Fertility outcomes after preconceptional laparoscopic abdominal cerclage for second-trimester pregnancy losses

Full

length

article

Fertility

outcomes

after

preconceptional

laparoscopic

abdominal

cerclage

for

second-trimester

pregnancy

losses

Cem

Demirel

,

Hale

Goksever

Celik

*

,

Firat

Tulek

,

Bengisu

Kucukdemir

,

Deniz

Gokalp

,

Tolga

Ergin

,

Arda

Lembet

a

AtasehirMemorialHospital,IVFandMinimalInvasiveSurgeryDepartment,Istanbul,Turkey

b

HealthSciencesUniversityIstanbulKanuniSultanSuleymanTrainingandResearchHospital,DepartmentofObstetricsandGynecology,Istanbul,Turkey

c

IstinyeUniversity,MedicalFaculty,Istanbul,Turkey

d_{LivUlusHospital,IVFDepartment,Istanbul,Turkey} e

AtasehirMemorialHospital,DivisionofMaternal-FetalMedicine,Istanbul,Turkey

f

LivUlusHospital,DivisionofMaternal-FetalMedicine,Istanbul,Turkey

ARTICLE INFO

Articlehistory: Received28June2020

Receivedinrevisedform28September2020 Accepted8December2020

Availableonlinexxx

Keywords:

Second-trimesterpregnancyloss Cervicalincompetence Laparoscopicabdominalcerclage Conceptionrate

Timetoconception

ABSTRACT

Objective(s): Cervical incompetence is an important cause of recurrent pregnancy loss, typically presentinginthesecondtrimesterwithsilentcervicaldilationandprematuredeliveryofthefetus.We aimedtoevaluatetheconceptionrateandtimetoconceptionorfailuretoconceiveafterpreconceptional laparoscopicabdominalcerclage(LAC).

StudyDesign:Weconductedthisretrospectiveobservationalcohortstudyatatertiaryreferralcenter. PatientswhounderwentLACinthenonpregnantstateforasecond-trimesterpregnancylossbetween June2012andFebruary2020wereincluded.

Results:Thesubjectswere40patientswithahistoryofoneormoresecond-trimesterpregnancylosses despitetheplacementof vaginalcerclage,whohad undergoneLACbeforecontemplating afuture pregnancy.Themeannumberofsecond-trimesterpregnancylossesbeforeLACwastwoperwoman.The agesofthewomenatthetimeofcerclagerangedfrom21to42years.Thetimetopregnancy,whichwas theprimaryoutcomeofthestudy,wasdeterminedasthenumberofmenstrualcyclesbeforethepatient becamepregnantafterLAC andthenumberofcyclesneededforthepatienttoachieveherlatest pregnancybeforeLAC.Ofthe40women,22.5%werenotedduringtheLACoperationtohaveapelvic peritoneal pathology that might have affected fertility, and all such pathologies were treated concomitantlyduringtheprocedure.SpontaneouspregnancyratesbeforeandafterLACwere96.4% and89.3%(p=0.299),andtimestopregnancybeforeandafterLACwere6.38.4and6.68.1cycles (p=0.897).Neitherdifferencewasstatisticallysignificant.Inmorethan84%ofpatientswhobecame pregnantafterLAC,pregnancywassustainedtothestageofviability.

Conclusion(s):Inpatientswithcervicalincompetence,LACisaveryeffectiveinterventiontosustain pregnancytothestage ofviability. If placedduringthe preconceptionalperiod, itdoesnot delay achievingpregnancyanddoesnothaveanegativeimpactonthechancesofconception.Thismaybe reassuringtowomenundergoingthisprocedurebeforetheyachieveapregnancy.

©2020ElsevierB.V.Allrightsreserved.

Introduction

Cervicalincompetenceoccursin0.5–1%ofallpregnanciesand

is an important cause of recurrent pregnancy loss, typically

presentinginthesecondtrimesterwithsilentcervicaldilationand

prematuredeliveryofthefetus[1].

