11/26/2010 Safety of endoscopic retrograde cholangiopancreatography (ERCP) in pregnancy: A systematic review and meta-analysis Azab M, Bharadwaj S, Jayaraj M, Hong AS, Solaimani P, Mubder M, Yeom H, Yoo JW, Volk ML, - Saudi J Gastroenterol
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SYSTEMATIC REVIEW/META ANALYSIS  
Year :   |  Volume :   |  Issue :   |  Page :
Safety of endoscopic retrograde cholangiopancreatography (ERCP) in pregnancy: A systematic review and meta-analysis


1 Department of Gastroenterology and Hepatology, Loma Linda University Medical Center, California, USA
2 Department of Gastroenterology, University of Nevada Las Vegas, Las Vegas, Nevada, USA
3 Department of Internal Medicine, University of Nevada Las Vegas, Las Vegas, Nevada, USA
4 Department of School of Community Health Sciences, University of Nevada Las Vegas, Las Vegas, Nevada, USA

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   Abstract 


Background/Aims: Endoscopic retrograde cholangiopancreatography (ERCP) is a technically challenging procedure rarely associated with severe postprocedure complications. Hormonal changes during pregnancy promote cholelithiasis, but there are limited clinical data available on the outcomes of ERCP in pregnant women. ERCP techniques without irradiation were recently introduced as potential alternative. We performed a systematic review and meta-analysis to assess the safety of ERCP in pregnancy and to compare outcomes of radiation versus nonradiation ERCP.
Materials and Methods: A systematic search of PubMed, Medline/Ovid, Web of Science, and Google Scholar through April 18th, 2018 using PRISMA and MOOSE guidelines identified 27 studies reporting the outcomes of ERCP in pregnancy. Random effects pooled event rate and 95% confidence intervals (CIs) were estimated. Heterogeneity was measured by I2, and meta-regression analysis was conducted. Adverse outcomes were divided into fetal, maternal pregnancy-related, and maternal nonpregnancy-related.
Results: In all, 27 studies reporting on 1,307 pregnant patients who underwent ERCP were identified. Median age was 27.1 years. All results were statistically significant (P < 0.01). The pooled event rate for overall adverse outcomes was 15.9% (95% CI = 0.132–0.191) in all studies combined, 17.6% (95% CI = 0.109–0.272) in nonradiation ERCP (NR-ERCP) subgroup and 21.6% (95% CI = 0.154–0.294) in radiation ERCP subgroup. There was no significant difference in the pooled event rate for fetal adverse outcomes in NR-ERCP 6.2% (95% CI = 0.027–0.137) versus 5.2% (95% CI = 0.026–0.101) in radiation ERCP group. There was no significant difference in maternal pregnancy-related adverse outcome event rate between NR-ERCP (8.4%) (95% CI = 0.038–0.173) and radiation ERCP (7.1%) (95% CI = 0.039–0.125). Maternal nonpregnancy-related adverse outcome event rate in NR-ERCP was 7.6% (95% CI = 0.038–0.145), which was half the event rate in radiation ERCP group of 14.9% (95% CI = 0.102–0.211).
Conclusions: ERCP done by experienced endoscopists is a safe procedure during pregnancy. Radiation-free techniques appear to reduce the rates of nonpregnancy-related complications, but not of fetal and pregnancy-related complications.

Keywords: Endoscopic retrograde cholangiopancreatography, gallstones, pregnancy


How to cite this URL:
Azab M, Bharadwaj S, Jayaraj M, Hong AS, Solaimani P, Mubder M, Yeom H, Yoo JW, Volk ML. Safety of endoscopic retrograde cholangiopancreatography (ERCP) in pregnancy: A systematic review and meta-analysis. Saudi J Gastroenterol [Epub ahead of print] [cited 2019 Dec 5]. Available from: http://www.saudijgastro.com/preprintarticle.asp?id=271339





