Maternal complications following open and fetoscopic fetal surgery: A systematic review and meta‐analysis

Abstract

Objective

To establish maternal complication rates for fetoscopic or open fetal surgery.

Methods

We conducted a systematic literature review for studies of fetoscopic or open fetal surgery performed since 1990, recording maternal complications during fetal surgery, the remainder of pregnancy, delivery, and after the index pregnancy.

Results

One hundred sixty‐six studies were included, reporting outcomes for open fetal (n = 1193 patients) and fetoscopic surgery (n = 9403 patients). No maternal deaths were reported. The risk of any maternal complication in the index pregnancy was 20.9% (95%CI, 15.22‐27.13) for open fetal and 6.2% (95%CI, 4.93‐7.49) for fetoscopic surgery. For severe maternal complications (grades III to V Clavien‐Dindo classification of surgical complications), the risk was 4.5% (95% CI 3.24‐5.98) for open fetal and 1.7% (95% CI, 1.19‐2.20) for fetoscopic surgery. In subsequent pregnancies, open fetal surgery increased the risk of preterm birth but not uterine dehiscence or rupture. Nearly one quarter of reviewed studies (n = 175, 23.3%) was excluded for failing to report the presence or absence of maternal complications.

Conclusions

Maternal complications occur in 6.2% fetoscopic and 20.9% open fetal surgeries, with serious maternal complications in 1.7% fetoscopic and 4.5% open procedures. Reporting of maternal complications is variable. To properly quantify maternal risks, outcomes should be reported consistently across all fetal surgery studies.

INTRODUCTION

The last 35 years have witnessed an expansion of fetal therapy options,1, 2 with surgery on the fetus, placenta, or cord now relatively common in tertiary‐level fetal medicine units. Enabled by advancements in imaging, surgical instrumentation and techniques, early diagnosis, and treatment of fetal anomalies are now possible for a wide range of conditions.3

The mother has been called an “innocent bystander” in fetal surgery,4 and generally, fetal therapy is almost exclusively offered to women who are healthy themselves. Fetal surgery poses risks to the mother not only during the procedure itself but also throughout the remainder of the index pregnancy, potentially during any future pregnancies and throughout the woman's entire life. Fetal surgery offers no direct medical benefit to the mother, and from an ethical perspective, maternal risks should be minor and acceptable to the mother and family.5

Information regarding safety of surgery is important for counselling and informed decision making; however, robust data on maternal complications of fetal surgery are lacking. One single‐centre study of maternal outcomes following both open fetal and fetoscopic surgery performed between 1989 and 2003 found a number of short‐term morbidities.6 A systematic review of maternal complications following fetoscopic laser coagulation for twin‐to‐twin transfusion syndrome (TTTS) in 1785 patients treated between7 1990 and 2009 observed an overall adverse event rate of 5.4% with severe complications in 1.0%. The aim of this study was to estimate the incidence of immediate and long‐term maternal complications of fetoscopic or open fetal surgery through a systematic review of the literature.

METHODS

Protocol and registration

This systematic review was conducted in accordance with preferred reporting items for systematic reviews and meta‐analyses (PRISMA) guidance.8 The protocol was registered with the international prospective register of systematic reviews (PROSPERO‐CRD42017082411).

Eligibility criteria

All randomised, cohort, and case‐controlled studies and case series reporting the results of open fetal or fetoscopic fetal surgery in humans from January 1990 to October 2018 were considered eligible. No language restrictions were applied. Systematic reviews, narrative review articles, and case reports were excluded. There is no accepted numerical definition of a case series.9 We used an empirical cut‐off of at least three cases because of the rarity of some procedures and conditions searched for.

Search strategy

A systematic review was conducted in MEDLINE, EMBASE, and Cochrane databases using free text and Medical Subject Headings (MESH). The electronic search strategy is described in the Supporting Information. Subsequently, a grey literature (first 100 hits in PubMed and Google Scholar) search was performed, and reference lists of relevant review articles were manually checked. Covidence software (Veritas Health Innovation Ltd, Melbourne, Australia) was used to eliminate duplicate articles and manage study screening.