Placementofavaginalcerclageduringpregnancyistheusual

practice for the treatment of cervical incompetence [2,3]. For

patients with a history of failed vaginal cerclage or when

placementofavaginalcerclageisnotpossiblepervaginabecause

ofanextremelyshortorabsentcervixduetoprevioussurgeries,an

*Correspondingauthorat:HealthSciencesUniversityIstanbulKanuniSultan SuleymanTrainingandResearchHospital,TurgutOzalBoulevard,No:1, Kucuk-cekmece,Istanbul,Turkey.

E-mailaddresses:[email protected]

([email protected](H.GokseverCelik),fi[email protected](F.Tulek),

[email protected](B.Kucukdemir),[email protected](D.Gokalp),

[email protected](T.Ergin),[email protected](A.Lembet).

https://doi.org/10.1016/j.ejogrb.2020.12.012

0301-2115/©2020ElsevierB.V.Allrightsreserved.

xxx–xxx

Pleasecitethisarticleas:C.Demirel,H.GokseverCelik,F.Tuleketal.,Fertilityoutcomesafterpreconceptionallaparoscopicabdominalcerclage

forsecond-trimesterpregnancylosses,EurJObstetGynecol,https://doi.org/10.1016/j.ejogrb.2020.12.012

ContentslistsavailableatScienceDirect

European

Journal

of

Obstetrics

&

Gynecology

and

Reproductive

Biology

abdominally placed cerclage is the next step. The use of

laparoscopyforabdominalcerclageplacementwasfirstdescribed

in1998andisnowawidelypracticedmethodinsuchcases[4].

Withabdominalcerclage,thesutureisplacedatahigherlevel

relativetotheinternalosandisthereforemorephysiologicaland

effective,withreportedsuccessfulpregnancyoutcomeratesof69–

95%inseveralreviews,althoughtheproceduremaybeassociated

with a 3.4 %likelihood of serious operativecomplications and

significant morbidity [5–10]. Today, laparoscopic placement of

cervico-isthmic cerclage(CI)is performed,eitheras aninterval

procedure before conception or during pregnancy, with the

expectedbene_fitofbeingaminimallyinvasiveinterventionover

the traditional laparotomy approach. The success rate of the

laparoscopicapproachis79–100%,similartothatoflaparotomy

[11–13].

Variousgroupshavereported42.9–90.9%pregnancyratesafter

preconceptional(interval)LAC[14–17]andexcellentfetalsurvival

ratesashighas90%duringongoingpregnancy[18].

In a systematic review of 1251 patients who underwent CI

cerclagebylaparotomyorlaparoscopyeitherduringpregnancyor

asanintervalplacement,thehighestfetalsurvivalrate(94%)was

reportedfortheintervaltransabdominalapproach,andthelowest

(80.9%) forlaparoscopiccerclageplacedduringpregnancy[14],

questioningthefeasibilityoflaparoscopicapproachatthetimeof

pregnancy. Amongall patientsin whom a cerclagewas placed

beforepregnancyusingthelaparoscopicorabdominalapproach,

>74%becamepregnant.

PlacingCIcerclagebylaparoscopyonagraviduteruspresents

some surgical challenges because the growing uterus impedes

surgical manipulation, the increased vascularity of pregnancy

predisposesthepatienttoseverebleeding,andperioperativeloss

ofthepregnancyisa majorconcern.However,whencerclageis

placedbeforepregnancy,asubstantialnumberofwomenwillnot

becomepregnantthereafter,ortheirsubsequentpregnancymay

endwithanearlyabortion.

FetalsurvivalratesafterLACareexcellent,providedthatthe

patientcanbecomepregnant.Inpreoperativecounseling,patients

should be informed of the potential effects of preconceptional

cerclageonfertility,andalsoaboutparameterssuchasthetimeto

pregnancyaftertheprocedure,sothattheycandecidewhetherto

use contraception topostpone theirnext pregnancy. Giventhe

paucity ofdataintheliteratureonthis issue,weevaluatedthe

postoperativefertilityoutcomesof patientsundergoing

precon-ceptionalLACinourinstitution,payingparticularattentiontothe

timeneededforasubsequentpregnancyaftertheprocedure.

