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Defining the Most Appropriate Delivery Mode in Women with Inflammatory Bowel Disease: A Systematic Review

Foulon, Arthur MD*; Dupas, Jean-Louis MD; Sabbagh, Charles MD, PhD; Chevreau, Julien MD*; Rebibo, Lionel MD; Brazier, Franck MD; Bouguen, Guillaume MD, PhD§; Gondry, Jean MD*; Fumery, Mathurin MD

doi: 10.1097/MIB.0000000000001112
IBD Live Articles

Introduction: High cesarean section (CS) rates are observed in patients with inflammatory bowel disease (IBD), but limited data are available to support this decision. We conducted a comprehensive review to evaluate the most appropriate mode of delivery in women with IBD according to disease phenotype and activity, as well as surgical history.

Materials and Methods: We searched MEDLINE (source PubMed) and international conference abstracts, and included all studies that evaluated digestive outcome after delivery in patients with IBD.

Results: A total of 41 articles or abstracts were screened, and 18 studies were considered in this review, with sample sizes ranging from 4 to 229 patients and follow-up ranging from 2 months to 7.7 years. Pooled CS rates in patients without Perianal Crohn's disease (PCD), healed PCD or active PCD, were 27%, 43%, and 46%, respectively. Regarding the median rate of new PCD (3.0% [IQR, 1.5–11.5] versus 6.5% [0–19.7]) or PCD recurrence (13.5% [3.2–32.7] versus 45% [0–58]), no increase was observed in patients with vaginal delivery compared to CS, but for patients with an active disease, worsening of symptoms was noted in two-thirds of cases. Episiotomy, perianal tears, and instrumental delivery did not influence the incidence of PCD. In patients with ileal pouch anal anastomosis, uncomplicated vaginal delivery seemed to moderately influence pouch function, with no significant difference in terms of overall continence, daytime, or night-time stool frequency, or incontinence. However, these parameters seemed negatively impacted by a complicated vaginal delivery.

Conclusions: New long-term data from well-designed studies are needed, but our review suggests that systematic CS in patients suffering from IBD should probably be limited to women at risk of perineal tears and obstetric injuries, with an active PCD, or with ileal pouch anal anastomosis.

Article first published online 14 April 2017Supplemental Digital Content is Available in the Text

*Obstetrics and Gynaecology Unit, Amiens University Hospital, Université de Picardie Jules Verne, Amiens, France;

Gastroenterology Unit, Amiens University Hospital, Université de Picardie Jules Verne, Amiens, France;

Digestive and Metabolic surgery Unit, Amiens University Hospital, Université de Picardie Jules Verne, Amiens, France; and

§Gastroenterology Unit, CHU Pontchaillou, Rennes, France.

Address correspondence to: Mathurin Fumery, MD, Gastroenterology Unit, Amiens University Hospital, Avenue Laennec Salouel, Amiens, France 80000 (e-mail: mathurinfumery@gmail.com).

Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal's Web site (www.ibdjournal.org).

The authors have no conflict of interest to disclose.

Received September 30, 2016

Accepted December 22, 2017

Inflammatory bowel diseases (IBDs) are chronic disabling diseases that typically affect young patients during the reproductive years.1 In case of pregnancy, delivery mode should be decided after a multidisciplinary discussion between the obstetricians, gastroenterologists, and colorectal surgeons.2 Indeed, many factors have an influence on the final decision such as the type, phenotype, and severity of the disease, a history of colorectal surgery and the global obstetrical context.2–6 As no clear international guidelines exist regarding delivery mode for women with IBD-marked variations in management can be confusing for patients.3 Current data regarding cesarean section (CS) indication are mainly derived from short, retrospective referral center cohorts with no large prospective studies assessing the most appropriate delivery mode for women with IBD.

The decision regarding delivery mode is driven by the fear of perianal injury, nonhealing wounds, fistula, and damage of the pelvic floor, all of which may lead to incontinence.4,7,8 High CS rates are consequently observed in patients with IBD regardless perianal status,4 although this procedure is itself known to be associated with morbidity, a risk of abdominal organ injury, as well as a risk of fistulization in the surgical wound.9,10

The European Crohn's and Colitis (ECCO) guidelines recommend standard vaginal delivery (VD) in patients with a quiescent or mild disease and CS in cases of women patients with active perianal lesions or active rectal involvements.4 However, in many other clinical situations, such as previous or nonactive perianal lesion, or ileal pouch anal anastomosis (IPAA), no guidelines are currently available from gastroenterological or obstetrical societies. The most appropriate mode of delivery according to disease phenotype, disease activity and previous surgery is currently unknown and remains debated.2,3

We conducted a rigorous and comprehensive literature review identifying articles that evaluated delivery mode in women with IBD. We aimed to summarize current knowledge on the most appropriate mode of delivery, according to disease history and phenotype.

