The British Journal of Radiology, 82 (2009), 279 285 The role of MR cholangiopancreatography in the evaluation of pregnant patients with acute pancreaticobiliary disease 1,2 AOTO,MD, 1,3 RERNST,MD, 4 L GHULMIYYAH, MD, 1 DHUGHES,MD, 4 G SAADE, MD and 1 G CHALJUB, MD 1 Department of Radiology, University Texas Medical Branch at Galveston, Galveston, Texas 77555, 2 Department of Radiology, The University of Chicago, Chicago, Illinois 60637, 3 MD Anderson Cancer Center, Houston, Texas 77030, and 4 Department of Obstetrics and Gynecology, University Texas Medical Branch at Galveston, Galveston, Texas 77555, USA ABSTRACT. This study aimed to determine the usefulness of MR cholangiopancreatography (MRCP) in the evaluation of pregnant patients with acute pancreaticobiliary disease and its additional value over ultrasound. MRI studies of pregnant patients who were referred because of acute pancreaticobiliary disease were included. MR images and patient charts were reviewed retrospectively to determine clinical outcome and the results of other imaging studies. 18 pregnant patients underwent MRCP because of right upper quadrant pain (n56), pancreatitis (n59), cholangitis (n51) or jaundice (n52). 15 patients were also evaluated with ultrasound. Biliary dilatation was detected in eight patients by ultrasound, but the cause of biliary dilatation could not be determined by ultrasound in seven patients. MRCP demonstrated the aetiology in four of these patients (choledocholithiasis (n51), Mirizzi syndrome (n51), choledochal cyst (n51) and intrahepatic biliary stones (n51)) and excluded obstructive pathology in the other four patients. MRCP was unremarkable in the seven patients who had no biliary dilatation on ultrasound. Three patients underwent only MRCP; two had choledocholithiasis and one cholelithiasis and pancreatitis. Choledocholithiasis diagnosed with MRCP (n53) was confirmed by endoscopic retrograde cholangiopancreatography. Mirizzi syndrome (n51) and a choledochal cyst (n51) were confirmed by surgery. The patients with normal MRCP (n512) and one patient with intrahepatic stones improved with medical treatment. MRCP appears to be a valuable and safe technique for the evaluation of pregnant patients with acute pancreaticobiliary disease. Especially when ultrasound shows biliary dilatation, MRCP can determine the aetiology and save the patient from unnecessary endoscopic retrograde cholangiopancreatography by excluding a biliary pathology. Received 4 March 2008 Revised 3 April 2008 Accepted 18 April 2008 DOI: 10.1259/bjr/88591536 2009 The British Institute of Radiology Biliary disease is the second most common gastrointestinal disorder requiring surgery during pregnancy [1, 2]. For the majority of patients, management consists of a conservative non-surgical approach followed by more definitive surgical treatment after delivery. Nonetheless, it is important to recognise the subset of patients who may need surgical or endoscopic intervention early during the course because delay in the diagnosis could lead to maternal and foetal morbidity [2]. Clinical diagnosis of biliary disease during pregnancy can be difficult. The symptoms of biliary tract disease, which include anorexia, nausea, vomiting and abdominal pain, are non-specific and can be encountered during a normal pregnancy. Physiologically, pregnant patients may have an elevated white blood cell count, elevated serum amylase and elevated alkaline phosphatase of placental origin [3]. A rapid, reliable and accurate imaging method is therefore needed for evaluation of the entire biliary system in pregnant patients suspected of having acute pancreaticobiliary disease. Address correspondence to: Dr Aytekin Oto, Department of Radiology, The University of Chicago, 5841 South Maryland Avenue, MC 2026, Chicago, IL 60637, USA. E-mail: aoto@radiology.bsd.uchicago.edu Ultrasound is the imaging tool of choice for evaluation of the biliary system and is accurate in diagnosing cholelithiasis in 97% of cases [2]. Its accuracy, however, is limited in the evaluation of the common bile duct and the pancreas [4]. MR cholangiopancreatography (MRCP) is already established as clinically useful and comparable with endoscopic retrograde cholangiopancreatography (ERCP) for the evaluation of various biliary and pancreatic ductal diseases [5]. Although several reports have recently demonstrated the success of MR imaging in the evaluation of acute abdominal pain and appendicitis in pregnant patients, to our knowledge, the role of MRCP in pregnant patients has not been investigated previously [6 9]. Our purpose in this study was to determine the usefulness of MRCP in the evaluation of pregnant patients who have acute pancreaticobiliary disease and to investigate its additional value over ultrasound. Methods and materials Patients Medical records at our institution were reviewed from May 2002 to April 2007 to identify all pregnant patients The British Journal of Radiology, April 2009 279