   Introduction Top


Physiologic changes during pregnancy are known to predispose to biliary disease.[1],[2] High levels of estrogen stimulate hepatic production and secretion of cholesterol.[3],[4] Rising progesterone also delays emptying of the gallbladder, which causes bile stasis and slows the release of bile acids that bind cholesterol.[3],[4] Together, these lead to the development of cholesterol gallstones. This risk is higher with each pregnancy, and multiparous women are 10 times more likely to develop biliary complications [Figure 1].[5] In a prospective study of 3,200 pregnant women without cholelithiasis on baseline abdominal ultrasound (US), new cholelithiasis or bile sludge was observed in 7.1% at second trimester, 7.9% at third trimester, and up to 10.2% at 6 weeks postpartum.[6] Of these, about 1.2% developed symptoms, and 10% of those with symptoms later developed serious complications such as acute cholecystitis, cholangitis, symptomatic choledocholithiasis, biliary strictures, or biliary pancreatitis that would necessitate therapeutic intervention.[6],[7]
Figure 1: Pathophysiology of gallstone formation in pregnancy

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Although the physiology of pregnancy itself increases the risk of biliary pathology, the management of these conditions in this patient population is poorly studied thus far. The mainstay in biliary intervention is endoscopic retrograde cholangiopancreatography (ERCP), which is therapeutic for many of these diseases.[8] In addition to the usual risks associated with ERCP, some inherent concerns arise in a pregnant female, including but not limited to exposure to radiation, medication teratogenicity, anesthesia, and changes in maternal anatomy.[3] The specific relative risks of these effects are not well established because current case studies are limited by small sample size. As opposed to esophagogastroduodenoscopy (EGD) or colonoscopy, ERCP requires real-time prolonged X-ray with significant amount of fluoroscopic radiation, which is a potential cause of developmental complications in utero. One study with 15 patients showed that on average, fluoroscopy time was 3.2 min [standard deviation (SD) ± 1.8 min] with total 3.1 millisievert (mSV) (SD ± 1.64 mSV) of radiation; in general, it is recommended during first trimester to limit exposure to less than 1 mSV, and over the entire pregnancy less than 5 mSV.[4]

Another concern is that the usual medications for sedation used during endoscopy are poorly studied in pregnant women. The most commonly used agents are propofol and ketamine.[9],[10] Both drugs at moderate doses are category B drugs and considered relatively safe to use in pregnancy due to rapid onset and short duration of effect.[9],[10] Of note, they require strict monitoring of levels by an experienced anesthesiologist and have not been well studied during first trimester pregnancy.[9] Other commonly used endoscopy agents such as benzodiazepines, meperidine, and narcotics are usually avoided due to their lower threshold for causing fetal neurobehavioral depression and potential birth defects.[4],[9] Finally, the usual post-ERCP adverse outcomes including postsphincterotomy bleeding (PSB), infection, pancreatitis, and perforation can have greater consequences in a pregnant woman.[3] Even less documented are any potential causal links between ERCP and induction of early labor, premature rupture of membranes, or even spontaneous abortion.[11]

Due to these concerns and the precarious nature of pregnancy itself, ERCP has historically been avoided in pregnancy. With the elevated risk of biliary disease that can occur in this patient population, avoidance of therapeutic measures can also become a cause of significant morbidity and mortality.[3] Currently, the management of these complications is poorly defined, and each case is decided on an individual basis – which can lead to clinician bias and postponement of critical care. Misunderstanding and misrepresentation of best standard of practice can lead to recurrent pain symptoms, high emergency department visits, more frequent hospitalization, or even death.[12] Fear of intervention stems from lack of access to information about the exact benefits versus risks. Available studies are few and scattered, so here we present a meta-analysis of retrospective case studies on ERCP in pregnancy to compare outcomes, establish methods to minimize risk of the procedure, and have better understanding of the procedure outcomes that can be used by gastroenterologists and physicians in future patient care.


   Materials and Methods Top


Search strategy

We performed a literature search using the keywords “ERCP,” “endoscopic retrograde cholangiopancreatography,” “pregnancy,” “endoscopy,” and “fluoroscopy” in various combinations to identify original studies published in English from PubMed, Medline/Ovid, Cumulative Index to Nursing and Allied Health Literature (CINAHL), Web of Science, and Google Scholar databases, through April 18th, 2018.

