branches going threw the prostatebyacentripetalspreading.

Classification

Our findings can be summarized in five typical cases, dependingonthedistributionmodeoftheprostaticartery andpresenceofextra-prostaticanastomoticbounds:

• type A: division of prostatic artery in two branches, medial andlateral, without any extra-prostatic anasto- moticbound(Fig.2);

• typeB:divisionofprostaticarteryinonemedialbranch andonelateralbranch,withathirdbranchfeedingthe transitional zone of the prostate. This third artery can take itsoriginfromthelateralbranch (B1,represented onFig.3),orfromtheprostaticarterybeforethedivision (B2,representedonFig.4);

• typeC:auniqueprostaticarterydistributingsmallmulti- plescentripetalbranches(Fig.5);

Figure1. Variabilityoforiginsoftheprostaticartery.Everysituationispointedbyanarrowandthenumberexpressthefrequency(%).

Figure2. DistributionoftypeA.

• typeD:extra-prostaticanastomoticbound,homo-orcon- trolateralwithacavernousarteryofthepenis(Fig.6);

• typeE: extra-prostaticanastomoticbound,homolateral with the middle rectal artery. This bound can take its origin: right from theprostatic artery(E1, represented onFig.7)oratthedistalpartofthelateralbranch(E2, representonFig.8).

Wecouldapplythisclassificationfor69ofthe80cases (86.25%),11ofthempresentingarteriographicreadingdif- ficulties. Prevalence of each cases (A, B, C, D, E) are

Figure3. DistributionoftypeB1.

summarizedinTable2.PrevalenceofdifferentBtypesare summarizedinTable3,andEtypesinTable4.

Annex1presentarecapitulativetableofthedistribution modesobserved.

Discussion

Ourfindingsoftheoriginsoftheprostaticarteryalignwith commonknowledge. In ourstudy,themost frequent situ- ationis the origin ofthe prostaticarteryfroma common trunkdistributingbranchesforbladderandprostate(ante- riortrunk,55%ofthecases).Theoriginfromthepudendal

Figure4. DistributionoftypeB2.

Figure5. DistributionoftypeC.

Figure6. DistributionoftypeD.

arteryorfromtheobturatorarteryarethemostfrequent variationsintheliterature[7],asinourpopulation.

In30%ofthecases,weobservedanaccessoryprostatic artery feeding the inferior part of the prostate. De Assis etal.[8]findlessthan10%ofdoublevascularizationintheir work.This differencecanbeexplainedbya smallpopula- tionsampleorbyvariationsofthearteriographicreading.

Figure7. DistributionoftypeE1.

Figure8. DistributionoftypeE2.

Table2 FrequencyofcasesA,B,C,DandE.

Type n %

A 23 28.75

B 7 8.75

C 16 20

D 9 11.25

E 14 17.5

Unclassified 11 13.75

Total 80 100

The prevalence of double vascularization should be con- firmedin futureworks,todiscussthebenefitof adouble embolization.

Before the arteriography era, only one autopsy study described distribution of the prostatic artery [5]. This descriptionfitstoour typeA,which is themost frequent

Table3 FrequencyofB1andB2.

Btype n %forn=14 %forn=80

B1 6 86 7.5

B2 1 14 1.25

Total 7 100 8.75

Table4 FrequencyofE1andE2.

Etype n %forn=14 %forn=80

E1 9 64 11.25

E2 5 36 6.25

situation(28.75%inourpopulation).Novariationoranasto- moticboundsweredescribedatthetime.

Among all the work using arteriography to describe arterial prostatic vascularization [6,8,9], only Amouyal described the distribution of the prostatic artery [6].

Amouyal described 3 subtypes: a presenting a prostatic arteryfeeding only the prostate, Bpresenting an anasto- moticboundwiththerectum,andCwiththepenis.These resultsarefittingwithours.

However, we tried to be more specific about the intra-prostatic distribution,and we isolatedfivedifferent situations. Type A fits the situation described by Garcia- Monaco[5]and then Amouyal[6]. Itis themost frequent situationobservedintheseworks,includingours,andseems tobethemodalsituation.TypesAandBarecloses,theonly differencebeingthethirdbranchintheBtype,feedingthe transitionalzone in the central part of the prostate. The onlydifferencebetweensubtypesB1andB2istheoriginof thisthirdbranch.

D and E types presents an extra-prostatic anastomotic bound, like the two last types described by Amouyal. D type presents an anastomoticbound between the lateral branchandacavernousartery,whileEtypepresentananas- tomoticboundwiththe homolateralmiddle rectalartery.

WeobservedtwosubtypesofE,dependingontheoriginof the boundwith the rectalartery: directly from the main prostaticartery(E1)orfromthelateralbranch(E2).

To the best of our knowledge, C type were never describedintheliterature.Itseemstobeaspecificanatom- icalvariation,becauseitdoesnotpresentaprecisedivision oftheprostaticartery,butamainonedistributinganarchic smallbranchesatitsdistalpart.

These results provide several perspectives for clinical practice of PAE, first concerning its safety. If an extra- prostaticanastomoticboundisfoundduringtheprocedure, a protection with resorbable coil or gelatine should be placed.Therefore,typeDandEpatientsshouldalwaysget theprotectionprocedure.However,weobservedthat77.7%

ofthetypeDhemi-pelvisofourpopulationdidgetthispro- tectionprocedure,andonly35.7%ofthetypeEhemi-pelvis.