Materialsandmethods

Thiswasaretrospectivecohortstudyperformedinatertiary

referralcenter.Themedicalrecordsofpatientswhohadundergone

LAC in the nonpregnant state for second-trimester pregnancy

lossesbetweenJune2012andFebruary2020wereretrospectively

reviewedafterobtainingapprovalfromourinstitutional review

board(2020/004).

AllpatientshadbeenselectedforpreconceptionalLACbasedon

theirhistoryofhavingoneormoresecond-trimesterpregnancy

lossesdespitetheplacementofvaginalcerclage,i.e.,amid-term

pregnancylosswithvaginalcerclageinsitu.Therefore,allincluded

patientshadatleastonevaginalcerclagefailureintheirobstetric

histories. None of the patientshad beenreferred for LAC as a

primaryprocedureforsuspectedcervicalincompetancewithout

vaginalcerclagehavingbeenpreviouslyattempted.

Theobstetrichistoryofeachcasewasrecorded,withattention

paidtowhetherpreviouspregnancieshadbeenachievednaturally

orbytreatment,whethertherewasahistoryofinfertility,when

thevaginal cerclagehad beenplaced,and howthepregnancies

ended.Itwasalsonotedwhethertherewasahistoryofretained

placentaltissuenecessitatingcurettagefollowingthelossofeach

pregnancy.

Laparoscopy videos of each case were reviewed for any

coexisting pelvic pathology that could hinder conception. The

statusofthefallopiantubes,fimbriae,andpelvicperitoneumwere

noted,togetherwiththepresenceofanyperiadnexaladhesions.

The interventions performed to treat these coexisting pelvic

peritonealpathologiesduringtheLACoperationwerealsonoted.

Surgicalprocedure

All operations were performed by the same surgeon (CD).

BeforetheLACprocedure,atranscervicaluterinemanipulatorwas

placedinposition.A10-mmtrocarwasintroducedthroughthe

umbilicus,withthreeadditional5-mmtrocarsinthelowerlateral

quadrants and suprapubic area. Abdominal insufflation was

maintainedat12mmHgusingCO2.Thevesicouterineperitoneum

wasincisedusinganUltracisionharmonicscalpel(SomaTechIntl.,

CT,USA)acrosstheloweruterinesegment,startinglaterallyand

eventually reaching the midline, as most cases had severe

adhesionsbetweenthebladderandloweruterinesegmentdue

topreviouscesareansections.Oncethebladderhadbeendissected

away from the anterior cervix, the peritoneal opening was

extended laterally toexpose the course of the uterinearteries

closetotheuterineisthmusonbothsides.

A5-mm Mersilene tape(Ethicon)withstraight needleswas

introducedintotheabdomenthroughthe10-mmumbilicalport.

Theneedlesatbothendsofthetapewerepassedmedialtothe

uterinevesselsbilaterally,attheleveloftheinternalcervicalos

Fig.1.Aflowchartofthestudydesign.

fromposteriortoanterior;theinsertionsiteswere2cmsuperior

and1cmlateraltotheattachmentoftheuterosacralligamentsto

theuterus.Attentionwaspaidtoensurethatthetipsoftheneedles

exited medial to the uterine arteries exposed anteriorly. The

Mersilene tape was then secured with five or six knots tied

intracorporeally,anteriortothecervix.Theneedleswerecutand

removed. The vesicouterine peritoneum was closed over the

cerclagesuturewithacontinuous2 0Vicryl(Ethicon)suture.

FollowingacaseofinadvertentpassageoftheMersilenetape

throughthecervicalcanal,theuseofofficehysteroscopyduring

insertionoftheMersilenetapeneedleswasincorporatedintoour

LACprocedure.

Outcomemeasures

The primary outcome of the study was time to pregnancy

beforeandaftertheoperation.Menstrualcycleswereregularinall

women,rangingfrom26to35daysinduration.