A Oto, R Ernst, L Ghulmiyyah et al who had undergone MRCP for acute pancreaticobiliary disease. The causes of this disease included obstructive jaundice, right upper quadrant pain, acute pancreatitis and cholangitis. We retrospectively reviewed the medical records and MR images of 18 pregnant women (age range, 15 33 years; mean age, 24.5 years) who met the above inclusion criteria. The mean gestational age was 18.6 weeks (range, 6 36 weeks). Informed consent was obtained from all patients before the MR examination, in accordance with institutional policy. Neither sedation nor anaesthesia was used during the examinations. Approval from the institutional review board was obtained. The institutional review board waived the informed consent requirement for retrospective study of patient records and images. MR imaging MR imaging was performed with a 1.5-T superconducting system (Signa; GE Medical Systems, Milwaukee, WI), with a phased-array coil placed over the abdomen. For some third-trimester patients, the body coil was utilised. The MRCP protocol included transverse and coronal T 2 weighted single-shot fast spin-echo (SE) imaging (repetition time (ms)/echo time (ms) (TR/ TE), /80; matrix, 256 6 256; bandwidth, 31.25 khz; section thickness, 6 mm; section gap, 2 mm); transverse fat-suppressed fast SE T 2 weighted imaging (TR/TE, 2500 3200/90 ms; two signals acquired; echo train length, 17; matrix, 192 6 256; bandwidth, 20.83 khz; section thickness, 7 mm; section gap, 1 mm); transverse in and out of phase T 1 weighted gradient recalled echo (GRE) sequences (TR range/first-echo TE range, secondecho TE range, 80 200/4.2 4.6 ms, 2.1 2.3 ms; bandwidth, 31.25 62.5 khz; one signal acquired; section thickness, 5 7 mm; gap, 0 mm; matrix, 256 6 160 192; and flip angle, 75 90 ); transverse three-dimensional (3- D) GRE fat-suppressed T 1 weighted images (TR, 7 ms; TE, minimum; flip angle, 12; 1 signal acquired; matrix, 192 6 256; bandwidth, 31.25 Hz/pixel; slice thickness, 5 mm with 2.5 mm overlap); coronal 3-D T 2 weighted fast SE MRCP sequence (TR/TE 3750/650 ms; bandwidth 31.25 62.5 khz; section thickness, 1.8 mm, reconstructed at 0.9 mm; matrix, 256 6 128 192); coronal thick-slab T 2 weighted fast MRCP sequence (TR/TE, 2500/900; slab thickness, 30 40 mm; bandwidth, 31.25 62.5 khz; matrix, 256 6 320). Single-shot fast SE sequences, T 1 weighted GRE sequences and thick-slab MRCP sequences were performed during sustained respiration at the end of expiration. All other sequences were performed during quiet respiration. The region of interest extended from the level of the diaphragm to the inferior pole of the kidneys. The field of view varied from 25 to 40 cm. Intravenous contrast was not administered to any patient. Image interpretation Two radiologists who were blinded to the information in the patient charts and to previous imaging results reviewed the MRI together in consensus. Both of these radiologists had subspecialty training in abdominal imaging, and more than 8 years of experience in abdominal MRI. Analysis of imaging findings included evaluation of the intrahepatic biliary tree, common bile duct, gallbladder, pancreas and pancreatic duct, and assessment of the presence of focal fluid collections or focal inflammation and any other abnormal finding in the abdomen. The common bile duct was considered normal if its maximum outer diameter measured less than 7 mm and there was no filling defect within the duct. Thin-slice coronal MRCP images were reviewed for detection of small filling defects within the entire biliary system and pancreatic duct. Round, hypointense foci within the biliary tree on thin-slice MRCP images were accepted as stones. If biliary dilatation was present, the location of the obstruction and its aetiology were specifically sought and noted. The size and signal intensity of the pancreas were evaluated on fat-suppressed T 1 weighted images. A focally or diffusely oedematous pancreas, peripancreatic increased signal on T 2 weighted images or streaky signals extending from the pancreas to the peripancreatic fat were accepted as MR signs of acute pancreatitis. On T 2 weighted sequences, fluid collections in the abdomen were specifically sought for detection of pseudocysts. The size, content and wall thickness of the gallbladder were evaluated on T 2 weighted images. A focally increased signal around the gallbladder was accepted as pericholecystic fluid or inflammation. Patients who had a distended gallbladder with wall thickening and pericholecystic fluid were accepted as having acute cholecystitis. Clinical information The medical records of 18 patients were reviewed for clinical progress, beginning at admission for acute pancreaticobiliary disease; for reports of right upper quadrant