Ourmain hypotheseswasthat theboundwasnotactually seenduringtheprocedure,butonlyduringthesecondread- ingforourstudy.Thiscouldbeexplainedbytheexperience oftheradiologists,superiorat thetimeof thestudythan theprocedure.

Furthermore, concerning the E types, for which we observed only 35.7% of protection,we calculated propor- tionsofsubtypesthatwereprotected(E1andE2).In80%

ofthecases,subtypesE2wereprotected, butonly11.1%

ofE1.Thiscouldbeexplainedbytheoriginoftheanasto- moticbound:E2presentsananastomosisatthedistalpartof thelateralbranch,asintypeD.The20%ofnon-protected E2 types werecaseswith‘‘proximal’’ selectiveemboliza- tion of themedial branch. In thosecases, theradiologist didnotembolizethelateralbranchonpurpose(andsothe rectalbranch),scarifyingsomebranchesgoingfor mostof themtotheperipheralzone.Thisdecisionwastakenwhen thediametersofthedistalbranchesweresmallercompared to thosefrom the medial branch. In thesesituations, we wereexposed tothe riskof majorrefluxof themicropar- ticlesinthelateralbranchduringtheprocedure.Nomajor complicationswerereported.

However,the89%ofnon-protectedE1subtypescanbe explainedby theorigin of theanastomosiscommon trunk of the prostatic artery. Therefore, the distal part of the cathetercouldbeplaced intheprostaticartery afterthe ostium ofthe rectalbranch andbeforethedivision,for a proximalembolization.

We used the protection procedure when, even with a catheterpositionaftertheostiumoftherectalanastomosis, therewasmajorrefluxintherectalbranch.Thelackofdata aboutcomplications(rectorrhagiaorerectiledisability)for thesepatientsisalimitofouranalysis.

Ourclassificationcouldallowtopredictriskysituations, andthusanticipateandtreatthemareproducibleway.

Asecond perspectiveistoimprovetheefficacy ofPAE, especially the‘‘PErFectED’’technique. The ‘‘PErFectED’’

techniqueismorecomplexbutfunctionalresultsseemedto bebetterthanthestandardone[10].

It was described by Carnevale et al. [1], and based on a second embolization at the distal part of medial branch,inadditionofproximalembolizationofmedialand lateral branches. In our study, we observed that 20% of the hemipelvics did not present these lateral and medial branches(typeC).Wecanassumetwohypothesis:thePEr- FectED technique was not realised in these cases, or an another branch was seen as the lateral branch and has been embolized instead. Our classification could improve the standardization of the technique, and thus itsrepro- ducibility,whichshouldimproveitssafety.

Ourobservationsalsoshowforthe firsttimethepossi- bilityofathirdbranchbetweenthemedialandthelateral, asdescribedinBtype.Thisbranchseemstofeedthecen- tralpartoftheprostate,andsothespecificregionofBPH.

This brings the question of selective embolization of this branch, evensoit wasnotdescribedbeforein thelitera- ture.Aprospectiveworkanalysingthefunctionalresultsof PAEaccordingtotheclassificationshouldbeabletoanswer thisquestion.

Several studies appear to be important in the future to investigate our classification, and particularly its pre- dictive skills.First, toassociateanatomicalsubtypeswith complications should allow to anticipate risky situations.

If the cases with extra-prostatic anastomosis are in fact morelikelytogivecomplications asrectorrhagia, erectile disabilityevennecrosis,itwouldbenecessarytoestablish a standardized prevention procedure, even sometimes

balance the benefits of the intervention. Secondly, to associatethesubtypeswithfunctionalresultsshouldallow topredictefficacyofPAE,andpotentialfailuresituations.

Weshouldalsobeabletoselectpatients,andimprovethe technique for complexcases. Thirdly, an association with prostaticvolumeand/orintensityofBPHsymptomsshould allow to predict evolution of BPH for each anatomical subtype. Thus, the classification could be an additional tooltoassistthepraticianinthetechniquechoiceandfor decisionofanearlymanagement.

Ourstudyhaslimitations,thefirstonebeingthelackof dataontheefficacyofPAEandcomplicationsinourpopula- tion.ToevaluatetheevolutionofBPHsymptomsafterPAE shouldanswerthequestionaboutthePAEefficacyfortype Cpatients.Toanalyzethecomplicationsshouldanswerthe questionaboutsecurityforunprotectedDandEpatients.

Our study has alsointernal validity limitations, due to retrospectiveandsinglecenteredcharacteristics;13.75%of arteriographies wereunclassified, due to reading difficul- ties.Inmostcases,thedivisionoftheprostaticarterywas not visible onthe imagessaved. Aprospective work with

‘‘perprocedure’’readingshouldprovidebetterresults.

Our observations, and especially the classification, shouldhaveexternalvalidationbyprospectiveworks.

Conclusions

Arterialprostaticanatomyishighlyvariable.Therearemul- tipleoriginsoftheprostaticartery,distributionmodesand possibilitiesofextra-prostaticanastomosis.

Theaimofintegratingthesevariationsintoaclassifica- tionistostandardizethePAEtechniqueandsoimproveits securityanditsfeasibility.

These preliminary results shouldbe validated by stud- ies with larger samples, and data about efficacy and complications.

Appendix A. Supplementary data

Supplementary data associated with this article can be found,intheonlineversion,athttps://doi.org/10.1016/j.

purol.2019.02.007.

Disclosure of interest

Theauthorshavenotsuppliedtheirdeclarationofcompet- inginterest.

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