The numberof menstrualcycles neededtoachieve a

subse-quentpregnancyaftercontraceptionhadbeendiscontinuedwas

calculated for each pregnancy. AfterLAC, thenumber of cycles

needed to become pregnant once contraception, if any, was

discontinued was also noted. Time topregnancy following the

operationwascomparedtothenumberofcyclesneededforthe

patienttoachievehermostrecentpregnancybeforeLAC.Because

ageisasignificantdeterminantofawoman’sfertility,thetimelag

between the last pregnancy before LAC and the date when

contraceptionhadbeendiscontinuedtobecomingpregnantafter

LACwasalsonoted.Finally,overallspontaneouspregnancyrates

beforeandaftertheinterventionwerealsocompared.

Statisticalanalyses

StatisticalanalyseswereperformedwiththeStatisticalPackage

fortheSocialSciences(SPSSInc;Chicago,IL,USA)statistics22.0

version for Windows. A flowchart shows the inclusion and

exclusioncriteriaof thestudypopulation.Meansarepresented

withstandard deviation(SD)andmedian valuesare shownfor

continuousvariables.Numbersofcasesandpercentages(%)were

used for nominal variables. Differences in mean values and

characteristicsbetweengroupswereanalyzedusingthe

indepen-dent-samplest-testandchi-squaretest.TheeffectofLAConthe

conceptionratewasinvestigatedusingthelogranktest.Life-table

analysiswasusedtoassesstheindependenteffectsofLAConthe

conceptionrateandtimetoconception.Apiegraphwascreated

usingthelegacydialogtovisualizepregnancyoutcomes.Forall

analyses, values of p < 0.005 were considered statistically

significant.

Results

BetweenJune2012andFebruary2020,40patientsunderwent

preconceptional LAC for a second-trimester pregnancy loss. Of

those,28patientsmettheeligibilitycriteriaforthestudy(Fig.1).

Themean number ofsecond-trimester pregnancy lossesbefore

LACwastwoperpatient.

Thewomen’sagesatthetimeofcerclagerangedfrom21to42

years. In seven patients, all pregnancies before and after the

operationwerebyIVF due tomale or tubal factor infertilities;

therefore these patients were excluded from the analysis.

Additionally, bilateral salpingectomy was performed in two

patients during the LAC procedure because of bilateral

hydro-salpinges.Twopatientswhowerestilloncontraceptionafterthe

operationatthetimeofwritingwerethereforeexcludedfromthe

study. One patient was lost to follow up after LAC,leaving 28

patientsforthefinalanalysis.Spontaneouspregnancyratesbefore

andafterLACwere96.4%and 89.3%(p=0.299),respectively;

timestopregnancybeforeandafterLACwere6.38.4and6.6

8.1 cycles (p = 0.897), respectively. The patients before and

after LAC were similar regarding their clinical characteristics,

numerically.

AKaplan–Meiersurvivalanalysisgraphshowednodifference

in time to pregnancy expressed as cycle number (p = 0.192)

(Fig.2).

Fig.2. TimetopregnancybeforeandafterLACoperation,expressedincycles.

Table1

Intraoperativefindingsthathavepotentialtointerferewithfertility,encounteredduringpreconceptionalLACoperationforthesecondtrimesterpregnancylosses. Patient

initials

Intraoperativefinding Co-treatmentduringLAC Postoperativepregnancy outcome

Time topregnancy (spontaneous conception) Patient1 Leftperi-ampullaryadhesions Leftsalpingo-ovariolysis Pregnant 4cycles Patient2 Rigtovaryfixedtobroadligament Rightovariolysis Pregnant

withIVF

– Patient3 Bilateralperitubaladhesions Bilateralsalpingo-ovariolysis FailedIVF – Patient4 Bilateralhydrosalpinges Bilateralsalpingectomy Pregnant