Study selection

Two authors (A.S. and L.VdV.) screened all titles and abstracts independently, excluded irrelevant studies and then independently assessed the remaining full‐text articles for eligibility; disagreements were resolved by consensus. Studies were excluded if the full text was unavailable online and the abstract contained insufficient information. Studies with interventions which were not fully described or were performed on the neonate instead of the fetus were excluded. Interventions involving access to the uterus using a device with a total outer diameter of less than 1.5 mm were excluded; this cut‐off was chosen to avoid procedures performed with needles only (eg, amniocentesis, fetal blood transfusion, thoracocentesis or vesicocentesis). Studies of shunting were only included if the outer shunt diameter was greater than or equal to 1.5 mm or the shunt was inserted fetoscopically. Studies which did not report maternal outcomes were excluded. For the purpose of this study, preterm rupture of membranes (PROM), chorionic membrane separation (CMS), preterm labour, preterm delivery, and gestational age at delivery, although relevant, were not considered to be maternal complications. Studies from which data could not be extracted (eg, composite or combined outcomes given) and studies containing patient cohorts which appeared to have been published previously by the same authors were excluded.

Data extraction

Two authors independently extracted data (A.S. and E.B. for open fetal surgery studies, A.S. and C.F. for fetoscopic studies) and entered them into a standardised Excel (Microsoft, Washington, USA) form. Disagreements were resolved by consensus. The ex utero intrapartum treatment (EXIT) procedure was classified as open fetal surgery. Study characteristics noted included study design, underlying fetal condition, type of intervention, presence of a control group, gestational age at surgery, and number of patients in each study. Outcomes recorded for the duration of the index pregnancy included intraoperative complications (maternal death, placental abruption, uterine bleeding/haemorrhage, blood transfusion, organ damage, or anaesthetic complications), post‐operative complications (classified from the end of surgery until delivery; maternal death, placental abruption, uterine bleeding/haemorrhage, blood transfusion, sepsis, chorioamnionitis, other infections, pulmonary oedema, amniotic fluid embolism and other respiratory, gastro‐intestinal, cardiac, or wound problems), complications at delivery of the index pregnancy (uterine dehiscence or rupture or blood transfusion), and the need for additional treatment at any time during the pregnancy. Outcomes noted at any time following the index pregnancy (late outcomes) included fertility (number of further pregnancies, difficulty conceiving, mean time to conception), future pregnancy complications (miscarriage or preterm delivery), complications during future deliveries (uterine dehiscence or rupture or haemorrhage at delivery), gynaecological and psychological symptoms. When a study reported “haemorrhage” or an actual blood loss of greater than 1000 mL we noted this as “haemorrhage.” This cut‐off is an accepted definition of severe bleeding both in pregnancy10 and post‐partum.11 If a study did not specify whether a complication occurred intraoperatively or post‐operatively (eg, placental abruption and requirement for blood transfusion), then this was assumed to have occurred post‐operatively.

All complications were independently graded according to the Clavien‐Dindo classification of surgical complications12 by two authors (A.S. and L.VdV.) (Supporting Information). Clavien‐Dindo grade I or II complications were defined as mild; grades III to V complications were defined as severe.12

Quality assessment of studies

Study quality and risk of bias were analysed by two authors (A.S. and L.VdV.) independently using a standardised form. Randomised trials were analysed using the Cochrane Collaboration's tool for assessing risk of bias.13 Case‐control studies were analysed using the Newcastle‐Ottawa scale for assessing the quality of nonrandomised studies.14 Case series were analysed using the National Institutes of Health study quality assessment tool.15

Assessment of heterogeneity

Methodological and clinical heterogeneity of data per study were evaluated. Variables were tested for statistical heterogeneity by applying the I² test to determine whether data could be pooled. An I² value less than 40% was taken to indicate minor heterogeneity; 40% to 75% moderate heterogeneity and greater than 75% substantial heterogeneity.13

Meta‐analysis

Meta‐analysis for all outcomes was carried out using MedCalc statistical software version 15.4 (MedCalc Software, Ostend, Belgium). Results were expressed as proportions with 95% confidence intervals (CI) as all outcomes were categorical variables. Pooled proportions were calculated using both the fixed and random effects model in case of homogeneity or heterogeneity respectively.