ultrasound studies; for type of treatment (e.g. medical, surgical or interventional); for diagnosis at discharge; for possible re-admission to the hospital within 1 month of discharge with recurrent symptoms; and for surgical and pathology findings (if applicable). MR findings were compared with information obtained from the clinical records of the patients. Results 18 pregnant patients underwent MRCP because of clinical indications of acute pancreatitis (n59), right upper quadrant pain (n56), obstructive jaundice (n52) or cholangitis (n51). Ultrasound findings Ultrasound was performed in 15 of these patients prior to MRCP. This showed biliary dilatation in eight patients, of whom seven had intrahepatic and common bile duct dilatation and one had only intrahepatic biliary dilatation. Ultrasound findings were consistent with a 280 The British Journal of Radiology, April 2009
The role of MRCP in pregnant patients with acute biliary disease choledochal cyst in one of the patients who had biliary dilatation but the aetiology of the biliary dilatation could not be determined in the other seven patients. Six of the seven patients with common bile duct dilatation had cholelithiasis, and two of them had sonographic findings consistent with both cholelithiasis and acute cholecystitis (gallbladder wall thickening, pericholecystic fluid and a positive sonographic Murphy sign). The patient with isolated intrahepatic biliary dilatation had a history of common bile duct cyst excision as well as hepaticojejunostomy and cholecystectomy. Ultrasound did not show any biliary dilatation in seven patients. Four of these patients had sludge in their gallbladder, two had cholelithiasis and one had a small gallbladder polyp without gallstones or sludge. None of these patients had sonographic findings of acute cholecystitis. The pancreas could not be completely imaged and evaluated by ultrasound in any of the 15 patients. The pancreatic head and body could be visualised partially in nine patients in whom they were unremarkable. MRCP findings MRCP demonstrated the aetiology of biliary dilatation in four of the eight patients who had been found to have biliary dilatation on ultrasound. One of these patients had a filling defect in her common bile duct consistent with choledocholithiasis (Figure 1). In another patient, the common bile duct was proximally dilated up to the point where the common hepatic duct was compressed by the distended and thick-walled gallbladder, which contained gallstones (Figure 2). No stones were seen in the common bile duct. These findings were accepted as indicating acute cholecystitis that caused Mirizzi syndrome. In the patient who had isolated intrahepatic biliary dilatation, MRCP showed intrahepatic biliary stones in the left hepatic duct but a patent hepaticojejunal anastomosis (Figure 3). MRCP findings were in agreement with ultrasound for the diagnosis of a choledochal cyst (Figure 4). No filling defects were seen in the common bile duct in the other four patients. The proximal common bile duct was mildly dilated in three of these patients (measuring 7 mm), but the distal common bile duct tapered normally without evidence of choledocholithiasis or stricture. Another patient who had sonographic findings of acute cholecystitis also had MR findings of acute cholecystitis. Gallstones were identified in the six patients in whom ultrasound also showed cholelithiasis. MRCP did not demonstrate any pathology in the common bile duct or intrahepatic biliary tree of the seven patients who had no biliary dilatation on ultrasound. Filling defects were present in the gallbladder of six of these patients, compatible with the sludge or gallstones noted on ultrasound. None of these patients had MR evidence of acute cholecystitis. Three patients underwent only MRCP. Two of these patients had cholelithiasis and choledocholithiasis causing biliary dilatation; neither showed MR evidence of acute cholecystitis. The third patient had cholelithiasis and an oedematous pancreas with peripancreatic inflammation consistent with acute pancreatitis. There was no Figure 1. 28-year-old female at 22 weeks gestation, who had obstructive jaundice. (a) Axial T 2 weighted fat-suppressed fast spin-echo image shows a punctate filling defect (arrow) within the dilated common bile duct, consistent with choledocholithiasis. (b) Thick-slab oblique MR cholangiopancreatography image reveals multiple stones (arrowheads) in the dilated common bile duct. The intrauterine pregnancy (arrow) is partially imaged. Stones were extracted with endoscopic retrograde cholangiopancreatography and by sphincterotomy. MR finding of acute cholecystitis in this patient and no pseudocysts were detected on MRCP. The pancreas was unremarkable on MRCP in the remaining 17 patients. The British Journal of Radiology, April 2009 281
