Abstract
Background
Endoscopic retrograde cholangiopancreatography (ERCP) is currently the treatment of choice for symptomatic choledocholithiasis in pregnant patients. We aimed to present our experience with pregnant patients who underwent nonradiation ERCP and to evaluate the safety and efficacy of a new technique.
Methods
A retrospective analysis of nonradiation ERCP in 22 pregnant patients with symptomatic choledocholithiasis between January 2002 and December 2013 was performed. The bile aspiration technique with wire-guided sphincterotome was used to confirm selective biliary cannulation. Transpapillary pancreatic septotomy was performed in cases with difficult biliary cannulation (n = 3). After endoscopic biliary sphincterotomy, endoscopic papillary balloon dilation was performed with a 6- or 8-mm dilation balloon in all patients to reduce the risk of recurrent cholangitis because of residual or additional stones. Stones were extracted by balloon sweeping after dilation. All patients were followed for 6 months after the ERCP procedure.
Results
Biliary cannulation was achieved in all patients. Endoscopic papillary balloon dilation was performed with a 6-mm balloon in 17 patients and an 8-mm balloon in five patients. The stones were extracted in 18 of the 22 patients by balloon sweeping, but no stones were extracted in the remaining four patients. There were two cases of mild post-ERCP pancreatitis. All patients delivered at term, and none experienced recurrence of choledocholithiasis and/or cholangitis during the 6-month follow-up.
Conclusions
Endoscopic biliary sphincterotomy plus endoscopic papillary balloon dilation in nonradiation ERCP is a safe and effective treatment method for symptomatic choledocholithiasis during pregnancy.
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Pregnancy is associated with an increased risk of gallstone formation because of increased cholesterol saturation of bile and a reduction in gallbladder motility [1]. Fortunately, complications due to cholelithiasis, such as cholecystitis, choledocholithiasis, cholangitis, and pancreatitis, are relatively uncommon; however, these complications can potentially result in fatal consequences to both the mother and fetus [2]. Approximately one in 1200 deliveries is complicated by symptomatic choledocholithiasis [3].
Endoscopic retrograde cholangiopancreatography (ERCP) is currently the intervention of choice for the treatment of symptomatic choledocholithiasis during pregnancy [4]. In a large series of pregnant patients, the calculated ERCP rate has been reported as one per 1415 births [5]. The use of ERCP in pregnancy is likely to be limited because of the concern regarding potential impacts of ionizing radiation on the fetus. A definitively safe radiation dose for ERCP in pregnancy is still unknown. Radiation risks associated with ERCP procedures are not insignificant and cannot be disregarded [6]. The radiation detriment to the conceptus is divided into two types of effects: deterministic and stochastic. Deterministic effects, such as growth and mental retardation, are expected for conceptus doses above 100–200 mGy [7]. Stochastic effects are those for which, in theory, there is no threshold dose, and these include cancer and genetic abnormalities. The dose threshold (more than 100–200 mGy) is not expected to be exceeded to induce deterministic effects during ERCP. The major concern is the potential increase in stochastic effects such as childhood cancer [6, 8]. There are no data regarding the long-term effects of fluoroscopically guided ERCP during pregnancy. Hence, for fetal safety, it seems that no exposure is better than any exposure [9]. Several published studies [8–14] have advocated that ERCP during pregnancy can be performed safely without using fluoroscopy. The major concern in using nonradiation ERCP during pregnancy is the possibility of failing to remove all biliary stones or sludge that can lead to recurrent cholangitis [15].
Gastrointestinal endoscopy societies recommend that ERCP should be performed by experienced ERCP endoscopists in pregnant women [16]. Ege University Medical School is an experienced center for therapeutic ERCP in Turkey, with approximately 1500 ERCPs performed annually. In this study, our aim was to present one of the largest single center experiences with nonradiation ERCP and to evaluate the safety and efficacy of our new approach.