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MATERIALS AND METHODS

Search Strategy and Selection Criteria

A computerized search of English and French language publications listed in the MEDLINE electronic databases (source PUBMED, 1966 to December 2015) was conducted by 2 independent researchers (A.F., M.F.) with the following search terms: “Inflammatory bowel disease,” “Crohn's disease,” “ulcerative colitis,” “delivery,” “ileal pouch anal anastomosis,” “ileorectal anastomosis,” “perianal lesion,” “perianal fistula,” “episiotomy,” “delivery,” “cesarean section,” “vaginal delivery,” and “pregnancy.” Abstracts from annual meetings of Digestive Disease Week (2012–2015), United European Gastroenterology Week (2012–2015), and European Crohn's and Colitis Organisation congresses (2012–2015) for the past 3 years, as well as references from review articles meta-analyses and published observational studies were also used to identify additional. The eligibility of study abstracts was evaluated according to pre-established inclusion criteria. Two reviewers (A.F. and M.F.) independently assessed the title and abstract of studies identified in the primary search for inclusion, and the full text of remaining articles were examined to determine whether they met the inclusion criteria. Any discrepancy in article selection was resolved by consensus after discussion with a third reviewer (J.-L.D.). All studies were referral center, hospital or population-based studies. Study inclusion criteria were (1) peer-reviewed observational studies, (2) English or French language, (3) including patients with Crohn's disease (CD) or ulcerative colitis (UC) and reported (4) digestive, perianal, or continence outcome after delivery.

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Data Extraction

Data extraction was performed independently by the 2 investigators (A.F. and M.F.) using a standardized data collection form. Collected data were (1) study characteristics: primary author, study period, year of publication, country of the population studied, population source, number of included patients, follow-up duration; (2) patients and IBD characteristics: age, disease duration, disease phenotype and location, history of digestive surgery, disease activity; (3) delivery characteristics: parity, delivery mode (CS and VD), episiotomy, perineal tear, instrumental delivery; (4) digestive outcome after delivery: disease activity and complications, PCD lesion and perianal healing, continence, manometry, and endoscopic ultrasound exploration (if available). Discrepancies in data interpretation were resolved by discussion and review of the studies and by consultation with the other clinical authors (J.-L.D., J.G.). One reviewer (M.F.) contacted the corresponding author for additional data or missing information, when necessary.

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Definitions

New PCD was defined by the occurrence of PCD in patients with no history of PCD-associated CD. PCD recurrence was defined by the recurrence of PCD in patients who had healed PCD before delivery. PCD worsening was defined by an aggravation of a PCD that was present before delivery.

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RESULTS

Literature Search

A total of 41 articles were selected according to the general search strategy (see Fig. 1, Supplemental Digital Content 1, http://links.lww.com/IBD/B493). Twenty-three studies failed to meet the inclusion criteria and were excluded. This included 11 studies evaluating fertility or pregnancy outcome in patients with IBD without providing any data neither on postpartum nor on the impact of delivery mode. Twelve other studies were also excluded for not being based on observational cohort. Detailed review finally identified 18 studies. These included 3 population-based studies, 7 different implicated countries, and patient enrollment spreading from 1984 to 2006. Sample sizes ranged from 4 to 229 patients and follow-up ranged from 2 months to 7.7 years.

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Crohn's Disease

Seven retrospective studies, 2 population-based studies and 5 referral center studies, including 544 patients, 640 deliveries with 455 (71%) VD were identified with follow-up ranging from 2 months to 5.2 years.5,11–16 Delivery mode in CD, which was mostly related to obstetrical features (64%) rather than IBD-related considerations, is detailed in Table 1, and indications for CS are reported in Table 2. Delivery mode according to perianal status (no PCD, healed PCD, active PCD) are detailed in Table 3. Mean CS rates in patients without PCD, healed PCD or active PCD were 27%, 43%, and 46%, respectively. The median rate of new PCD (3.0% [IQR, 1.5–11.5] versus 6.5% [0–19.7]) or PCD recurrence (13.5% [3.2–32.7] versus 45% [0–58]) did not seem to be increased by VD in comparison to CS. The outcome of PCD according to delivery mode is reported in Table 4. Five studies evaluated outcomes of 12 patients with VD and active PCD.5,11–14 Eight of them presented PCD exacerbation after delivery while 4 stayed stable and no PCD cicatrization was described over the study period. The PCD rates observed after the 2 types of delivery in the study by Ananthakrishnan et al15 was not significantly different after adjusting the propensity score according to the patient's risk.

