ultrasound-guided umbilical cord occlusion using bipolar diathermy for stage iii/iv twin–twin...

Ultrasound-guided umbilical cord occlusion using bipolardiathermy for Stage III/IV twin–twin transfusion syndrome

M. J. O. Taylor1*, E. Shalev2, S. Tanawattanacharoen1, M. Jolly1, S. Kumar1, E. Weiner2, P. M. Cox3 andN. M Fisk1

1Centre for Fetal Care, Department of Maternal & Fetal Medicine, Imperial College School of Medicine, Queen Charlotte’s &Chelsea Hospital, Du Cane Road, London W12 0HS, UK2Department of Obstetrics & Gynecology, Haemek Hospital, Afula, Medical Faculty, Technion Israel Institute of Technology,Haifa, Israel3Department of Perinatal Pathology, Imperial College School of Medicine, Queen Charlotte’s & Chelsea Hospital, Du CaneRoad, London W12 0HS, UK

Objectives To evaluate bipolar diathermy as a technique for selective fetocide in the treatment of advanced(Stage III/IV) twin–twin transfusion syndrome (TTTS).

Methods A prospective observational study in two tertiary referral fetal medicine centres: QueenCharlotte’s Hospital, London, UK and Haemek Hospital, Afula , Israel. Fifteen cases of TTTS (14 twinsand one triplet pregnancy) were treated by selective occlusion of either the donor (n=8) or recipient’s (n=7)umbilical cord using ultrasound-guided bipolar diathermy. Following each procedure, patients werescanned serially for fetal growth, liquor volume and umbilical Doppler measurements. Proceduralcomplications and obstetric outcome were recorded. Postnatal placental injection studies were performed.

Results Overall co-twin survival in Stage III/IV TTTS was 13/14 (93%). There were no treatment failures.The incidence of preterm prelabour rupture of membranes (PPROM) within 3 weeks of the procedure was3/15 (20%). In those cases where pre-procedure umbilical artery Dopplers were abnormal, the Dopplerfindings normalised post-procedure in all non-cord-occluded fetuses. Growth velocities of surviving donorswere similar to those of surviving recipients.

Conclusions Bipolar diathermy appears an effective technique for the selective reduction of monochorionictwins complicated by severe as well as preterminal TTTS, with recipient and donor fetuses being equallyappropriate choices for fetocide. We suggest that for advanced-stage disease where the parents cancontemplate this option, cord occlusion as a single pre-emptive procedure maximises the opportunity forintact survival of a single survivor. Copyright # 2002 John Wiley & Sons, Ltd.

KEY WORDS: cord occlusion; twin–twin transfusion; bipolar diathermy

INTRODUCTION

In the absence of randomised controlled trials, reviewof the available observational series indicates thatlaser ablation and serial amnioreduction havebroadly comparable survival rates in the region of 60%(Fisk and Taylor, 2000) in the treatment of twin–twin transfusion syndrome (TTTS). Compared to 20%survival with conservative therapy, modern therapieshave substantially improved outcome, but neverthelessremain suboptimal.

Until recently, TTTS has been regarded as ahomogenous disease receiving uniform treatment– either amnioreduction or laser ablation – for allcases. In reality, TTTS is a heterogeneous disorderwhose severity can be determined by assessment

of prognostic factors identifiable at presentation(Quintero et al., 1999; Taylor et al., 2000a). Certainfactors independently predict outcome. Thus theprobability of at least one twin surviving falls tobelow 40% if there is absent end diastolic flow (AEDF)in the donor umbilical artery (UA) or abnormalvenous recordings in the recipient. Conversely, detec-tion of an arterio-arterial anastomosis (AAA) atdiagnosis substantially improves the chance of bothtwins surviving (Taylor et al., 2000a). Quintero et al.have developed a formal staging system (Quinteroet al., 1999) in which both laser and amnioreductiongive the worst results in Stage III/IV disease (j50%overall survival). Such poor results expose the limita-tions of both techniques. Amnioreduction fails toaddress the underlying pathophysiology, while non-selective laser dissects the placental vasculature,resulting in high procedure loss rates from devitalisedcotyledons, especially if there is a major discordancy inplacental share as is often the case in advanced disease(Ville et al., 1998). In a recent meta-analysis of 158

*Correspondence to: M. J. O. Taylor, Centre for Fetal Care,Department of Maternal & Fetal Medicine, Imperial College Schoolof Medicine, Queen Charlotte’s & Chelsea Hospital, Du Cane Road,London W12 0HS, UK. E-mail: [email protected]

PRENATAL DIAGNOSIS

Prenat Diagn 2002; 22: 70–76.DOI: 10.1002 /pd.256

Copyright # 2002 John Wiley & Sons, Ltd. Received: 29 May 2001Revised: 6 August 2001

Accepted: 14 August 2001

cases of TTTS treated by amnioreduction before28 weeks and 257 cases treated by laser at <28weeks, we noticed that laser treatment appeared toincrease single survival at the expense of reduction indouble deaths (and also double survivors), suggestingat least in part that it may be acting as a form ofselective fetocide (Fisk and Taylor, 2000).

