Review
article
Demystifying
endoscopic
retrograde
cholangiopancreatography
(ERCP)
during
pregnancy
Vítor
Magno-Pereira
a,*
,
Pedro
Moutinho-Ribeiro
b,
Guilherme
Macedo
baGastrenterologyDepartment,HospitalCentraldoFunchal,Madeira,Portugal b
GastrenterologyDepartment,CentroHospitalardeSãoJoão,FacultyofMedicineofPortoUniversity,Porto,Portugal
ARTICLE INFO
Articlehistory: Received5August2017
Receivedinrevisedform30September2017 Accepted4October2017 Availableonlinexxx Keywords: ERCP No-radiation Pregnancy EUS Choledocholithiasis ABSTRACT
Background:Formanyyears,ERCPwasavoidedinpregnancygiventheconcernsregardingtheadverse
effects that, with special focus on radiation, could occur in the developing fetus. However, the
postponementorrejectionofERCPinpregnantwomen,mayleadtoahigherriskformotherandfetus,
especiallywhentheindicationisunequivocal,namelycholangitis,biliarypancreatitisandsymptomatic
choledocholithiasis.
Summaryandkeymessages:Thisreviewaimstosummarizethescarceliteratureonthesubjectinorderto
planERCPinpregnancywiththehighestsafety.Theuseoftechniquesthatreduceradiationandincrease
theprotectionofpregnantwomenallowradiationlevelsfarbelowthesafetylimits.
WealsodiscussthevariousalternativesofERCPwithoutradiation.EUScaneliminatetheneedforERCP
withdoubtfulcholedocholithiasisandplanthebestapproachinthosewithpreviousevidence.The
possibilityofperforming“ERCP”withalinearechoendoscopeuniquelyunderultrasoundcontrolhas
beendescribed.Conversely,thetwo-stepstrategy(initialsphincterotomywithstentplacementwithout
fluoroscopyandafterdelivery,ERCPwithlithiasisextraction)provedtobesafeobviatingfluoroscopy.In
conclusion,ERCPcanbeperformedinpregnancysafelyandeffectivelywithminimalradiationoreven
no-radiationatall.
©2017ElsevierB.V.Allrightsreserved.
Contents
Introduction ... 35
Endoscopicretrogradecholangiopancreatography(ERCP):patientselectionandindications ... 36
Risksofradiationexposureandstrategiesofreduction ... 36
ERCPcomplications ... 37 Non-radiationERCP ... 37 ERCPtiming ... 37 Cholecystectomy ... 38 Conclusion ... 38 References ... 38 Introduction
Womenareabouttwiceaslikelytodevelopcholedocholithiasis comparedtomen,regardlessoftheprevalenceofcholelithiasis[1]. This discrepancy is more pronounced at younger ages, with a significant reduction in the woman-to-man ratio as the age progresses[2],reflectingthemagnitudeoftheeffectofpregnancy andsexhormones.
Thelitogenicityoffemalesexhormonesisreinforcedbystudies inwhichestrogenshavebeenadministeredtomen.Inastudywith * Correspondingauthorat:DepartmentofGastroenterology,HospitalCentraldo
FunchalAvenidaLuísdeCamões,no579004-514Funchal,Portugal.
E-mailaddresses:magnovitorp@gmail.com(V.Magno-Pereira),
pmoutinhoribeiro@gmail.com(P.Moutinho-Ribeiro),
guilhermemacedo59@gmail.com(G.Macedo).
https://doi.org/10.1016/j.ejogrb.2017.10.008
0301-2115/©2017ElsevierB.V.Allrightsreserved.
ContentslistsavailableatScienceDirect
European
Journal
of
Obstetrics
&
Gynecology
and
Reproductive
Biology
patientswithprostaticadenocarcinoma,therewasanincreasein hepaticcholesterolsecretionthatresultedinanincreaseinboth bilecholesterolsaturationandrateofgallstoneformationduring estrogen treatment [3]. Also, in men with acute myocardial infarction,estrogens increasedtherisk of biliary lithiasismore thantwice[4].