Inclusion and exclusion criteria

We included studies that reported outcomes of pregnant patients who underwent ERCP. We excluded studies that reported other endoscopic procedures in pregnancy.

Study selection and data extraction

Two authors (M.A. and M.J.) independently screened titles and abstracts. They obtained full articles that met the inclusion and exclusion criteria, and after an independent review, they extracted the data. For all phases, discrepancies were resolved in consultation with two other authors (M.M. and A.H.). We also hand-searched the eligible articles. Forty-seven studies relevant to inclusion criteria were added. The actual numbers of ERCP cases were collected from tables and manuscript text in each study. When actual data were not presented in certain studies, two authors (J.Y. and M.A.) directly contacted the corresponding authors of their studies to obtain the data. Since data were from previously published studies, an institutional review board approval was waived. Finally, 27 studies were selected. [Figure 2] presents the study selection process in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement.[13] A summary of studies is shown in [Table 1].[11],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23],[24],[25],[26],[27],[28],[29],[30],[31],[32],[33],[34],[35],[36],[37],[38],[39]
Figure 2: Study selection process

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Table 1: Summary of studies

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Study outcomes

We divided outcomes of ERCP in pregnancy into three categories. First, fetal outcomes, which included any fetal adverse outcomes reported during pregnancy, labor, or the follow-up period like intrauterine growth retardation, congenital malformations, fetal demise, and low birth weight. Second, maternal pregnancy-related outcomes, which included any pregnancy adverse outcomes reported after the ERCP procedure such as preterm labor, preeclampsia, or bleeding. Third, maternal nonpregnancy-related outcomes, which included all ERCP-related adverse outcomes that are not related to pregnancy, such as post-ERCP pancreatitis (PEP), PSB, or cholecystitis.

Quality assessment

We used the Newcastle–Ottawa Scale (NOS) to assess the risk of bias in the included studies.[40],[41] Risk of bias in relation to selection, comparability, and assessment of the exposure/outcome was assessed according to nine items using a star allocation scheme. Stars were allocated if a study was deemed to have a low risk of bias within each item, according to the coding manual provided.[42] A study was categorized as being of low risk of bias if a total of 8–9 stars were allocated, medium risk of bias if 6–7 stars were allocated, and of high risk of bias if the study was given ≤5 stars.

Data synthesis and analysis

We combined individual study results to calculate the pooled odds ratio (OR) and 95% confidence intervals (CIs) using the random effects method.[43] Between-study heterogeneity was assessed using the I2 static values of 50%, representing extensive statistical inconsistency. Subgroup analysis was performed to examine effects of irradiation on fetal and maternal outcomes. All analyses were performed using Comprehensive Meta-Analysis version 3 (Biostat Inc., Englewood, NJ, USA; 2014). A two-sided P value <0.05 was considered statistically significant.


   Results Top


A total of 1,307 patients from 27 retrospective studies were analyzed. Baseline characteristics from pooled study participants are reported in [Table 1]. The characteristics were grouped by adverse outcomes (fetal, maternal pregnancy-related, and maternal nonpregnancy-related): fetal adverse outcomes (n = 9), maternal pregnancy-related outcomes (n = 22), maternal nonpregnancy-related outcomes (n = 143).

[Figure 3] presents the meta-analysis results of the overall adverse events in pregnant patients; the pooled event rate was 15.9% (95% CI = 0.132–0.19). The results were statistically significant (P < 0.01). Heterogeneity was low (Q = 26, P = 0.370, I2 = 6.3%). Inamdar et al.'s study could be an outlier resulting in increasing the degree of heterogeneity.[16] When this study was removed from current meta-analysis, the magnitude of pooled event rate slightly increased to 18.1% (95% CI 0.144–0.226) and heterogeneity dropped to near zero (I2 < 0.01%).
Figure 3: Meta-analysis result of overall adverse events in pregnant patients undergoing ERCP

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The large number of patients in Inamdar et al. generated the outlier effect [Figure 4].[16]
Figure 4: Overall adverse events in pregnant patients undergoing ERCP without outlier effect