The standard technique of selective fetocide indichorionic twins of intra-cardiac KCl injectioncannot be used in monochorionic twins due to highrisk of the co-twin exanguinating into the terminatedtwin (Evans et al., 1994) leading to death orneurological sequelae in approximately 50% of cases(Nicolini and Poblete, 1999). Instead, isolation of theterminated twin’s vasculature is necessary by anocclusive method. A variety of ultrasound-guidedand fetoscopic techniques have been used with mixedresults (Denbow et al., 1999). Injection of sclerosants,i.e. absolute alcohol or enbucrilate gel, is nowconsidered contraindicated because of failure rates>50%. The same applies to other techniques such asthrombogenic coils that occlude only one cord vessel.Laser occlusion of the umbilical cord is not feasibleafter 18–20 weeks, consistent with rodent studiesshowing that the successful occlusion rates decreasewith increasing vessel diameter (Evrard et al., 1996).Fetoscopic cord ligation, although effective (Quinteroet al., 1994), is a lengthy procedure, requires more thanone port (Quintero et al., 1996), and is associated witha high incidence of amniorrhexis. The use of ultra-sound-guided bipolar diathermy forceps has recentlybeen described for selective cord occlusion in mono-chorionic twins discordant for fetal anomaly orcompromise (Deprest et al., 2000).

Experience with selective fetocide in TTTS has beenlimited largely to case reports in end-stage disease withsigns of imminent fetal demise. The role of fetocide insevere as well as preterminal TTTS has not beendetermined. In particular, the question of whether toselect donor or recipient fetus for fetocide remainscontroversial.

We report preliminary experience in two fetalmedicine centres of the use of bipolar diathermycord occlusion in the treatment of Stage III and IVdisease.

PATIENTS AND METHODS

Fifty-nine consecutive monochorionic twin and onedichorionic triplet pregnancy complicated by TTTSwere seen at a tertiary referral fetal medicine centre inthe UK (April 1999–June 2000) or in Israel (November1997–April 2000).

We confirmed monochorionicity using standardultrasound criteria (Fisk and Bennett, 1995) andperformed fortnightly ultrasonic surveillance using anAcuson Sequoia or XP10 (Acuson Co., MountainView, CA, USA) or HDI 3000 (ATL, Bothell, WA,USA) for fetal growth, liquor volume and Dopplerstudies. Fetal weight was estimated using Hadlock’sformula and discordance calculated as a percentage of

the weight of the larger twin (Rydhstrom, 1994).Gestational age was based on the date of the lastmenstrual period if certain, or ultrasonography in thefirst trimester.

We based the diagnosis of TTTS on ultrasoundcriteria of discordant amniotic fluid volume, i.e.polyhydramnios in one and oligohydramnios in theother, defined by deepest vertical pools of >8 cm and<2 cm, respectively (Wittmann et al., 1981; Brennanet al., 1982). We recognised the donor twin by thefollowing features: smaller size, reduced liquor volumeand non-visible bladder size. Characteristic features ofthe recipient included increased size, polyhydramnios,a chronically full bladder and on occasion evidence ofcardiomegaly. We sought evidence of fetal hydrops,defined as the abnormal collection of fluid in any ofthe abdominal, pleural and pericardial body cavities orwithin the subcutaneous tissue space, in either thedonor or recipient fetus.

We obtained UA Doppler recordings from eachtwin taking care to ensure that these were notinadvertently taken from the co-twin by followingeach cord to its insertion using colour flow imaging.Venous Doppler insonation was undertaken of theumbilical vein (UV) and ductus venosus (DV) in therecipient (Hecher et al., 1995). We deemed abnormalany regular pulsatility in the UV synchronous with thecardiac cycle or absent or reversed flow in the DVduring atrial contraction. We sought evidence ofmitral valve and/or tricuspid regurgitation (MR/TR)in the four-chamber view of the recipient by colourand pulsed wave Doppler (Zosmer et al., 1994). Ifthere was an abnormal systolic colour jet of flowwithin the right or left atrium, we confirmed reg-urgitation on pulsed-wave Doppler by placing thesample volume (minimum 4 mm) at the level of thecoaptation of the atrioventricular valve leaflets anddemonstrating the presence of reversed flow across thevalve. We defined significant regurgitation as pansys-tolic with a maximum velocity >2 m/sec (Respondeket al., 1994). We confirmed non-visualisation of thebladder in the donor over time by persistent lack ofseparation of the vitelline arteries on colour Doppler.