WithIVF

– Patient5 Totallyadherentuterinecorpustoanterior

abdominalwall

Adhesiolysis Pregnant 18cycles

Patient6 Bilateralperi-fimbrialadhesions Bilateralfimbriolysis Pregnant 1cycle Patient7 Bilateralhydrosalpinges Bilateralsalpingectomy NottriedIVFyet – Patient8 Lefttubo-ovarianadhesions Leftsalpingo-ovariolysis Pregnant 5cycles Patient9 Bilateraladnexialadhesions,leftfimbrial

phimosis

Bilateralsalpin-ovariolysisandleft neosalpingostomy

Pregnant 2cycles

Table 1showsintraoperative findingsduringLACthatmight

have presented obstacles to spontaneous conception and thus

affected postoperative fertility outcomes. Of 40 patients who

underwentLAC,9(22.5%)werefoundtohavepelvicperitoneal

pathology that might have affected their chances of natural

conception.

Among sevenpatientswho had achievedpregnancies solely

withIVFbeforeLAC,sixtriedanIVFcycleaftertheoperation,and

of these, four had a positive outcome. One patient who was

previouslyabletobecomepregnantonlybyIVFbecamepregnant

naturallyafterperifimbrialadhesionsweretreatedconcomitantly

duringLAC(Table1).

Of25 patientswhobecamepregnant,11delivered ahealthy

infant after 366/7 _{weeks’ gestation. An additional 5 patients}

delivered between326/7 _{and 36}1/7 _{weeks’ gestation.Another 5}

haveanongoingpregnancythathaspassed29weeksatthetimeof

writing.Therefore,inourcaseseries,atleast84%ofthepatients

whohadpreconceptionalLAChaddeliveredorwouldpotentially

deliverhealthyinfantsfollowingtheoperation.Inaddition,two

pregnancies were ongoing at <12 gestational weeks’ duration

when this manuscript was being written. Two patients had a

missedabortionat7gestationalweeks(Fig.3).

Comment

LACisaveryeffectiveprocedureinpatientswithahistoryof

failed vaginal cerclage for cervical incompetence or when an

extremelyshortenedcervixmakesthevaginalapproach

impossi-ble.Inourcaseseries,wedocumentedasuccessrateofatleast84%

inhavingaviableinfant.

AveryrecentrandomizedcontrolledstudybyShennanetal.

[19] documented the superiority of placing cervical cerclage

abdominally rather than vaginally in patients with a previous

historyofsecond-trimesterpregnancylosswithvaginalcerclagein

situ. Abdominal cerclage was associated with a statistically

significantreductioninpretermbirthat<32weeks’gestational

agecomparedwithvaginalcerclage(8%vs.33%:relativerisk0.23,

95 % confidence interval 0.07–0.76, p = 0.0157). Although

laparotomy was the method of choice in that study, in the

current eraofminimallyinvasive surgerylaparoscopyperforms

equallywell.

Because of the risk of major intraoperative bleeding or

miscarriage and the difficulty of handling the large size of a

pregnant uterus, it is generally preferred to perform LAC

preconceptionally. Cerclage sutureplacement by laparoscopyis

quitechallengingduringpregnancy,asnouterinemanipulatorcan

beused;additionally,thelargesizeoftheuterusimpedesproper

visualization.However,thedrawbackofpreconceptional timing

for the procedure is that somewomen will not conceive after

surgery,andarethussubjectedtoanunnecessaryprocedure.

InastudybyWhittleetal.,sevencasesofLACwereconvertedto

laparotomyduetoeithermajorbleedingfromuterinevesselsor

impairedsurgicalvisibility,andsixofthosepatientswerepregnant

[13]. Therefore LAC during pregnancy risks conversion to

laparotomy.Inthesamestudy, althoughthetimingofcerclage,

i.e., whetherbefore or duringthe pregnancy, didnotinfluence

gestationalageatdelivery,thereappearedtobefewer

periopera-tivecomplicationsandsecond-andthird-trimesterlosseswhena

cerclagewasplacedbeforepregnancy.