Patients and methods
All pregnant patients who underwent nonradiation ERCP because of symptomatic choledocholithiasis in the Ege University Medical School, Division of Gastroenterology, between January 2002 and December 2013 were retrieved through the database and analyzed through chart review. A total of 22 pregnant patients were included. The patients’ history, physical examination, procedure indications, laboratory investigations, radiologic imaging, ERCP complications and outcomes, delivery, and fetal outcomes were reviewed. The institutional review board approved the study protocol, and all patients included in the study signed an informed consent for the ERCP procedure.
Evaluation of patients before the ERCP procedure
Complete blood count, prothrombin time, and biochemistry tests, including liver function tests, renal function tests, electrolytes, and serum amylase, were obtained and repeated after ERCP. Transabdominal ultrasonography (US) was performed in all patients to determine the presence of cholelithiasis, cholecystitis, choledocholithiasis, pancreatitis, and common bile duct (CBD) dilation. All patients had an intact gallbladder. Biliary dilation greater than 6 mm was defined as biliary ductal dilation.
Eighteen patients had a high probability (>50 %) of choledocholithiasis based on clinical predictors according to criteria from the American Society for Gastrointestinal Endoscopy (ASGE) guidelines [17]. Accordingly, these 18 patients had the presence of one very strong predictor of choledocholithiasis (i.e., choledocholithiasis on transabdominal US, clinical ascending cholangitis, or bilirubin level > 4 mg/dL) or both strong predictors (dilated CBD on transabdominal US [>6 mm] and bilirubin level 1.8–4 mg/dL). The remaining four patients were assigned to an intermediate probability of choledocholithiasis based on clinical predictors (i.e., cholelithiasis on US, typical pain, and abnormal liver biochemical test other than bilirubin). In these four patients, choledocholithiasis was confirmed by magnetic resonance cholangiopancreatography (MRCP).
ERCP technique
All ERCP procedures were performed by an endoscopist (GE) with experience in more than 10,000 ERCP procedures. After an overnight fast, patients were positioned in the lateral decubitus position to avoid caval or aortic compression and mild-to-moderate conscious sedation was achieved using midazolam and/or propofol. Maternal monitoring was performed by recording pulse, blood pressure, and electrocardiography. Fetal heart tones were assessed by obstetricians before and immediately upon completion of the procedure. Prophylactic antibiotics were not given routinely.
ERCP was performed with a therapeutic duodenoscope (Olympus TJF-160, JF-240, TJF-145; Olympus, Tokyo, Japan). Selective biliary cannulation was attempted with a sphincterotome and a 0.035-inch hydrophilic-tipped guidewire (Jagwire, Boston Scientific, Natick, MA). Successful biliary cannulation was confirmed by aspirating bile into the sphincterotome with a syringe. If the pancreatic duct was entered (defined by clear aspirate in the sphincterotome and syringe), the guidewire was simply withdrawn and attempts to redirect it toward the CBD were made. If biliary cannulation was not achieved after three attempts, transpancreatic papillary septotomy (TPS) was performed to facilitate biliary cannulation. After biliary cannulation was achieved, an endoscopic biliary sphincterotomy (EST) was performed using pure cut electrosurgical current (ERBE, Tubingen, Germany) and the guidewire was advanced at least 10 cm into the bile duct; if resistance was detected, the tip of the sphincterotome was bowed slightly and reoriented for optimal guidewire advancement. By assuming that residual stones might be present, we modified our technique in the following way; to facilitate spontaneous passage of residual or additional stone(s) into the duodenum, endoscopic papillary balloon dilation (EPBD) was performed using a balloon-tipped catheter (Eliminator Biliary Balloon Dilators, ConMed, Utica, NY) according to the diameter of the CBD on the US and/or MRCP: a gradual inflation up to 6 mm in patients with CBD diameter ≤ 7 mm and up to 8 mm in patients with CBD diameter >7 mm. Thereafter, a 10-mm stone extraction balloon catheter (DURAglide Stone Balloon, ConMed, Utica, NY) was advanced over the guidewire, inflated, and pulled back gently until the stone was extracted through the papilla. The balloon sweep was repeated several times until the duct clearance was considered to be fully achieved. A biliary stent was not placed in any case. Fluoroscopy or spot radiographs were not used throughout the procedure.