TABLE 1

TABLE 1

TABLE 2

TABLE 2

TABLE 3

TABLE 3

TABLE 4

TABLE 4

Smink et al compared postdelivery outcome after episiotomies in patients with and without PCD. Half of patients with PCD and episiotomies reported CD progression including 18% reported fistula-related progression. Regarding patients without PCD having required episiotomies, half also reported postdelivery CD progression, but only 5% were related to fistula occurrence.14 In another referral center study, the occurrence of perianal fistula in patients with PCD was not impacted delivery mode, which included episiotomy, perianal tears or instrumental delivery. In terms of the need for anal surgery, number of anal surgeries after the diagnosis of fistulizing perianal CD and the need for a permanent stoma, there was no difference whether an episiotomy was performed or not.16

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Impact of Delivery Mode on Postpartum Disease Activity

Two studies assessed the impact of delivery mode on postpartum CD activity. In the population-based survey by Brandt et al,11 4 VD occurred in patients describing active luminal disease. Three of them reported worsening of their symptoms after VD. Smink et al compared postpartum outcome in 21 women with active luminal disease before pregnancy, to 93 with inactive disease. As expected, CD progression occurred more often in patients with active disease (Hazard Ratio 9.7, 95% CI, 2.1–44.3), but no significant difference was observed after a 2year follow-up between VD and CS (inactive luminal disease, 47% versus 45%; active luminal disease, 92% versus 88%).14

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Continence After Pregnancy in UC and CD

One population-based study was designed to compare fecal incontinence after VD among patients suffering from UC, CD, or none. A 100 cases of UC, 129 of CD, and a control group consisting of 116 healthy women were analyzed. Two cases of fecal incontinence after VD with episiotomy were observed in the control group. Twenty-seven patients with UC and 31 patients with CD described fecal incontinence after pregnancy, and 8 patients in each group attributed this symptom to their VD (relative risk, 8.27; P < 0.01).17

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Ileal pouch Anal Anastomosis

Ten retrospective referral center studies, including 470 patients with IPAA, evaluated the impact of delivery mode on their disease. Ninety per cent of these IPAA were due to UC. Follow-up ranged from 3 months to 7.7 years.6,18–26 See Table 5 for details.

TABLE 5

TABLE 5

When delivery took place before the disease's evolution led to IPAA, CS was performed in 10% of cases. However, when patients already had IPAA, 56% of delivery modes were CS (Table 5). Indications for CS (obstetrical vs IPAA-related considerations) are reported in Table 5. Delivery mode decision was based on the obstetrical situation in 56% of cases, the rest being guided by IPAA-related considerations in 44% of deliveries. In their work on IPAA-bearing pregnant women, Remzi et al reported that CS was indicated in 63% of cases by the colorectal surgeon and only in 14% by the obstetrician. Likewise, although 44% patients were informed by their obstetrician that VD was most suited in their cases, only 8% had this delivery mode recommended to them by their colorectal surgeon.18

Continence outcome according to delivery mode was reported in 8 studies involving a total of 358 patients (Table 5). The mean frequency of incontinence symptoms was 33% after VD and 54% after CS, with no significant difference in terms of overall continence, daytime, or night-time stool frequency, or incontinence. Worsening of incontinence after delivery (CS and VD), reported in 3 studies, affected 5% to 25% of patients, with follow-up ranging from 3 months to 2.4 years.19–21

Hahnloser et al compared pouch outcome after deliveries in 135 women (110 VD and 122 CS) to 307 nulligravida women after IPAA with a mean follow-up of 5.7 years. No significant difference was observed with the exception of a higher rate of use of stool regulating medications in patients with a history of pregnancy. Continence before and after pregnancy was also evaluated. More occasional day- and night-time incontinence was observed after delivery in comparison to before: 36% versus 20% (P = 0.01) and 63% versus 33% (P = 0.06), respectively.22 In the studies by Nelson et al and Juhasz et al, including a total of 63 patients with either VD or CS, 9 (14%) patients reported worsening of daytime incontinence after delivery, 45 (71%) reported no change, and 7 (11%) reported improvement. Ten (17%) patients reported worsening of night-time incontinence, 44 (70%) reported no change and 7 (10%) reported improvement.20,21