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[Figure 5] presents the meta-analysis results of the fetal adverse outcomes; the pooled event rate was 5.4% (95% CI = 0.035–0.083). The pooled event rate for maternal pregnancy-related adverse events in pregnant patients was 6.1% (95% CI = 0.040–0.093). The pooled event rate for maternal nonpregnancy-related adverse events in pregnant patients was 11.9% (95% CI = 0.102–0.138). The quality of evidence started low because analyzed studies were all observational. Symmetrical funnel plot was consistent with the absence of publication bias. No evidence of publication bias by Egger's regression test for all-cause was found. The final quality of evidence was high because no serious limitation was found in the NOS as shown in [Table 2].
Figure 5: Fetal outcomes' meta-analysis

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Table 2: Newcastle-Ottawa Scale for the included studies

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Subgroup analysis results were done by radiation exposure. Nine of 27 studies included both ERCP with radiation and NR-ERCP. They did not specify the outcomes based on radiation exposure. Nine studies included only NR-ERCP and another nine studies included radiation ERCP. NR-ERCPs were performed using three different techniques: abdominal US-guided ERCP, endoscopic ultrasound (EUS)-guided ERCP, and choledochoscopy-guided ERCP. Overall adverse events were less prevalent in the NR-ERCP group (pooled event rate of 17.6%, 95% CI = 0.109–0.272) versus radiation ERCP group (pooled event rate 21.6%, 95% CI = 0.154–0.294). There was no significant difference in the fetal adverse outcomes between the radiation ERCP group (pooled event rate 5.2%, 95% CI = 0.026–0.101) and the NR-ERCP group (pooled event rate 6.2%, 95% CI = 0.027–0.137).

Maternal pregnancy-related adverse outcomes were less prevalent in the radiation ERCP group (pooled event rate 7.1%, 95% CI = 0.039–0.125) in comparison to the NR-ERCP group (pooled event rate 12.0%, 95% CI = 0.065–0.211). However, the overlap in CI makes the results less statistically significant. Maternal nonpregnancy-related outcomes were more prevalent in the radiation ERCP group (pooled event rate 14.9%, 95% CI = 0.102–0.211) in comparison to 7.6% (95% CI = 0.038–0.145) in the NR-ERCP group. Again, the CI overlap affects the statistical significance despite the low P value. All results were statistically significant with P value <0.01.


   Discussion Top


To our knowledge, this is the first meta-analysis of the ERCP outcomes in pregnancy and the first to provide a head-to-head comparison between radiation ERCP and NR-ERCP. In this systematic review and meta-analysis, we found ERCP to be a relatively safe procedure during pregnancy. Intraoperatively, no complications were reported. Maternal post-ERCP adverse events included pancreatitis, PSB, cholecystitis, and one incidence of acute respiratory distress syndrome resulting in the only case of maternal death. The rate of ERCP-related maternal adverse outcomes was found to be slightly higher than the usual ERCP outcomes.[16] ERCP was also associated with an increased risk of preterm labor and preeclampsia, but there were no reported cases of abortion, bleeding, or intrauterine fetal death. With regard to fetal outcomes, ERCP was found to be relatively safe on the fetus without any reported cases of fetal congenital malformation or stillbirth, despite the increased risk of preterm labor and low birth weight. A subgroup analysis was performed to compare the outcomes of radiation ERCP versus NR-ERCP. NR-ERCP had a higher safety profile in terms of maternal nonpregnancy-related outcomes with lower rates of PEP and PSB. Regarding fetal outcomes, NR-ERCP showed no superiority to radiation ERCP. No congenital malformations were reported in both groups. However, both groups had an increased risk of preterm labor and intrauterine growth retardation.