All measurements were taken at the time ofpresentation with TTTS and at subsequent visits.Each case was staged according to the presence ofprognostic factors (Quintero et al., 1999). A total of28/60 patients (47%) had Stage III or IV disease, werecounselled and offered selective termination. Of these,15/28 patients (54%) consented to the procedure.

Selective termination was performed in the scanningroom under sterile conditions. We injected 1%lignocaine subcutaneously to provide local anaesthesiaand, where required, gave 2.5–5 mg boluses of intra-venous diazepam for maternal sedation. We made a2–3 mm skin incision to facilitate percutaneous intro-duction of the 3.3 mm port. If necessary, we perfor-med amnioreduction or amnio-infusion (n=4) withHartmann’s solution at 38uC to enable better access tothe target umbilical cord. We then introduced thebipolar diathermy forceps (Everest2; Figure 1) andunder ultrasound guidance grasped a free loop of

CORD OCCLUSION FOR ADVANCED TWIN–TWIN TRANSFUSION 71

Copyright # 2002 John Wiley & Sons, Ltd. Prenat Diagn 2002; 22: 70–76.

umbilical cord at a site away from the uterine wall toavoid uterine trauma. In Israel, the donor twin wasselected for termination in all cases on account of thegrowth restriction and critically abnormal Dopplers.In the UK, a combination of factors including thecondition of each twin or the accessibility of theumbilical cord were used in the selection criteria fortermination, with hydrops or severe cardiac dysfunc-tion used as relative indications for the affected fetusto be selected. We used colour Doppler to confirmcomplete cessation of umbilical cord blood flow. Webegan coagulation at 20 W, increasing in increments of10 W to a maximum of 50 W. We judged the effect ofcoagulation by the appearance of turbulence andsteam bubbles. Each coagulation episode lasted up to60 s. We then released the jaws of the forceps andinsonated the cord with colour Doppler to confirmabsence of flow. If flow was present further episodes ofdiathermy were applied. To ensure complete cordocclusion, we then coagulated two adjacent segmentsof cord in a similar manner (Figure 2). We admittedpatients to hospital overnight and rescanned thefollowing morning.

Following the procedure patients were scanned

every 2 weeks for fetal growth, liquor volume andumbilical Doppler. We noted the presence, timing andduration of preterm prelabour rupture of membranes(PPROM) together with delivery details. After deliv-ery, we examined all placentae and terminated fetuses

Figure 1 — Instrumentation and technique for bipolar diathermy of umbilical cord. (A) The 3 mm bipolar diathermy forceps (Everest2).(B) The target umbilical cord is visualised using colour Doppler and grasped with the diathermy forceps. (C) Diathermy is applied. (D) Thecord is released and absence of umbilical flow confirmed

Figure 2 — An umbilical cord from a monochorionic twin fetusselectively terminated at 20 weeks by bipolar diathermy (Case 1)inspected after delivery of the remaining twin at 35 weeks

M. J. O. TAYLOR ET AL.72


histologically to confirm prenatal diagnosis, mono-chorionicity and cord occlusion. In the UK weattempted placental injection studies in 7/10 cases(3/10 were unsuitable for study) to demonstrateintertwin anastomoses but placental infarction madethis technically difficult in most cases. We obtaineddetails of neonatal and paediatric outcome directlyfrom our own units and received discharge summariesfrom external units.

We used multiple linear regression to comparesubsequent growth (change in abdominal circum-ference) in surviving donors and recipients.

RESULTS

We performed cord occlusion on fifteen patients (sevenrecipients and eight donors) at a median gestation of21 weeks (range 18–28 weeks) (Table 1). Seven (47%)had Stage III and eight (53%) had Stage IV disease.The median length of procedure was 30 min (range7–60 min) and the median maximum power used was50 W (range 25–50 W). There were no failures of cordocclusion.