Although the ability of preconceptional LAC to achieve

prolongation of pregnancy to fetal viability in patients with a

history offailed vaginalcerclage hasbeenconsistently

demon-stratedbyobservational studies,its effectoninfertilityhasnot

beenadequatelyassessed.Actually,theonlypaperreportingabout

theeffectof placingcerclageabdominallyonthepostoperative

conceptionratesandthetimetakentoconceive,inaRCTsetting

wasbyVousdenetal.[20].Thisstudywasasubgroupanalysisof

MAVRICtrial[19],comparingthefertilityoutcomesof19women

who underwent preconceptional abdominal cerclage with 48

womenwhohadvaginalcerclageduringpregnancy.Overall,there

wasnosigni_ficantdifferenceinthetimetakentoconceiveandin

ratesofconception betweenthetwo groupsrandomized.What

differsfromourstudyistheplacementofabdominalcerclageby

laparotomy.Additionallyourpatientsservedastheirowncontrols

which may confer a more direct comparison of the fertility

outcomesbeforeandafter.

Theresultsofalargesystematicreviewof1251patientswho

underwentabdominalcerclageeitherbylaparoscopy(n=135)or

laparotomy(n=1116)beforepregnancyshowedthat>74%ofthe

patientsbecamepregnantaftertheoperation[14]. Inourstudy

population,only10.7%ofthepatientsfailedtobecomepregnant.

Amongthethreepatientswhofailedtobecomepregnant,onewas

Fig.3.PregnancyoutcomesafterpreconceptionalLAC.

41yearsoldatthetimeofcerclage,andanotherstoppedtryingfor

a spontaneouspregnancyafter1yearwhenshewas diagnosed

with breast cancer. Therefore, preconceptional placement of

abdominalcerclagebylaparoscopydidnothaveanymajorimpact

onsubsequentfertility.

Inourstudy,22.5%ofpatientsundergoingLAChadatleastone

pelvicperitonealpathologythatmighthavehadanadverseeffect

onthechanceofspontaneousconceptionandthatwas

simulta-neously resolved. One such patient in our study, who was

previouslyabletobecomepregnantonlybyIVFbutthendelivered

herinfantprematurely,becamepregnantspontaneouslyafterLAC

becauseofconcomitantlyperformedbilateral_{fimbriolysis.}Inthis

sense, preconceptional LAC can even be viewed as a

fertility-enhancingprocedure.

To date, there has been no randomized controlled study

comparing the outcomes of patients who undergo abdominal

surgery prior to conception with those of patients whose

placementisinearlypregnancy.Similarly,nostudyhasexamined

whetherittakeslongertoachieveaspontaneouspregnancyafter

thelaparoscopicabdominalcerclageoperation.Thisinformationis

of particular importance when counseling patients abouttheir

reproductivechancesaftertheprocedure.Iftheoperationmight

causesignificantdelaysinnaturalconception,itwouldbeprudent

to advise patients not to use any contraception for extended

periodsoftime.Ourfindingsinthissmallgroupofpatientsprovide

reassurance that preconceptional LAC does not interfere with

future fertility, and once contraception is discontinued, the

chancesofconceptionaresimilartothosepreoperatively.

In conclusion, our study is the first to show that time to

pregnancyisnotalteredafterLACandthelikelihoodofpregnancy

isthesameasbeforetheoperation.LACdoesnotresultininfertility

and can therefore be safely proposed preconceptionally, thus

avoidingamoredifficultprocedureduringpregnancy.DuringLAC,

additional pelvic peritoneal factors for infertility can also be

corrected. A word of caution maybe necessary for women of

advancedmaternalagewhoarebeingconsideredascandidatesfor

LAC.Thesewomenmaybeadvisedtoundergotheprocedureafter

theybecomepregnantduetotheage-relateddeclineinconception

ratesandincreasedriskofabortioninearlypregnancy.

TheEnglishinthisdocumenthasbeencheckedbyatleasttwo

professional editors, both native speakers of English. For a

certificate, please see: http://www.textcheck.com/certificate/

HnujRe

Funding

Thereisnospecificfundingforthisstudy.

DeclarationofCompetingInterest

Theauthorsdeclarethattheydonothaveanycon_flictofinterest

inregardtothisarticle.

Acknowledgements

Theauthorswouldliketothanktheparticipantsofthisstudy.

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