Radiation exposure during fluoroscopy time in ERCP is used to visualize the anatomy of the biliary tract and ensure safe and successful biliary cannulation, stone extraction, and sphincterotomy. Different NR-ERCP techniques have recently been introduced to avoid possible radiation exposure fetal malformations. However, these techniques were not associated with better fetal outcomes in comparison to the radiation ERCP. This may be attributable to the fact that radiation exposure in ERCP is lower than the exposure needed to cause congenital fetal anomalies.[44] Fetal risk of anomalies, growth restriction, or abortion has not been reported with radiation exposure of less than 50 mGy, a level above the range of exposure in ERCP according to the American College of Obstetrics and Gynecology.[44] In one study, the estimated fetal radiation exposure in 17 cases of ERCP with limited fluoroscopy time (range 1–48 s) is 0.4 mGy (range 0.01–1.8 mGy).[11] Other factors that can affect the fetal absorbed dose of irradiation include orientation of the fetus, fetus size, procedure position, and body composition of the mother.[45] Although most of the fetal irradiation exposure comes from the radiation diffused from the maternal tissue, application of a lead apron is still routinely recommended.[11] Several other strategies are recommended to reduce the fetal irradiation exposure and complications, including decreasing fluoroscopy time, minimizing exposure areas, and application of electric grounding pad higher in the posterior thoracic wall level to avoid transmission of electric current to the fetus.[46],[47] Gestational age at the time of irradiation exposure is also crucial. Significant irradiation exposure before 16 weeks of gestational age has a higher risk of intellectual disability.[48]

The NR-ERCP group had lower rates of PEP and PSB in comparison to the radiation ERCP. This finding is unexpected and should be interpreted cautiously due to CI overlap. It may be attributable to the fact that NR-ERCP is a more sophisticated procedure which requires more equipment and a higher level of expertise in endoscopy and is thus only performed by high-volume practitioners. NR-ERCP is achieved through empirical bile aspiration technique and can be done with imaging guidance. Bile aspiration technique allows confirmation of common bile duct (CBD) cannulation and endoscopic sphincterotomy to be carried out without radiation, while imaging guidance can be provided by EUS, transabdominal US, or choledochoscopy. US allows recognition of the CBD stone site, confirmation of wire placement, and cannulation of the CBD. An US contrast agent (sulfur hexafluoride microbubbles) was injected through ERCP to improve visualization of the CBD as an alternative to fluoroscopy in a single case report.[49] No fetal complications were reported in this case report; however, the safety profile of this contrast material on the fetus is still unclear. US-guided ERCP showed higher rate of stone clearance in comparison to empirical NR-ERCP (89% vs 60%, P < 0.05) and lower complication rates (14% vs 3%, P < 0.05).[50] EUS can be carried out in the same session before ERCP to determine the number and site of stones before NR-ERCP is carried out with bile aspiration technique to clear the CBD.[51],[52] Another way to confirm biliary cannulation and stone clearance without radiation is by insertion of a choledochoscope through the working channel of EGD to directly visualize the bile duct.[53] Due to the scarcity of available literature, there are currently no available data that compare EUS-guided ERCP or peroral choledochoscopy-guided ERCP to empiric NR-ERCP.

Two-stage ERCP technique was introduced in a few reports. During pregnancy, NR-ERCP with empiric biliary aspiration and CBD stenting is performed. After delivery, a repeat ERCP is performed to remove the stent and ensure CBD clearance.[31] Extensive experience in ERCP is required in this technique as stent placement without fluoroscopy might lead to the stent misplacement either in the gallbladder or before the stone. A postprocedural US is required to confirm the position of the stent.

The following few points strengthen our confidence in the current meta-analysis results. First, statistical heterogeneity was very low. Second, the quality of the included studies was moderately high. Third, we found no evidence of publication bias. Nonetheless, we acknowledge several limitations. First, the risk of selection bias could have resulted in underreporting of ERCP adverse outcomes in pregnancy. Second, the duration of follow-up differed from one study to the other, and most patients were lost to follow-up 1 month after delivery. Third, studies were performed at different locations around the world with varying levels of expertise in endoscopy. Fourth, the heterogeneity in the NR-ERCP techniques could have affected the outcomes.

In conclusion, our findings support the notion that ERCP should continue to be the procedure of choice for bile duct decompression in pregnancy to prevent potentially life-threatening complications to both mother and fetus. Nonradiation techniques may decrease the risk of nonpregnancy-related outcomes, but do not impact fetal or pregnancy-related outcomes.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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Correspondence Address:
Mohamed Azab,
Department of Gastroenterology, Loma Linda University School of Medicine, 11234 Anderson Street, MC 1503A, Loma Linda, California - 92354
USA
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/sjg.SJG_92_19

PMID: 31744939



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