Pregnancyis a majorrisk factorfor biliarylithiasis.Therisk increaseswithfrequencyandnumberofpregnanciesandreduces with breastfeeding [5]. The risk increases up to 10 times in multiparouscomparedtonulliparous[6].Duringpregnancythere isadecreaseingallbladdermotilityandabreakdownofcholesterol inbile.These changesareinduced byestrogen whichincreases cholesterolsecretionandprogesteronewhichreducesthe secre-tionofbileacidsanddelaystheemptyingofthegallbladder.There is also a relative overproduction of hydrophobic bile acids (chenodeoxycholate) which reduces bile's ability to solubilize cholesterol[1,7].
In a prospective ultrasound study with more than 3200 pregnantwomenwithoutlithiasis(baselineultrasound),lithiasis ornewbilesludgewasobservedin7.1%uptothesecondtrimester, 7.9%uptothethirdtrimesterand10.2%upto6weekspostpartum. Ofthepregnantwomenwithlithiasisorbiliarysludge,only1.2% developed symptoms of biliary pathology [8]. Up to 10% of symptomatic pregnant women develop serious complications suchasacutecholecystitis,choledocholithiasisorpancreatitis[9]. RisksofERCPinpregnancyincluderisksofsedation,radiation or electrocautery to the fetus, as well as technical difficulties relatedtothechangingmaternalanatomyandanincreasedriskto post-ERCPpancreatitis.Thereforewereviewedeachpotentialrisk basedonthebestavailableevidencetodate.
Endoscopicretrogradecholangiopancreatography(ERCP): patientselectionandindications
ERCP is currently established as an essentially therapeutic techniqueand,inpregnancy,itbecomesevenmorepressingthatit is performed for this purpose alone. In this population, it is indicated, as treatment in biliary pancreatitis, symptomatic choledocholithiasis and cholangitis or in the lesions of the pancreaticor biliary duct [10].The usual risks associated with ERCP,suchasperforation,infection,hemorrhageandpancreatitis canhaveimportantconsequencestobothmotherandfetus.The fearofinducingirreversiblelesionspostponedERCPuseformany yearsinpregnantwomen.
Nonetheless, itisalsorelevanttoreferthattheconservative approachforsomeoftheseindicationscanalsobedeleterious.As showedina retrospectivestudy, theconservative management (versusERCPand/orsurgery)ofcholelithiasisanditscomplications in pregnancy is significantly associated with higher recurrent biliary symptoms, number of emergency department visits, numberof hospitalizations and cesarean sectionoperations for childbirth[11].
Risksofradiationexposureandstrategiesofreduction Fluoroscopy radiation may have both stochastic effects and deterministiceffects.Theformers,donotpresentadosethreshold, thelikelihoodofdevelopingdeleteriouseffectsisproportionalto thedosebutitsseverityisdose-independent(e.g.leukemia).Inthe latters,thedoseandseveritythresholdareproportionaltothedose (e.g. cataracts) [12]. Hence the concept “as low as reasonably achievable” radiation has emerged [13]. In fact, the European SocietyofDigestiveEndoscopy(ESGE)recommendsinitsradiation protection guideline that KAP (kerma-area product) should be monitored,anditscumulativevalueshouldberecordedforevery ERCPandpatient[14].
The American College of Obstetricians and Gynecologists (ACOG) has stated in 2016diagnostic imaging guidelines that: “Fetalriskofanomalies,growthrestriction,orabortionhavenot beenreportedwithradiationexposureoflessthan50mGy,alevel abovetherangeofexposureforthediagnosticprocedures.”15
In fact,inastudyinvolving17ERCPsinpregnantwomenwithamean fluoroscopy time of 14s (range 1–48s), the estimated fetal radiation exposure was 0.40mGy (range 0.01–1.8mGy). There was a correlation between fluoroscopy time and radiation exposure,buttherewasawiderangeofexposureforindividual fluoroscopy times [16]. In another study, the estimated fetal radiation was 1.02–5.77mGy (0.00102–0.00577Gy) [17]. The International Commission on Radiological Protection (ICRP) recommendsmonitoringfetalradiationwhenadoseisexpected toexceed0.01Gy[18]Studiesinclinicalpracticehaveestimated fetal radiation induced by ERCP of <0.1–5.77mGy (0.0001– 0.006Gy).Althoughmeasurementsshowlowfetalabsorbeddose values(clearlybelowICRP radiationcutoff),methodologiesalso demonstrate that minute variationsin the procedure including degree of incidence of fluoroscopy, position of the patient, orientation of the fetus and endoscopist experience can have dramaticeffectsonthefinaldoseabsorbed[19].