One study evaluated anorectal manometry in a cohort composed of 58 patients. Women with CS had significantly higher mean squeeze pressure than the VD group (150 versus 120 mm Hg, P = 0.049). Pudendal nerve motor latency and electromyography measurements were normal in both groups, but anal sphincter defects evaluated by endosonography were significantly associated with VD (OR 4.8; 95% CI, 1.1–21.7).18 In the study by Lepisto et al, 26% of patients had had surgically treated perineal tears, but none subsequently reported fecal incontinence.19

A survey from the Mayo Clinic cohort compared outcome of patients with VD without complications and women with vaginal tears or forceps delivery. No difference was observed in terms of day- and night-time stool frequency or incontinence, but there was an increase of occasional night-time incontinence as well as tendency toward a higher pad use in the second group.22 Poll et al evaluated pouch function after VD in 100 patients with a median follow-up of 7.7 years and identified the following incontinence risk factors: forceps or vacuum delivery, episiotomy, vaginal tears requiring perineoplasty, baby weight superior to 4 kg, prolonged second-stage labor, and emergency CS after a failed VD attempt.6

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Enterostomy

One study evaluated CD outcome after deliveries in 4 patients with ileostomy and one with sigmoidostomy. Delivery occurred by cesarean in 6 cases and vaginal in one. No stoma complication was observed.27

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DISCUSSION

We aimed to summarize the current knowledge on the impact of delivery mode on pregnant patients with IBD according to disease phenotype and history of intestinal surgery. All studies reported higher CS rates in patients with IBD compared with the general population, reflecting the physician's fear of the potential impact of VD on continence and the development of PCD. However, all studies also reported no significantly increased risk of developing PCD in patients with CD who did not have a previous history of such localization when comparing VD to CS (risk of developing PCD ranged from 0% to 31% of deliveries). Despite the limited data, episiotomy, instrumental delivery, and perineal tears do not appear to be associated with an increased risk of PCD; this led European ECCO guidelines to allow VD for women without history of PCD.2 A higher rate of episiotomies was observed in patients suffering from IBD in comparison to the general population and no explanation was provided by the various authors. A credible hypothesis could be that obstetricians, fearing an inclination of these women to develop higher degree perineal tear, have a tendency to readily perform so called “prophylactic” episiotomies. However, no study has compared systematic episiotomy to natural perineal tears on the risk of PCD occurrence or worsening.

As expected, CS rates were higher in patients with an active or a history of PCD. ECCO guidelines indeed recommend CS in patients with active perianal lesions with a grade C recommendation (defined as based on case-reports, inferior quality cohorts, and case–control studies).2 The few studies that investigate this subject had a small number of participants, and most of these patients had shown worsening of active PCD lesions after VD. Nevertheless, the decision of delivery mode in those women should not be entirely based on the mere presence of these lesions. Several others parameters could have an influence and should be taken into account: chronic lesions, multiparity, history of tears, and/or episiotomy as well as inexisting perineal tearing risk factors. Moreover, other items probably also have an impact such as type of perianal lesion, fistula differentiation (simple or complex/anterior or posterior), presence of strictures or anal canal ulcers (Fig. 1). Some well-selected patients may benefit from a VD even in the case of PCD. However, the paucity of the current literature means that we should act cautiously in promoting CS to these patients and wait for new studies to assess this hypothesis.

FIGURE 1

FIGURE 1

No evident increase in the risk of recurrent PCD was observed in patients with a history of healed PCD between VD and CS. Although the risk of recurrent PCD after VD may be higher in patients with history of healed PCD, this risk is moderate and can be estimated to be between 0% and 26% in the various studies. One study identified colonic CD (Hazard Ratio 3.3; CI 95%, 1.3–11.3) and perianal fistula before surgery (Hazard Ratio 2.8; CI 95%, 1.3–4.5) as risk factors for PCD after delivery.16

Current data, though limited, tend to be in favor of VD in patients with no history of PCD. For patients with healed PCD, the identification of certain factors, predictive of perineal tears, should guide the practitioner toward the most appropriate delivery mode. These factors are primiparity, estimated fetal weight superior to 4000 g, and other identified risk of shoulder dystocia, dystocic cephalic or breech presentations, induction of labor, prolonged second-stage of labor, epidural analgesia, short anopubic distance, and stiff perineal fiber consistency (Fig. 1).27–35 In any case, the final decision should be taken after a multidisciplinary, primarily between obstetricians and gastroenterologists. However, the insufficient data on long-term continence after VD in patients with IBD limit the general application of our algorithm. Finally, the recent Toronto consensus group recommended that decision of the mode of delivery should be based primarily on obstetric considerations while also considering patient preference. For women with CD who have active perianal disease, cesarean delivery is recommend over VD to reduce the risk of perianal injury.