RESULTS

Study selection

The electronic literature search identified 70 367 studies published between 1990 and 2018 (Figure 1); search of the grey literature and reference lists identified a further 16 studies. Following this, 48 248 studies were immediately removed as duplicates. The remaining studies (22 135) were screened by title and abstract, and a further 21 384 were excluded as irrelevant. Full texts of the remaining 751 articles were reviewed, and 585 were excluded for the following reasons: no reporting of maternal outcomes (175/585, 29.9% of studies excluded and 23.3% [175/751] of all studies assessed), insufficient information available (conference abstract/poster only or full text unavailable) (119/585, 20.3%), study design other than randomised trial, case‐control trial or case series (110/585, 18.8%), and uterine access using a device less than 1.5 mm (59/585, 10.1%). Thirty studies were translated from French (10), Spanish (seven), Polish (five), German (three), Dutch (two), Portuguese (two), and Turkish (one), of which 16 were included following review. Two Chinese‐language papers were identified, but the full text could not be accessed online. Eventually, 166 studies were included; 41 on open fetal surgery, 122 on fetoscopic surgery, and three studies including both surgery types.

Figure 1 Flow diagram of study selection adapted from preferred reporting items for systematic reviews and meta‐analyses (PRISMA)8 2009 (Figure not reproduced here; see the original article.)

Study characteristics

Characteristics of included studies are shown in Tables 1, 2, 3. Studies of open fetal (Table 1) and fetoscopic (Table 2) surgery are presented and analysed separately as the difference in surgical technique was considered too great for combined analysis. Seven studies specifically focused on late complications, ie, after the index pregnancy and are presented separately (Table 3). The majority of studies (68.1%, 113/166) were case series, ie, without a control group; 27.1% (45/166) were case control studies, and 4.8% (8/166) were randomised trials.

Risk of bias

Quality assessment of the studies is given in the Supporting Information. Most studies (139/166, 83.7%) had a low risk of bias or were high quality. All remaining studies (27/166, 16.3%) had an unclear risk of bias or were fair quality. No studies were found to have a high risk of bias or be low quality overall. For randomised trials, included studies had a high risk of bias with regards to blinding. For case control studies, included studies did not describe statistical methods well overall.

Statistical heterogeneity

Maternal outcome data were pooled in 64 separate meta‐analyses, of which 37.5% (24/64) had no or minor heterogeneity. In 39.1% (25/64), there was moderate heterogeneity, and in 23.4% (15/64), there was considerable heterogeneity. The levels of heterogeneity per outcome measure are listed in the Supporting Information. As both clinical and statistical heterogeneity were found, pooled proportions were given using the random effects model for meta‐analysis.

Maternal complications in the index pregnancy—intraoperative

Table 4 summarises maternal complications according to type of surgery performed. No maternal deaths (Clavien‐Dindo grade V) due to fetal surgery were reported in any study (10 596 procedures). One study86 reported a patient at 20 weeks' gestation experiencing a cardiorespiratory arrest prior to fetoscopy for laser photocoagulation. The cause was considered to be a combination of morbid obesity, spinal anaesthesia, and aortocaval compression and not related to the procedure, which had not commenced. An immediate delivery was conducted by hysterotomy as part of maternal resuscitation, and the patient made a full recovery. Another study47 reported brief maternal seizure‐like activity during open fetal surgery, which was thought to be anaesthesia‐related.

Haemorrhage severe enough to prompt delivery or termination of pregnancy at the time of surgery as a life‐saving procedure for the mother (Clavien‐Dindo grade III) occurred in 0.92% of open fetal (95% CI, 0.46‐1.62) and 0.26% of fetoscopic surgeries (95% CI, 0.17‐0.38). Three cases38, 45, 46 occurred because of placental abruption during open fetal surgery for myelomeningocele (MMC) repair, following which delivery occurred, with all three fetuses surviving. Two cases59, 75 occurred following laser photocoagulation for TTTS said to be due to “excessive bleeding from placental anastomoses” and the uterine wall, respectively. Two cases119, 121 occurred during selective reduction, with haemorrhage from the uterine wall prompting delivery. Finally, one pregnancy was terminated because of bleeding from a trocar placental injury during fetoscopic MMC repair.172