Therisktothefetusisalsodependentonthegestationalage. Basedondatafromatomicbombsurvivors,itappearsthattherisk tothecentralnervoussystemisgreatestwhentheexposureoccurs at 8–15 weeks of gestation. It has been suggested that the minimumdoseforthisadverseeffectmightbe60–310mGybut thelowestrecordeddosetoinducesevereintellectualdisability was 610mGy.After16weeksthere isa lowrisk forintellectual disability.[15]
Inastudyinvolving23pregnantpatientssubmittedtoatotalof 29ERCPS,3womendidnotknowthattheywerepregnant[20].Itis importanttoconfirmwithallwomenofchildbearingageiftheyare pregnantatthetime oftheprocedure duetotherisksinearly pregnancy.Beforeimplantation(0–2weeksafterconception),with aminimumdoseof50–100mGytheeffectcanbe“allornone”: deathofembryoornoconsequence.Duringorganogenesis(2–8 weeks)theestimatedthreshold doseis 200mGyfor congenital anomalies(skeleton,eyes,genitals)andgrowthrestriction[15].
Fetalradiationexposuredependsonmultiplefactorssuchas size and body composition of the mother, gestational age as discussed, position of the mother and fetus and exposure techniques.Theuseofaleadapronplacedinferiorlytothepelvis and lower abdomen of the pregnant woman is recommended although most of the exposure of fetal radiation comes from radiationdiffusedbythemother,soitisessentialtocomplement thisprotectionwithotherstrategies[16].
Thereareseveralstrategiestoreducetheradiationexposureto themotherandfetusduringfluoroscopy:useaslittlefluoroscopy timeandobtainasfewspotexposuresaspossible;keeptheimage intensifierasclosetothepatientaspossible;useBoostModeand Magnification Mode only when necessary; use a modern fluoroscopy equipment; collimate x-ray beam to the area of interestandusealowframe-rate.Inmanualmode,usehigherkV (atleast75)andlowermAsettings(decreaseinpatientdoseof50% can be achieved by increasing voltage from 75kV to 96kV). Monitoring and recording the amount of fluoroscopy time is another strategy toincrease awareness of the endoscopist and reducethetotalexposuretime[13].
Amnioticfluidisapossibleconductorofcurrenttothefetus. Thus,theuterusshouldnotbebetweenthegroundingpadandthe electricalcatheter.Thepadshouldbeplacedhigherintheposterior thoracicwall(ratherthanthehip).Bipolarelectrocauteryshould bepreferred,tominimizethisrisk[10].
National Radiological Protection Board advises magnetic resonance imaging (MRI) avoidance during the first trimester
duetolimitedexperience.Itstatedthatitmaybeusedonlyafter criticalrisk-benefitanalysisandonlyifthediagnosticinformation cannotbeprovidedbyultrasound[21].Thisrecommendationis basedontheoreticalpossiblebiologicaleffects andthereareno harmfulreportsofMRIduringpregnancyknownuntilthedateof writing.