After the ERCP procedure, patients were monitored for early complications and were observed daily in the hospital until discharge. Post-ERCP pancreatitis (PEP) was defined as abdominal pain within 48 h following the ERCP with at least threefold elevated levels of serum amylase, requiring prolongation of hospitalization. Elective cholecystectomy was routinely scheduled in all patients after discharge. All patients were followed for 6 months after the procedure for post-ERCP late complications: recurrent choledocholithiasis and cholangitis. Fetal outcomes were assessed at delivery and at 6 months post-delivery.
Results
During the study period, a total of 22 pregnant patients underwent nonradiation ERCP because of a diagnosis of symptomatic choledocholithiasis. Table 1 shows the baseline characteristics of the patients. The median maternal age was 26 years (range 19–32 years), and the mean duration of gestation was 26 weeks (2 in first trimester, 3 in second trimester, and 17 in third trimester). Fifteen women were in their first pregnancy; the other seven were in their second pregnancy. Before ERCP, choledocholithiasis was identified in radiologic studies in 12 patients (eight with US, four with MRCP). All patients had cholelithiasis ranging from 2 to 5 mm as documented by US. Elevated liver enzymes in varying degrees were noted in all patients (Table 1). Two patients had acute cholangitis clinically, and two patients had acute cholecystitis.
Therapeutic ERCP was successfully performed in all patients. Table 2 summarizes the ERCP findings, outcomes, and complications. Biliary cannulation was achieved following a TPS in three patients. Stones between 2 and 6 mm were extracted in 18 of the 22 patients by balloon sweeping, but no stones were extracted in four patients. MRCP correctly diagnosed choledocholithiasis in four patients; all of these had a stone on ERCP. EPBD was performed with a 6-mm balloon in 17 patients and an 8-mm balloon in five patients.
There were no complications related to medications used for sedoanalgesia in the mother and fetus after the procedure. Complications of the ERCP procedure occurred in five patients; all were mild in severity. Post-ERCP epigastric pain was observed in two patients. No amylase or lipase elevation was detected in these patients, and the pain was resolved within 24 h. Two patients developed mild pancreatitis, but responded well to conservative treatment. Minor post-sphincterotomy bleeding occurred in one patient, who was successfully treated with an epinephrine injection without the need for a blood transfusion. In all patients, no secondary ERCP procedures were needed until discharge and the end of the follow-up period. All patients were completely relieved of their symptoms.
The course of pregnancy was, in each case, entirely normal with delivery of a healthy child at term. None of the patients had symptoms of choledocholithiasis and/or cholangitis during the 6-month follow-up after ERCP.
Discussion
In the current study, we presented one of the largest series of pregnant patients who underwent nonradiation ERCP because of symptomatic choledocholithiasis. Biliary cannulation was successfully achieved in all patients, and only two patients experienced post-ERCP pancreatitis. Our results demonstrated that endoscopic biliary sphincterotomy and endoscopic papillary balloon dilation in nonradiation ERCP is a safe and effective treatment option for pregnant patients suffering from symptomatic choledocholithiasis. To our knowledge, this is the first study to evaluate this technique in pregnant patients.
To increase the success rate, we used the wire-guided cannulation technique for biliary access, and cannulation was successful in all patients. If there was difficulty in achieving deep biliary cannulation, TPS was performed. After an EST, EPBD was carried out to facilitate spontaneous passage of residual stones that might be otherwise missed or additional stones that could migrate from the gall bladder. Following this, the bile duct was cleared with balloon sweeping.
The major limitations of nonradiation ERCP during pregnancy include difficult cannulation without fluoroscopy guidance, lacking clear definition of the biliary anatomy, missing additional stones, or cannulating the cystic duct instead of the common duct [11, 15]. In our cases of difficult biliary cannulation, we performed TPS. When selective biliary cannulation is in doubt or is difficult, another technique is the placement of a short 5F stent into the selected duct [11]. In this technique, a stent-guided biliary sphincterotomy or an access papillotomy is performed according to bile or pancreatic fluid observed in the stent lumen. Precut sphincterotomy using a needle knife can also be performed for biliary cannulation [9, 11, 13]. A study on non-pregnant patients with inaccessible bile ducts found that TPS had a significantly higher rate of bile duct cannulation and a lower complication rate than needle-knife sphincterotomy [18]. More studies are needed to assess the efficacy and safety of the TPS technique in pregnant patients with difficult biliary cannulation during ERCP.