In total, placental abruption (Clavien‐Dindo grade III) occurred intraoperatively in 1.28% of open fetal (95% CI, 0.73‐1.98) and in 0.28% of fetoscopic surgeries (95% CI, 0.18‐0.39). Bleeding during the procedure was noted in 1.97% of open fetal (95% CI, 0.97‐3.31) and in 1.74% of fetoscopic surgery cases (95% CI, 1.25‐2.32). Intraoperative blood transfusion was required in 1.00% of patients undergoing open fetal surgery (95% CI, 0.53‐1.64) and in 0.27% undergoing fetoscopic surgery (95% CI, 0.18‐0.38). Intraoperative skin burns at the site of diathermy pads occurred in 0.26% of patients (95% CI, 0.17‐0.37) during fetoscopic surgery; this outcome was not reported in any open fetal surgery.

Maternal complications in the index pregnancy—postoperative

One study on laser photocoagulation for TTTS (n = 132)110 reported a maternal death from disseminated intravascular coagulation (DIC) 4 weeks following an uneventful procedure. A post‐mortem examination did not find any evidence of chorioamnionitis or amniotic fluid embolism, and the authors therefore concluded that this death was unrelated to the procedure.

Haemorrhage severe enough to prompt return to theatre for termination or delivery of the pregnancy within 24 hours was not reported following any open fetal surgeries but occurred following 0.25% of fetoscopic procedures (95% CI, 0.16‐0.37). This included one171 4‐hour post‐fetoscopic tracheal balloon removal with no cause of the bleeding found. There were two late placental abruptions, one113 12‐hour post‐laser photocoagulation, and one142 within 24 hours of bipolar cord coagulation.

Placental abruption occurred in 1.80% of patients following open fetal (95% CI, 1.14‐2.63) and in 1.29% following fetoscopic surgery (95% CI, 0.90‐1.75). Post‐operative blood transfusion was given to 3.36% after open fetal surgery (95% CI, 1.85‐5.29) and in 0.32% following fetoscopic surgery (95% CI, 0.22‐0.44).

Chorioamnionitis following open fetal surgery or endometritis following an EXIT procedure occurred in 4.13% of women (95% CI, 3.03‐5.40), and in 1.45% undergoing fetoscopic surgery (95% CI, 1.06‐1.90). Of those, PROM was reported to have occurred in 47.78% following open fetal surgery (95% CI, 23.01‐73.16) and in 36.31% following fetoscopic surgery (95% CI, 22.00‐51.99). One study reported severe chorioamnionitis 5 days after bipolar cord coagulation131 with septic shock and acute kidney injury, which resolved leaving 70% residual renal function. Sepsis was also reported in one patient61 with chorioamnionitis following fetoscopic laser photocoagulation and in one patient49 following open MMC repair who developed post‐operative peritonitis requiring an emergency laparotomy and delivery. Post‐operative pneumonia occurred in two patients—one132 following fetoscopic radiofrequency ablation (RFA), necessitating 3 days of intubation and intensive care unit (ICU) care and one requiring ICU admission36 following open MMC repair.

Pulmonary oedema occurred in 4.32% of open fetal surgery cases (95% CI, 2.32‐6.90), and in 0.63% of fetoscopic cases (95% CI, 0.43‐0.87). Three studies in which post‐operative pulmonary oedema occurred reported on perioperative fluid management (3/102, 2.9%), and 33 reported on the use of magnesium sulphate (33/102, 32.4%) without specifically suggesting causality. Six women required ICU admission, with four requiring intubation and ventilation; three following open fetal surgery,6, 20 and three following fetoscopic surgery.69, 87, 99

Maternal complications in the index pregnancy—at delivery

Only a few fetoscopic surgery studies (4/121 studies, 0.33%) reported findings or complications at delivery. Complications at delivery following open fetal surgery are shown in Table 4. Hysterectomy at or around the time of delivery was reported in two patients (Clavien‐Dindo grade III). In one case,44 caesarean delivery following open MMC repair in a woman with two previous caesareans, intra‐abdominal scarring and friable tissue eventually resulted in hysterectomy. In the second case,99 following laser photocoagulation for TTTS and PROM, a caesarean section was performed at 33 weeks' gestation. A hysterectomy was eventually required because of haemorrhage with DIC, and the patient spent 5 days in ICU, where she also experienced an iatrogenic pneumothorax.