One patient (7%) with dichorionic triplets (Case 6)had a major intra-amniotic haemorrhage observedfrom a transplacental puncture site with the donorsubsequently dying in utero within 3 days. No obviouscause of death was seen at autopsy performed afterdelivery 8 weeks later. Another (Case 14) had anabruption requiring delivery within 24 hr of theprocedure with the recipient dying neonatally onDay 7. Cause of death was thought to be intractablecardiac failure, but no postmortem was performed.The incidence of PPROM within 3 weeks of theprocedure was 3/15 (20%) and the median intervalbetween treatment and PPROM (j3 weeks) was2 weeks (range 1–3 weeks). The median interval fromprocedure to delivery was 10 weeks (range 0–20 weeks)

and the median gestation at delivery 33 weeks (range24–38 weeks).

Overall single survival was 13/15 (87%). Excludingthe case with triplets, the overall co-twin survival inStage III/IV disease was 13/14 (93%). All survivors hadnormal neonatal outcome with no neurologicalabnormalities evident prior to discharge.

Three donors and four recipients had absent/reversed end diastolic flow (AEDF) in the umbilicalartery prior to the procedure. After the procedure (inmost cases <24 hr later) positive end diastolic flow(EDF) was seen in all cases where it was previouslyabsent. Further, AEDF did not later develop wherepreviously EDF had been present. Growth velocitiesfor non-terminated donors and recipients are shownin Figure 3. Comparison of regression slopes showedno significant interaction term (p value for inter-action=0.92) indicating that the regression lines wereparallel. The linear equations were AC (mm)=x25.08+10.096 (weeks) – 40.651(X) where X=0 fora recipient or 1 for a donor twin.

Monochorionicity was confirmed in all cases inwhich placentae were injected. Arteriovenous anasto-moses from donor to recipient were identified in allthree placentae where injection was not technicallyprecluded by placental infarction.

DISCUSSION

The present pilot study suggests that bipolar cordocclusion is an effective method for selective fetocidein monochorionic twins, and is associated with a highrate of single survival in advanced or preterminalTTTS.

Empirically, the 93% co-twin single survival ratedocumented in the present series seems marginallybetter than the 80% survival reported in the only smallseries (five patients) reported to date (Deprest et al.,

Table 1 — Clinical details of the cases included in the present study

CaseDonor(D)/recipient(R) selected

Gestational ageat intervention(weeks)

TTTSStage

Operationtime (min)

Maxpower (W)

Gestationalage at delivery(weeks)

Birthweight (g) Outcome

1 R 20 3 60 50 35 1420 Alive and well2 D 24 4 20 45 38 2440 Alive and well3 D 21 3 60 50 29 1255 Alive and well4 R 20 4 50 50 40 3126 Alive and well5 R 18 4 50 50 33 2020 Alive and well6a R 18 3 38 50 26 464 IUD 18/40 weeks7 D 21 3 30 50 27 1081 Alive and well8 R 21 4 31 50 24 565 Alive and well9 R 25 3 9 50 37 2900 Alive and well

10 R 18 4 25 50 36 2080 Alive and well11 D 25 3 15 35 35 2740 Alive and well12 D 21 4 12 25 35 2530 Alive and well13 D 22 3 7 25 31 1740 Alive and well14 D 28 4 30 30 28 1350 NND at 7 days15 D 25 4 10 35 35 2640 Alive and well

aDichorionic triplets.IUD, Intrauterine death, NND, Neonatal death.



2000) of cord occlusion in TTTS. Most experiencewith selective fetocide in monochorionic twins hasbeen with twin reversed arterial perfusion sequence(TRAP) rather than TTTS. Blood flow within theacardiac twin’s cord is likely to be lower than eitherthe donor or the recipient twins’ cord in TTTS,making occlusion technically easier. This may alsoexplain the success of monopolar diathermy in TRAP(Rodeck et al., 1998) but apparent failure in TTTS(Rodeck, personal communication).

In the present series, the two cases complicated byperinatal loss arose because of intra-amniotic haemor-rhage and abruption. As these occurred within 24 hr,they are probably procedure-related and are unlikelyto be specific to this technique, reflecting insteaduterine instrumentation, since similar complicationshave been reported at both amnioreduction and lasertreatment.

Although effective at cord occlusion, a drawback tothis technique is the high rate of PPROM within3 weeks of the procedure (20%). This probably reflectsthe length of the procedure and the calibre ofinstrument. Despite this, the average gestation atdelivery was 33 weeks and procedure to deliveryinterval 10 weeks. As experience increases, proceduretimes, seen to reduce over the course of the presentstudy by half in both centres, should shorten furtherand then PPROM rates fall.