For women with an active luminal disease, the impact of delivery on the IBD activity has been but poorly evaluated. One author, notwithstanding, has assessed that delivery mode had no significant influence on luminal disease activity.14

Another complex situation concerns patients with IBD with IPAA. Abundant literature is available regarding the impact of delivery mode on pouch outcome, but results are discordant. The first reason explaining these inharmonious outcomes is the fact that the different practitioners implied in the decision often disagree. Indeed, the answers to a recent survey showed that one-half of patients with IPAA asked 2 or more specialists for advice regarding the best mode of delivery and 70% of them received conflicting recommendations.3 Although only 12% of obstetricians agreed with most colorectal surgeon's advice for CS as delivery mode in patients with IPAA, obstetric indications for VD should nevertheless, in those situations, be weighed up against the potential consequences of sphincter and pelvic floor impairment on present and future bowel function. In everyday practice, although uncomplicated VD is proven to have a little impact on patients with optimal pouch function before delivery, CS is generally the preferred choice of delivery by fear of anal sphincter injury, which is the key factor implicated in continence in these women. And this is where one of the major issues resides: when is it safe to authorize VD for a patient with a satisfactory pouch function? One study addressed this question with the following conclusions: VD associated with an increased risk of obstetric injury was associated with significantly poorer functional outcome probably because of occult sphincter and pelvic floor damage.6 These situations included instrumental delivery, episiotomy, vaginal tears requiring perineoplasty, baby weight superior to 4 kg, and prolonged second-stage labor. Last, another reason explaining the complexity of evaluating the potential repercussions of VD on pouch function in case of IPAA is the fact that all available data are derived from retrospective referral center cohorts with a maximum follow-up of only 7 years. Only limited long-term information is available, and occult sphincter injuries, observed in up to one-third of women, may not become clinically significant for many years. Indeed, one study reported impaired anorectal manometry and an increased sphincter defect rate after VD in comparison to CS.18 To conclude on patients with IPAA, they should be thoroughly informed about the risk of VD on long-term pouch function and the choice of delivery mode should be based on a careful assessment of the patient's situation and preferences. New long-term data are needed, but CS may probably not be systematic in these women. VD may be considered in patients with optimal pouch function before delivery, and without risk for obstetric injuries or abnormal perineal scar tissue. In the absence of long-term data, the Toronto consensus suggests consideration of CS to reduce the risk of anal sphincter in women with IBD who have undergone IPAA.36

Currently, decision of delivery mode regarding pregnant patients with IBD is currently based on weak medical proof. Indeed, the studies on which obstetricians and gastroenterologists base their recommendations are often retrospective, monocentric, and with a short follow-up. In our literature review, median follow-up was only 2 years (0.25–7.7), whereas impact of occult sphincter injuries usually becomes clinically significant only after many years. New long-span prospective studies are therefore a necessity. Moreover, patients included in studies taking place in referral centers, which was most cases of works done on this subject, usually presented more severe or/and complicated diseases than the general population. This constitutes a major bias in the elaboration of global guidelines, as delivery mode, being based on the patient's risk, is greatly influenced by the different characteristics of her IBD. Indeed, CS was easily recommended in most situations in these high-risk patients, and those for whom VD was nonetheless approved probably were in fact at a lower risk of complication than most women forming the everyday baseline population, thus a likely underestimation of the real rate of VD complications. Randomized control trials would be the best method to definitely assess the question. However, it does not seem to be ethically feasible. Actual data are provided by small retrospective referral center studies. We think that new prospective, large-scale population-based studies are still needed to assess the actual impact of VD in women with IBD. Propensity scores adjustment (for selection of mode of delivery) could help to take into account variables that predict CS. New long-term follow-up data are now essential to assess the impact of VD on long-term continence. Finally, certain factors and their influence on VD outcome need to be urgently addressed, as they currently seem to be insufficiently evaluated. These include: type of fistula, strictures, or anal canal ulcers and luminal disease activity.

In conclusion, choosing the most appropriate delivery mode in patients with IBD is a complex decision. It must be based on a multidisciplinary approach, but it seems that in most circumstances, VD is an acceptable option. Though new data from well-designed population-based cohorts with long-term follow-ups are needed, our comprehensive review suggests that CS indications may therefore be limited to the usual obstetrical situations in most of patients with IBD, except women at high risk of obstetric injuries, patients with active PCD and probably in patients with IPAA.

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    Keywords:

    Crohn's disease; ulcerative colitis; vaginal delivery; cesarean section; perianal disease; ileal pouch anal anastomosis

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