Uterine rupture occurred in 0.90% of patients at delivery following open fetal surgery (excluding EXIT procedures) in the index pregnancy (95% CI, 0.41‐1.59), and uterine dehiscence occurred in 3.67% (95% CI, 2.01‐5.81). Blood transfusion was given to 1.83% of women (95% CI, 1.16‐2.65) at delivery following open fetal surgery.

Overall maternal complication rates

Table 4 displays maternal complications. In open fetal surgery, there was a 4.51% severe (95% CI, 3.24‐5.98), a 16.26% minor complication rate (95% CI, 11.17‐22.09), and a total complication rate of 20.86% (95% CI, 15.22‐27.13). For fetoscopic surgery, the corresponding rates were: 1.66% severe (95% CI, 1.19‐2.20), 4.33% minor (95% CI, 3.33‐5.45), and 6.15% total complications (95% CI, 4.93‐7.49). Complication rates in the six commonest fetal surgical procedures performed are displayed in Table 5.

Maternal outcomes following the index pregnancy (long‐term)

Table 6 shows subsequent pregnancy outcomes and long‐term maternal outcomes following a pregnancy in which fetal surgery was performed. New difficulties in conceiving were described in 3.81% of women after open fetal surgery (95% CI, 1.22‐7.76, reported in four studies); this outcome was not reported to occur after fetoscopic surgery (three studies). Pregnancy loss prior to 24 weeks' gestation occurred in 19.95% of pregnancies conceived following open fetal surgery (95% CI, 13.37‐27.48, three studies) and 13.67% of pregnancies conceived after fetoscopic surgery (95% CI, 9.34‐18.68, three studies). Preterm birth occurred in 20.49% of pregnancies following open fetal surgery (95% CI, 10.48‐32.81, four studies) and in 2.12% of pregnancies following fetoscopic surgery (95% CI, 0.02‐9.01; three studies). Uterine rupture or dehiscence occurred, respectively, in 6.89% (95% CI, 1.34‐16.27, reported in three studies) and 11.09% (95% CI, 5.34‐18.59) of pregnancies following open fetal surgery. None were mentioned in fetoscopy studies.

DISCUSSION

In this systematic review of the literature, we found an overall complication rate of approximately 21% for open fetal surgery and 6% for fetoscopic fetal surgery, of which minor complications occurred in 16% and 4% of surgeries, respectively. This maternal complication rate excludes obstetric complications, which may also have occurred (eg, PROM, CMS, preterm labour, and preterm delivery). Additionally, many studies of fetal surgery fail to document maternal complications. Out of 751 full‐text articles reviewed, 175 (23.3%) were excluded as no maternal outcomes were stated. Although 68 of these studies focused on a specific aspect of the surgery or its neonatal outcome, 107 studies (92 fetoscopic and 15 open) involving over 9000 patients did not comment on the presence or absence of any complications specifically affecting the mother's health. Often, the “maternal outcomes” stated meant in reality obstetric outcomes (eg, PROM and preterm labour). We also found that maternal complications were often presented from the fetal perspective (eg, fetal demise caused by placental abruption). Thirty included studies (18.1%) contained a statement that no adverse maternal outcomes were observed without specifying what was meant by maternal outcomes. Among these studies were some large series, including a study of 201 patients undergoing fetoscopic tracheal balloon removal150 and studies of 20073 and 50081 patients undergoing fetoscopic laser coagulation. It is unlikely that such large numbers of procedures had no maternal complications, and more likely that complications were either not perceived as serious, not reported and/or the patient follow‐up was incomplete. This lack of reporting has most likely led to an underestimation of the actual risk of maternal complications in our meta‐analysis. Conversely, when maternal complications were reported, there was a wide variability in which outcomes were discussed and how they were presented.

There was a severe complication rate (Clavien‐Dindo grade III or IV) of 4.5% in women undergoing open fetal surgery and 1.7% undergoing fetoscopic surgery. This is in keeping with a previous multi‐centre review of maternal complications following laser photocoagulation for TTTS,7 which found a 1.0% rate of severe complications and a 5.4% total rate of complications across all studies; however, when the authors only included studies, which systematically assessed maternal complications as a primary or secondary outcome, this rose to 1.8% for severe and 17.4% for all complications.