Before ERCP, MRCP is a valid and noninvasive option to document the ductal system and bile duct stones. In our study, MRCP was performed before ERCP in four patients who had an intermediate probability of choledocholithiasis based on clinical predictors and it documented choledocholithiasis in all. The diagnosis of choledocholithiasis was based on clinical predictors according to ASGE criteria [17] in the majority of our patients. Although the clinical findings suggested choledocholithiasis in these patients, no stone extraction was observed in four patients. One possibility was that the stones might have fallen spontaneously in these patients. Because ERCP is an invasive procedure associated with potentially serious complications, MRCP, which is noninvasive and avoids radiation exposure, should be considered before ERCP in all eligible patients, e.g., not critically ill ones [19]. When there is an uncertain need for an ERCP, an endosonography can be performed with a plan for a therapeutic ERCP [11]. A single-session endosonography-based ERCP without fluoroscopy has also been described [20].
To minimize cystic duct cannulation, optimal guidewire advancement was used as a guiding tool in our study. Clearly, this does not completely eliminate cystic duct cannulation. Ultrasonographic confirmation of biliary cannulation in pregnant patients during nonradiation ERCP has been described [13, 21]. Recently, contrast-enhanced US-guided ERCP for the treatment of choledocholithiasis during pregnancy was reported [22]. A study from China proposed that US-guided ERCP was preferred over conventional nonradiation ERCP because of the higher stone clearance and lower complication rates [13]. However, US-guided nonradiation ERCP needs additional professional staff, equipment, and training that restricts its wide application [19]. Intraductal US, rather than fluoroscopy, can be used to confirm the location of the guidewire within the CBD [23]; however, this equipment is not widely available.
The major concern in nonradiation ERCP is that residual stones or debris left in the CBD might lead to recurrent cholangitis with a more serious effect on both the fetus and the mother leading to a second unwarranted procedure [15]. The potential risk of recurrent cholangitis may outweigh the risk of the small exposure to fluoroscopy. An adequate sphincterotomy may allow residual stones (if any) to pass uneventfully; however, this is commonly true for stones with a diameter of less than 1 mm [15]. To minimize this risk, we modified the conventional technique. An EPBD was performed with a 6- or 8-mm dilation balloon according to CBD diameter to facilitate spontaneous passage of residual or additional stones or debris. All patients were successfully treated with our modified nonradiation ERCP technique with no further choledocholithiasis and/or cholangitis noted at the end of the 6-month follow-up. In questionable cases with an incomplete clearance of the common bile duct, an alternative option may be to place a bile duct stent; however, stent placement requires subsequent procedures and stent occlusion and migration can occur [9, 24]. In our study, a biliary stent was not placed in any case. A two- or three-stage ERCP has also been reported to achieve stone clearance after delivery. Sharma and Maharshi [9] treated 11 pregnant patients with choledocholithiasis by two-step ERCP, in which initial biliary sphincterotomy and stenting without radiation exposure was followed by definitive ERCP and stone clearance after the birth. Recently, Yang et al. [14] reported the use of ERCP and endoscopic nasobiliary drainage without fluoroscopy in 24 patients with severe acute biliary pancreatitis. In this study, 15 patients in late pregnancy underwent a second conventional ERCP with fluoroscopy to remove choledocholithiasis after birth. In nine patients in early or mid-pregnancy, three-stage ERCP was performed; after initial nonradiation ERCP with nasobiliary drainage, patients underwent a second ERCP without fluoroscopy for insertion of a stent to achieve biliary drainage, followed by a third ERCP with fluoroscopy 1 week after parturition to remove their stents and stones. However, two- or three-stage ERCP is a technically demanding procedure [19]. Peroral choledochoscopy is another potential option to confirm stone clearance in ERCP without fluoroscopy [11, 25]. In a study by Shelton et al. [11], stone clearance was confirmed by using peroral choledochoscopy (Spyglass Direct Visualization System, Microvasive) without complications in five of 21 patients. Choledochoscopy revealed that there were no retained stones or biliary abnormalities, but the cystic duct was cannulated in one patient. All mentioned techniques (endosonography-based ERCP, intraductal US, choledochoscopy, two- or three-stage ERCP) include technical and fiscal challenges, lengthen the procedure time, and may necessitate additional sedoanalgesia, which has a potentially harmful effect on the fetus.