A Oto, R Ernst, L Ghulmiyyah et al treated medically with antibiotics. The patient s symptoms improved and she was discharged without surgical or endoscopic treatment. The second patient who had sonographic and MR findings of acute cholecystitis had undergone a cholecystectomy and acute cholecystitis was confirmed. No intraoperative cholangiography was performed. Twelve patients who did not have biliary dilatation on MRCP (including the patient with acute pancreatitis) improved clinically with medical treatment and were discharged without undergoing ERCP or surgery. Figure 2. 27-year-old female at 36 weeks gestation who had obstructive jaundice and right upper quadrant pain. (a) Coronal T 2 weighted single-shot fast spin-echo image shows distended gallbladder with cholelithiasis (arrow) and intrahepatic biliary dilatation (arrowheads). (b) Thin-slice MR cholangiopancreatography (MRCP) images showed that the distal common bile duct is normal in calibre and the common hepatic duct was compressed by the inflamed and distended gallbladder. Maximum intensity projection reconstruction of thin-slice MRCP images demonstrates the distended gallbladder fundus compressing the proximal common bile duct (arrow), causing intrahepatic biliary dilatation and a normalcalibre distal common bile duct (arrowheads), consistent with Mirizzi syndrome. The patient underwent cholecystectomy and these findings were confirmed on surgery. Clinical outcome and correlation Choledocholithiasis diagnosed with MRCP was confirmed by ERCP in all three cases. Sphincterotomy and stone extraction were performed and the jaundice was relieved. The patient who was diagnosed as having Mirizzi syndrome underwent surgery and the patient s jaundice improved after cholecystectomy without endoscopic sphincterectomy or exploration of the common bile duct. Intraoperative cholangiography was not performed. The patient with a choledochal cyst had the cyst drained percutaneously during pregnancy and resection of the choledochal cyst was performed after delivery. The patient with intrahepatic biliary stones was Discussion Hormonal effects predispose pregnant patients to gallstone formation and increase the incidence of biliary disease [10, 11]. Oestrogen increases cholesterol synthesis and leads to increased bile volume and lithogenicity. Progesterone induces cholestasis by relaxing the smooth muscles and thus impairing gallbladder and bowel motility [10, 11]. Gallbladder sludge has been identified in 25% of women immediately post partum and symptomatic cholelithiasis is reported to be increasingly common in pregnancy [12, 13]. Ultrasound is an excellent technique for evaluation of the gallbladder. It has no known harmful effects on the foetus and has traditionally been the initial imaging modality of choice for evaluation of suspected biliary pathology in pregnant patients. However, the sensitivity of ultrasound in the detection of common bile duct stones has been reported at only between 20% and 38% [4, 14]. In addition, ultrasound is highly operator dependent, and factors such as intervening bowel gas, the gravid uterus and obesity may interfere with the quality and adequacy of the examination. Even experienced sonographers can have difficulty in evaluating the distal common bile duct and the entire pancreas. CT scanning is another non-invasive method for evaluation of the biliary tree and pancreas, but its accuracy is limited by its low sensitivity in the diagnosis of common bile duct stones [4]. CT is also of limited use in obstetric patients because of concerns about radiationinduced teratogenesis [15]. ERCP is an effective treatment method for common bile duct stones but is performed under fluoroscopic guidance. Although there are some technical modifications that can limit foetal exposure, such as shielding of uterus and minimising fluoroscopy time, it will be best to restrict the utilisation of this technique to therapeutic indications during pregnancy [16]. ERCP is also associated with morbidity related to pancreatitis, sepsis, perforation and haemorrhage [16]. The American College of Obstetricians and Gynecologists recommends that imaging methods not associated with ionising radiation should be considered whenever possible [17]. MR imaging has no known deleterious effects on the foetus, and the Society of Magnetic Resonance Imaging has recommended the use of MR imaging for pregnant women when other nonionising forms of diagnostic imaging are inadequate and when the examination provides important information that would otherwise require exposure to ionising radiation [18]. 282 The British Journal of Radiology, April 2009