ERCPcomplications
AretrospectivecohortstudyoftheNationalInpatientSample with907pregnantand2721non-pregnantwomendemonstrated thattherewasnodifferenceinratesofperforation,infectionand bleeding of ERCPs performed in pregnant women. Post-ERCP pancreatitis(PEP)occurredin12%ofpregnantwomenvs.5% non-pregnant.Pregnancywas anindependentriskfactor(OR 2.8,CI 2.1–3.8) for PEP[22]. Thepregnancy grouphad less pancreatic stents placed than the control group, which was statistically significant. Nevertheless, even after adjusting for the stents, pregnancywasstillanindependentfactor.Theauthorssuggested severalpossiblemechanismsforthis:thetendencytousetheleast radiationpossiblecould leadtomore difficult cannulation; the physicianscouldbelesspronetogivelargevolumesofintravenous fluidduring/afterERCPortotreatwithNSAIDs(nonsteroidal anti-inflammatorydrugs)whichcanbeteratogenic.Therecouldalsobe a physiologic mechanism that inherently predisposed pregnant womentoPEP.However,theauthorsemphasizethatERCPshould notbediscouragedinpregnantwomenwithclearindication.Itis stilltheleast-invasiveapproachtotherapyforbileductpathology (vs.surgicalorradiologicmanagement).
Another unicenter retrospective study had previously sug-gestedthishypothesiswithPEPin16%ofthe68ERCPsperformed on65pregnant[23].
Non-radiationERCP
Ina retrospectivestudy, 21ERCPs withoutfluoroscopywere analyzedinpregnantwomen[24].Apreviousimagingstudywas performed(allhadabdominalultrasound,6echoendoscopy(EUS) and 4 magnetic resonance cholangiopancreatography (MRCP)). The bile cannulationwas confirmed by the observation of bile aroundtheguidewire(withforwardandbackwardmovements). Whenbilewasnotvisible,a5French(Fr)2cmstentwasplaced.In the case of drainage of bile by the stent, sphincterotomy was performedwithneedle-knifefollowed bycannulationand stent removal.Incaseofdrainageofpancreaticjuice,accesspapillotomy wasperformed.Peroralcholangioscopy(Spyglass1)wasusedto confirmtechnicalsuccessin5caseswithoutpreviousEUS/MRCP. One case of PEP was reported (catheter advancement prior to cannulationconfirmation)buttherewas nosymptomatic recur-renceinanyofthecases.
A two stage ERCP approach has been described in a study involving11pregnantwomen[25].ERCPwasperformedwithout fluoroscopyorEUS.Allthewomenpresentedwithjaundiceand pain,registering2casesofcholangitis.Inafirsttime,theinitial sphincterotomy was performed with stent placement without using fluoroscopy. After delivery, ERCP was performed with lithiasis extraction. In this second ERCP, 1 case presented no lithiasis,8caseswithstoneswith5–8mmremovedwithDormia basket, and 2 cases with stones >15mm (1 resolved with extracorporeal lithotripsy and 1 surgically). Alldeliveries were of term,with noneed for rehospitalization and nochanges in infantdevelopmentduringthefollow-upperiodupto6years.A similartwo-stageinterventionwascarriedinaretrospectivestudy involving17third-trimesterpregnancies(34ERCPS):7caseswith endoscopicnasobiliarydrainageand10withbileductplasticstent
[26]. There were two complications, namely, one biliary tract
hemorrhageandonecaseofacutemildpancreatitis.Allsymptoms weresignificantlyalleviated.Elevencaseshadtermlaborsand6 hadprematuredelivery.
The strategy of only placing a stent has the advantage of fluoroscopy being minimal but carries a risk of migration or occlusionofthestentthatcouldcausecholangitisand needfor another ERCP. Performing only sphincterotomy facilitates the passageofstonesandispreferabletostentonlybutmightnotbe sufficienttomaintaindecompressionuntilpostpartum cholecys-tectomy[25].