The complication rate in our study was low and maternal/fetal outcomes were favorable. In the published literature regarding the use of nonradiation ERCP during pregnancy, 180 patients in 22 studies were reported [19]. The overall morbidity rate in these series was 15.6 % (28/180). The reported complications include incomplete stone clearance (n = 12), PEP (n = 2), hemorrhage (n = 4), stent occlusion (n = 4), stent migration (n = 2), cholangitis (n = 1), hyperamylasemia (n = 2), repeat ERCP for persistent fistula (n = 1), and biliary colic (n = 1) [19]. In the present study, two patients had post-ERCP epigastric pain and one patient had minor post-EST hemorrhage. Mild PEP was observed in two of the 22 patients (9 %), which was within the range of that observed in general populations (1.6–15.7 %) [26]. In three large series’ results (n > 10), the rate of PEP range was found to be from 0 to 4 % [9, 11, 13]. However, one of these studies [9], in which no PEP was reported, did not include any data regarding the definition of PEP. In the study of Shelton et al. [11], PEP was reported in one of 21 patients, which can be considered as similar to this study. A recent study from China [13] reported PEP in one of 68 patients (1.5 %). In comparison with our study, the lower rate of PEP might be because of the younger age of our patients (median age 26 vs. 29 years) and the fact that ERCP was carried out with US guidance in a group of their patients. In the largest series of fluoroscopy-guided ERCP during pregnancy (68 ERCPs on 65 pregnant patients), Tang et al. [5] reported a higher rate of PEP with a rate of 16 %. One might expect that EPBD could be a risk factor for PEP in our study. In two meta-analyses of prospective randomized controlled trials of EPBD versus EST, a higher rate of PEP was found in the EPBD group [27, 28]. In these studies, however, EPBD was performed without an EST. In contrast, we performed EPBD following a standard EST according to the CBD diameter. The mechanism of post-EPBD pancreatitis may be because balloon compression of the papilla or the pancreatic duct orifice may provoke peri-papillary edema or a sphincter of Oddi spasm [29, 30]. After a standard EST, the pancreatic orifice is separated from the biliary orifice and a sphincter of Oddi spasm is not expected. Accordingly, we believe that EPBD following a standard EST is not a major concern for PEP in nonradiation ERCP during pregnancy.
In conclusion, when performed by experienced endoscopists, nonradiation ERCP appears to be safe and effective for the treatment of symptomatic choledocholithiasis in pregnant patients. MRCP, which is a noninvasive imaging tool for the evaluation of pancreaticobiliary system, should be considered before ERCP in eligible pregnant patients. EPBD following a standard EST can reduce the risk of recurrent cholangitis because of residual or additional stones. While further research is needed on our new technique, this study has potential implications for future patient care of pregnant women with symptomatic choledocholithiasis.
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Disclosures
Drs. Galip Ersoz, Ilker Turan, Fatih Tekin, Omer Ozutemiz, and Oktay Tekesin have no conflicts of interest or financial ties to disclose.
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Ersoz, G., Turan, I., Tekin, F. et al. Nonradiation ERCP with endoscopic biliary sphincterotomy plus papillary balloon dilation for the treatment of choledocholithiasis during pregnancy. Surg Endosc 30, 222–228 (2016). https://doi.org/10.1007/s00464-015-4190-1
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DOI: https://doi.org/10.1007/s00464-015-4190-1