The role of MRCP in pregnant patients with acute biliary disease Figure 3. 22-year-old female at 17 weeks gestation. The patient had a history of choledochal cyst excision during her infancy and had possible cholangitis. (a) Axial T 2 weighted fast spin-echo image and (b) coronal T 2 weighted single-shot fast spin-echo image show round filling defects (arrows) within the dilated intrahepatic biliary tree in the left lobe, consistent with intrahepatic biliary stones. (c) Thin-slice MR cholangiopancreatography sequence confirms the patency of anastomosis (arrow) and normal-sized right and left hepatic ducts closer to the anastomosis. This patient was treated with antibiotics and discharged without any need for intervention or surgery. MRCP emerged during the 1990s as a non-invasive imaging method. Today, it is an established but stillevolving technique for imaging in cases of biliary and pancreatic disease [5, 19]. Recent refinements in the technique and the development of 3-D MRCP sequences further improved MRCP, allowing the reconstruction of overlapping slices of less than 1 mm [20, 21]. With a reported accuracy close to 100% in determining the presence and level of biliary obstruction, MRCP has replaced diagnostic ERCP in many institutions and the utilisation of ERCP for diagnostic purposes steadily decreased from 1996 to 2002 [22, 23]. The results for our series of patients indicated that there are several advantages to using MRCP in the evaluation of pregnant patients who have suspected biliary disease. First, MRCP excluded choledocholithiasis and other common forms of bile duct pathology in four of the eight patients who were found to have biliary dilatation of unknown aetiology on ultrasound. These patients improved with supportive treatment and were discharged without surgical or endoscopic intervention. Therefore, MRCP saved the foetuses in these patients from unnecessary risk of exposure to ionising radiation. MRCP confirmed the normal bile duct findings on ultrasound in seven other patients, again precluding further work-up with methods that are more invasive or require ionising radiation. Second, MRCP was able to demonstrate the correct cause of biliary dilatation in six patients, leading to the identification of a subset of patients who required immediate treatment. The ability of MRCP to provide an accurate evaluation of the entire biliary system allowed the detection of some rare and complex pathologies, such as intrahepatic biliary stones, Mirizzi syndrome and choledochal cyst. MRCP enabled a fast, reliable and accurate diagnosis and these patients were not investigated further with invasive, ionising radiation-requiring tests such as ERCP during their pregnancy. MRCP also obviated the need for intraoperative cholangiography in two pregnant patients who had undergone cholecystectomy. The third advantage of MRCP was its ability to evaluate the entire pancreas and abdomen for acute pancreatitis and fluid collections. The diagnosis of acute pancreatitis can be complicated during pregnancy because of mild physiological elevation of amylase, and MRCP may be helpful especially in the detection of complications of acute pancreatitis [24, 25]. Ultrasound is limited in imaging of the pancreas, and this limitation is particularly prominent when the gravid uterus displaces the abdominal organs superiorly. In our series, the pancreas could not be completely visualised by ultrasound in any of the patients. On the other hand, in our series, MRCP did not provide additional information when ultrasound did not show any biliary dilatation. Limitations Our study was limited by its retrospective design, leading to a lack of reference standard and selection bias as not all of the pregnant patients with suspected pancreaticobiliary disease had undergone MRCP. Owing to the retrospective design of the study, we are not sure whether these patients were consecutive pregnant patients presenting with acute biliary pain. A second limitation is the lack of follow-up data after the discharge of patients who recovered spontaneously or after medical treatment. We reviewed their medical records only for a possible re-admission in the 1-month period following their discharge. We cannot exclude the possibility that these patients visited other medical facilities following their discharge, neither can we exclude spontaneous resolution of a pathological condition in the common bile duct, such as a small stone, in patients who had negative MRCP studies. Another limitation is our inability to determine the exact cause of clinical symptoms in patients who improved following medical or supportive treatment. In conclusion, MRCP provides a systematic and accurate evaluation of the entire biliary system and allows the diagnosis of various diseases that cause acute pancreaticobiliary disease in pregnant patients. MRCP can help in the identification of a subset of patients who require immediate intervention, and it can save the patients from unnecessary ERCP by excluding a biliary The British Journal of Radiology, April 2009 283
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