In a retrospective study, Vohra et al. demonstrated the successful single-session endosonography-based ERCP without fluoroscopyin10pregnantpatientswithsuspected choledocoli-thiasis [27]. IDUS (miniprobe intraductal ultrassound) was not usedgiven theneedforfluoroscopy. EUSexcluded choledocho-lithiasisin4cases,thusavoidingERCP.Lithiasiswasconfirmedin theremaining6cases,thenumberofbilestonesextractedbeing equaltothenumbervisualizedintheEUS.Bilecannulationwas confirmedbyaspirationofbile.Anumberedguidewirewasusedto monitortheprogressioninsidethebileductendoscopically.Biliary sphincterotomywithendocutmodewasperformed,followedby stoneextractionusingastandardDormiabasket.Cholangioscopy was usedintwopatientsgiventhefragmentationoflithiasisto confirm complete extraction. There were no complications, repetitionofprocedures,adverseeventsorabortions.
TheseresultssupportthestudiesofsinglesessionEUS-ERCPin non-pregnant patients, demonstrating that ERCP can be safely avoidedinasignificantnumberofpatients(44–75%,dependingon the risk stratification for suspected choledocholithiasis of the patients)[28,29].
Nonradiation ERCP with endoscopic biliary sphincterotomy plus papillaryballoondilationwas retrospectivelyevaluatedfor the treatment of choledocholithiasis in 22 pregnant patients. Balloondilationwasperformedwitha6-mmballoonin17patients andan8-mminfivepatients,accordingtothediameteroftheCBD (common bile duct) on US (ultrasonography) or MRCP, with effectivestoneextractionin18patients.Nobiliarystentwasused. Allpatientsdeliveredatterm,andnoneexperiencedrecurrenceof symptomsduringthe6-monthfollow-up.Therewere2casesof PEP[30].
FailedcannulationwhileperformingERCPduringpregnancyis atechnicallydemandingsituation.Therehasbeenacasereportofa successfully attempted EUS guided rendezvous technique,with fluoroscopyusedonlytoconfirmtheexitofthewirefromampulla, wirerepositioninintrahepaticbiliarysystemandthepositionof thestent.Thewholefluoroscopyexposuretimewas3s[31]. ERCPtiming
Thereisthegenericrecommendationtoavoidendoscopyinthe firsttrimesterwheneverpossible[10].InERCP,therehasalsobeen worriesduringthefirsttrimester.Inaretrospectivereviewof68 ERCPs performed in 65 pregnant patients, there were no perforation, sedationadverseevents, postsphincterotomy bleed-ing, cholangitis,or procedure-related maternal or fetal deaths. However,womensubmittedtoERCPinthefirsttrimesterhadthe lowestpercentageoftermpregnancies(73%),thehighestriskof pretermdelivery(20%)andlowbirthweightnewborns(21%)[23]. However,theauthorssuggestedthatitwas thedevelopmentof hepatobiliarydiseaseinthefirsttrimesterofpregnancythatcould beassociatedwithpretermdeliveryorlowbirthweightandnot the procedure itself. They suggested therefore “to intervene appropriatelyasearlyaspossible”.
In fact, asshowed in a retrospective study of 112 pregnant women, the conservative management (versus ERCP and/or surgery) of cholelithiasis and its complications (mainly biliary
colic, biliary pancreatitis, acute cholecystitis and choledocholi-thiasis) in pregnancy is significantly associated with higher cesareansection operationsfor childbirth and higherrecurrent biliarysymptoms,number ofemergency departmentvisits and numberofhospitalizations[11].ERCPwasperformedatameanof 3.7daysaftertheonset ofthesymptomsbyexperienced endo-scopists. CBDcannulation rate was 100%and biliary sphincter-otomywasdonein88%.Onlyonecomplicationwasreported,one case of PEP that resolved in a few days with conservative management.Butitisimportanttoreferthatthisstudyincluded only4ERCPinthefirsttrimester.Anotherstudy,demonstratedthat upto72%ofpregnantwomenwithbiliarypancreatitiswillhavean intercurrenceduringpregnancyifaconservativeapproachistaken
[32].
In a retrospective matched-cohort study with 907 ERCP performed in pregnant women, there is no reference to the trimesters or week of gestation. Nevertheless, there were no differencesinmaternalmortality,fetaldistressorfetallosswhen comparedtoage-matchedpregnantwomen.Curiously,theriskof pretermlaborinpregnantpatientsundergoingERCPwaslower thanthenationalaverage[22].