The choice of fetus for termination is controversial.Traditionally, the donor has been chosen for tworeasons. First, it was thought that the usual directionof anastomoses from donor to recipient made reverseexsanguination less likely. However, it is well knownthat recipient to donor exsanguination can occur(Denbow et al., 1998a) and indeed to be anticipated

given that anastomoses from recipient to donor areoften present (Denbow et al., 2000). Second, the donoris often growth-restricted and has abnormal Dopplerrecordings – features previously thought unlikely toresolve. It had been argued that if the recipient wasterminated the donor might continue in utero for onlya few weeks more before delivery would be indicatedfor fetal compromise/growth restriction. However, thepresent series suggests in contrast that the recipientmay also be a suitable choice. First, abnormal donorUA Doppler changes normalised in both recipient anddonor survivors immediately after the procedure.Second, growth velocities of surviving donors did nottail off and were similar to those of recipients, albeitstarting from a lower level. Third, the recipient is moreaccessible and does not need a facilitatory amnio-infusion as was required in 4/8 donor terminations inthe present series. In addition, the recipient is morelikely than the donor to display hydrops and todevelop neonatal sequelae of neurological lesions(Denbow et al., 1998b) and cardiac dysfunction(Zosmer et al., 1994). Conversely, there has beenconcern that the oedematous recipient’s cord may betoo big to occlude. However, we encountered notechnical difficulty in completely occluding recipientcords up to 25 weeks’ gestation.

As well as suggesting that selection of the recipient isreasonable, the present findings also suggest that themajor determinants of abnormal umbilical Dopplers indonor fetuses are unbalanced intertwin transfusionrather than reduced placental territory and/or poorplacentation, since the latter are considered chronicchanges unlikely to reverse after selective termination.

A major difficulty with selective fetocide as atreatment option for severe TTTS is not only patients’

Figure 3 — Abdominal circumference growth curves for recipient and donor fetuses



and physicians’ natural reluctance to choose a treat-ment which can achieve a maximum overall survivalrate of only 50%, but that the treatment involvestermination of a structurally normal fetus at arelatively advanced gestation. Instead, conventionaltherapies are preferred with at least some hope of bothbabies surviving. Particularly difficult are Stage IIIcases where ‘prophylactic’ fetocide is offered based onidentification of poor prognostic markers (Taylor et al.,2000) to patients whose understandable preference isfor expectancy, opting for cord occlusion only whereone or both fetus(es) is/are preterminal. In the timeperiod of the present study, there were 13 Stage III/IVcases who declined selective termination. Excludingone case which was lost to follow-up and anotherwhere the parents opted to terminate the pregnancyat 22/40 weeks, the overall survival in those managedby non-selective termination techniques (amnio-reduction, septostomy or interstitial laser) was only23% (5/22).

Parents should be counselled that co-twin survivalrate exceeds 80% in this and other series (Lemery et al.,1994; Deprest et al., 1998, 2000). This equates with the85% (23/27) single survival achieved with laser in thetreatment of Stage III or IV disease (Quintero et al.,2000) when quoted in terms of at least one babysurviving. The overall survival rate of 46% (13/28)(=number of survivors/total number of twin fetuses)in this preliminary series is only marginally lowerthan the 57% (31/54) survival after laser treatment(Quintero et al., 2000) of Stage III/IV disease in theonly study to quote results by stage. Notwithstandingthis, the theoretical maximum total survival with cordocclusion is 50%.

At early gestations (<16 weeks) with smaller cords,there is the concern that selective fetocide by thistechnique may result in cord rupture. In addition, theinstrument calibre is relatively large raising concernsabout procedure-related loss. Instead, endoscopic orinterstitial laser cord coagulation in the first and earlysecond trimester remain alternatives. At later gesta-tions, an important factor is the size of the umbilicalcord, especially in the recipient, which, if too large,may render complete occlusion impracticable. Afurther consideration in gestations over 24 weeks isthe legality of the procedure. In the UK and Israel,late termination is legal if a fetus has a substantial riskof serious physical or mental handicap when born.

The present study suggests that bipolar diathermy isan effective technique for selective reduction ofmonochorionic twins complicated by Stage III or IVTTTS. We suggest that recipient and donor fetuses areequally appropriate choices for fetocide.

ACKNOWLEDGEMENTS

The authors wish to thank the Richard and JackWiseman Trust for financial support, and SportAiding Research into Kids (SPARKS) and theChildren Nationwide Medical Research Fund forequipment support.

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ultrasound-guided umbilical cord occlusion using bipolar diathermy for stage iii/iv twin–twin...

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