In almost all studies of fetal surgery reviewed, long‐term maternal follow up was not described. The seven studies that did so had a wide variation in the parameters described. Fertility does not appear to be negatively affected by fetal surgery, with the rates of de novo difficulties for conceiving in this review (3.81% following open fetal surgery and none following fetoscopic surgery) being comparable, if not less, than published rates of secondary infertility in the general population.180 Similarly, the rates of miscarriage described (19.85% following open fetal and 13.67% following fetoscopic surgery) are similar to rates of spontaneous miscarriage in women who have not undergone fetal surgery.181, 182, 183 Epidemiological studies184 have suggested a worldwide preterm birth rate of 11.1% with a rate of 8.6% in “developed regions.”184 In the United States and United Kingdom, it is estimated at 9.8%185 and 7.3%,186 respectively. The preterm birth rate in this review following open fetal surgery (20.49%) is higher than the usual prevalence, but not higher following fetoscopic surgery (2.12%). Open fetal surgery was followed by uterine rupture or dehiscence in 6.89% and 11.09% of subsequent pregnancies, respectively, which is in line with published rates of rupture (6.2%) and dehiscence (12.5%) following a classical caesarean section.187 Conversely, no uterine ruptures were reported following fetoscopic surgery.

This study included the commonest fetal procedures and, from a maternal perspective, involved similar surgical manipulations yet variable operating times. We included studies from multiple centres worldwide and attempted to identify the non‐English literature. It is therefore likely that these results are generalisable to fetal surgery performed outside the included studies. An obvious weakness of this systematic review is that most studies did not include a control group. Furthermore, we decided to pool data for meta‐analysis despite having high heterogeneity in some results. Another weakness is the extraction of patient data from papers, which is prone to error given the variable reporting; it is possible that some patients had more than one complication and this was not noted or cumulative rates were as a consequence miscalculated.

This systematic review has identified a significant rate of maternal complications, which should be discussed with patients before embarking on fetal surgery. Large studies allow an estimation of the likelihood of these events, insomuch as the cases in these series are unselected and consecutive. Our systematic review search strategy may have missed relevant yet rare complications. For example, a letter to a journal editor describing maternal convulsions during general anaesthesia188 was excluded as a case report according to our criteria. In this circumstance, it appears that the patient was also part of the cohort of a study that was included,47 but it is possible that other rare events published as case reports have been missed. An international, prospective registry of fetal and fetoscopic surgery, such as the Eurofoetus189 and NAFTNet190 registries, would be the best way to accurately determine complication types and rates and avoid missing rare complications.

CONCLUSION

The maternal risks of fetal surgery are accepted by many patients and health care professionals for the possible benefit to the fetus.191, 192 This systematic review finds that studies of fetal surgery focus on the fetal outcomes of the procedure, and many fail to describe maternal complications. Fetal surgery comes at a risk to the mother, which may be underestimated by fetal therapists because of under‐reporting and variable reporting quality. In order to properly quantify maternal risks, outcomes should be reported consistently across all studies of fetal surgery, preferentially in prospective registries.

CONFLICT OF INTEREST

All authors report no conflict of interest.

FUNDING INFORMATION

This research is funded by the Wellcome Trust (WT101957) and Engineering and Physical Sciences Research Council (ESPRC) (NS/A000027/1). J.D. is also funded by the Great Ormond Street Hospital Children's Charity Fund. A.L.D. is supported by the National Institute for Health Research University College London Hospitals Biomedical Research Centre. LvdV is funded with support of the Erasmus + Programme of the European Union (Framework Agreement number: 2013‐0040). This publication reflects the views only of the author, and the commission cannot be held responsible for any use, which may be made of the information contained therein.

Supporting information

Sacco A, Van der Veeken L, Bagshaw E, et al. Maternal complications following open and fetoscopic fetal surgery: A systematic review and meta‐analysis. Prenatal Diagnosis. 2019;39:251–268. 10.1002/pd.5421

REFERENCES

Associated Data

Supplementary Materials

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