Finally,theevidenceisscarcerelatingspecificallytothebest timingforeachindication.Takingintoaccounttheaforementioned studies,ERCPshouldnotbedeferredincasesofcholangitis,biliary pancreatitis and symptomatic choledocholithiasis. Each case shouldbediscussedwiththeobstetriciantoproceedwithERCP eveninthefirsttrimester.Lesionsofthepancreaticorbiliaryduct should be evaluated case-by-case in terms of urgency of the procedure.Whentheeventoccursinthethirdtrimester,thetiming ofdelivery shouldbediscussed withtheobstetrician todecide betweenanearlydeliveryandERCPpost-partumorERCPinthe thirdtrimester,consideringthatERCPisasafeprocedureinthird trimester.
Cholecystectomy
Surgery during pregnancy increases the risk of fetal loss. Therefore,theindicationisusuallylimitedtourgentsituationsas acutecholecystitis.Thesecondtrimesterisconsideredtobethe optimaltimefor cholecystectomy,withthelowestriskfor fetal morbity[33].However,therearealsoseveralstudies demonstrat-ing the safety in urgent cases during the first trimester [34]. Surgeryin thethird trimester was generallylimited forfear of inductionof pretermlabor (upto40% in initialstudies). Most recentstudieslimitedtolaparoscopicapproachhaveshownthat surgeryissafeinanytrimesterwithoutsignificantincreasedrisk
[35].
Womenwhohavecomplicatedgallstoneareunlikelysubmitted tocholecystectomy during pregnancy. Nevertheless, the risk of symptomrecurrenceeitherduringpregnancyorintheearly post-partumishigherwhencholecystectomyisnotperformed.ERCP withbiliarysphincterotomy significantlyreducesthis risk [36]. Cholecystectomyshouldbeconsideredin complicatedgallstone disease during pregnancy, especially in patients that do not undergoor fail ERCPwithbiliary sphincterotomy.The valueof intrapartumcholecystectomyafterERCPhasnotbeenspecifically studied,butthesmallstudiesofERCPduringpregnancypreviously statedsuggestthatendoscopicsphincterotomymaybesufficient to prevent recurrence during pregnancy [24,25,30]. Likewise, laparoscopiccholecystectomycouldbesafelydoneimmediately postpartuminthesepatients.
Conclusion
ERCPcanbeperformedinpregnancysafelyandeffectivelyin womenwhohaveaclearindication.Therearemultiplestrategies
for reducing maternal and fetal risks associated with this technique.
EUScaneliminatetheneedforERCPanditsrisksinpregnant womenwithnoconcreteevidenceofcholedocholithiasis,andeven planthebestapproachinthosethatpresentpreviousevidenceby specifyingthenumber,sizeandlocationofthelithiasis.EUS-CPRE thuspresentsitselfastheidealapproachinpregnancy.Theuseofa linear EUS scope for the entire procedure has already been described. Also, thetwo-step strategy provedto bea safeand effectivealternativewithouttheneedforfluoroscopy.However, stentplacementincreasestheriskofrecurrenceofERCP,sothe risks of repetitionof theprocedure should beweighed against controlled radiation exposure from a single ERCP. Whichever method is used, it should be combined with other radiation reductionstrategiesinERCP,namely:aleadapronplacedinferiorly to the pelvis and lower abdomen of the pregnant; as little fluoroscopytime and asfew spotexposuresaspossible; image intensifierasclosetothepatient;dismissboostandmagnification modes;collimatex-raybeamanduselowframe-rate;usehigher kVandlowermAsettings.Monitoringandrecordingtheamountof fluoroscopytimeisencouragedandtheprocedureshouldbedone byanexperiencedendoscopist.
Therearenoprospectivestudiestoquantifythesuperiorityof EUS-ERCP in the different outcomes and demonstrate cost-effectivenessversusotherapproaches.However,giventhesmall series and the rarity of the procedure compared to other populations,thisisalevelofevidencedifficulttoachieve. References
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