© 2013, Hepatobiliary Pancreat Dis Int. All rights reserved.

doi: 10.1016/S1499-3872(13)60100-9

 

 

Contributors: BE and RJM proposed the study. RL and YT performed research and wrote the first draft. CC and DR collected and analyzed the data. All authors contributed to the design and interpretation of the study and to further drafts. RJM is the guarantor.

Funding: None.

Ethical approval: Not needed.

Competing interest: No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.

 

 

BACKGROUND: The Frey procedure (FP) is the treatment of choice for symptomatic chronic pancreatitis (CP). In cases of biliary stricture, biliary derivation can be performed by choledochoduodenostomy, Roux-en-Y choledochojejunostomy or, more recently, reinsertion of the common bile duct (CBD) into the resection cavity. The objective of the present study was to evaluate the outcomes associated with each of these three types of biliary derivation.

 

 

 

 

(Hepatobiliary Pancreat Dis Int 2013;12:637-644)

 

KEY WORDS: common bile duct stricture; chronic pancreatitis; Frey procedure; pancreatectomy

Biliary obstruction in chronic pancreatitis (CP) may have several etiologies (pseudocysts, cancer, etc.) but is most often due to fibrosis.^[1] This obstruction may manifest itself through clinical signs (jaundice and cholangitis) and/or biochemical signs (elevated serum bilirubin and alkaline phosphatase levels) and increases the risk of developing biliary cirrhosis in the longer term.^[2] When faced with a symptomatic biliary stricture in CP, the physician will typically first administer endoscopic treatment. In fact, this dogma is now being challenged by the good results obtained with surgery, with low complication and recurrence rates. Indeed, endoscopic treatment is associated with a higher rate of recurrences requiring prosthesis implantation.^{[3, 4]}

 

As part of the surgical management of CP, the Frey procedure (FP) has become the procedure of choice over other duodenum-preserving pancreatic head resection (DPPHR) procedures (such as the Beger or Izbicki procedures) because of its relative ease^{[5, 6]} and its significantly lower morbidity and mortality rates when compared with non-preserving procedures (such as pylorus-preserving pancreaticoduodenectomy, as known as Whipple resection).^{[7, 8]}

 

In cases of CP with an inflammatory pancreatic head mass and biochemical and morphologic signs of biliary stricture for over three months, FP is indicated (once pseudocyst compression and acute pancreatitis have been ruled out).^[9] However, if local resection of the pancreatic head fails to restore bile flow after cholangiography, intraoperative decisions concerning the biliary tract will depend on individual findings. In this situation, biliary derivation must be performed via Roux-en-Y choledochojejunostomy (CJ), choledochoduodenostomy (CD) or, more recently, reinsertion of the common bile duct (CBD) into the resection cavity.^{[10, 11]} The latter can be performed in its own right or in the event of incidental damage to the CBD during pancreatic head resection. The objective of the present study was to describe the outcomes after FP with biliary derivation, with a focus on the recurrence rate of stricture.

 

 

We performed a retrospective analysis of our prospective data on patients having undergone FP as part of surgical biliary derivation between January 2004 and December 2012. All procedures were performed by the same pancreatic surgeon (RJM).

 

Patients included in the study had to meet all of the following inclusion criteria: symptomatic CP, radiologically confirmed CBD stricture with clinical and/or biological signs of obstruction and FP combined with biliary derivation. Patients not having undergone FP combined with biliary derivation or those suffering from pancreatic cancer, cirrhosis, primary sclerosing cholangitis, postsurgical stricture, secondary stenosis caused by gallstones or pseudocysts were excluded from the study.

 

The diagnosis of CP was based on one or more of the following criteria: (i) at least moderate duct anomalies (according to the Cambridge classification);^[12] (ii) the presence of pancreatic calcification; and (iii) fibrosis in histological specimens.^[13]

 

Stricture was defined as a narrowing of the CBD with prestenosis dilatation or delayed run-off of contrast during magnetic resonance imaging, computed tomography or endoscopic retrograde cholangiopancreato­graphy. The clinical criteria for obstruction were jaundice and/or cholangitis. Cholestasis was defined as a serum total bilirubin level ≥1.3 mg/dL (normative value for our laboratory: 0.2-1.3 mg/dL) or a serum alkaline phosphatase level ≥126 U/L (normative value: 38-126 U/L). An inflammatory pancreatic head mass was defined as a head diameter ≥4 cm.^[3]

 

In patients with CP, the indication for surgery was discussed and validated in a multidisciplinary staff meeting comprising specialist surgeons, radiologists and a gastroenterologist. Surgical treatment of symptomatic CP with an inflammatory pancreatic head mass consisted of FP as the DPPHR procedure.^{[14, 15]} In cases of persistent biliary stricture after FP, we performed a biliary bypass (via CJ or CD) or reinsertion of the CBD into the resection cavity^[10] (Fig. 1).

 

After surgery, patients were followed up for at least 12 months in the outpatient clinic, with regular clinical examinations and laboratory tests. Follow-up information was obtained from hospital charts. We specifically looked for signs of stricture recurrence, including clinical symptoms of obstruction (jaundice or cholangitis), cholestasis (abnormally high total serum bilirubin or alkaline phosphatase values) and radiologic evidence of a CBD stricture. In the event of recurrent CBD stricture, revisional surgery was performed after endoscopically and/or radiologically-guided biliary drainage.

 

The study's primary efficacy endpoint was the postoperative stricture rate. The secondary endpoints were surgical parameters, complications (according to the Clavien classification),^[16] follow-up data and risk factors for secondary strictures.

 

The recorded study parameters included: (1) pre-operative data: age, gender, body mass index (BMI), percentage weight loss, diabetes mellitus status (with the proportion of patients on insulin therapy), pre-operative exocrine pancreatic insufficiency, and chronic abdominal pain (with the proportion of patients on morphine therapy); (2) data related to CP: etiology, time since onset, past endoscopic procedures, and preoperative imaging data; (3) surgical data: the types of DPPHR procedures performed, operating time, other associated surgical procedures, and blood loss; (4) follow-up data: mean follow-up time, postoperative complications (according to the Clavien classification), revisional surgery, stricture recurrence and management, diabetes mellitus status (with the proportion of patients on insulin therapy), chronic abdominal pain (with the proportion of patients on morphine therapy) and exocrine pancreatic insufficiency.

 

Pancreatic fistula was defined and graded (A, B or C) according to the International Study Group of Pancreatic Fistula (ISGPF) criteria.^[17]

 

The statistical analysis was performed with SAS software (version 4.3, SAS Institute Inc., Cary, NC, USA) using tests intended for small sample sizes. Associations between categorical variables were assessed using the Chi-square test. The results are presented as the median (range) or a percentage (n). Quantitative variables were compared in an analysis of variance. In two-tailed tests, the threshold for statistically significance was set to P<0.05.

 

 

A total of 80 patients with CP underwent surgical procedures during the study period. Fifteen of them [12 men (80.0%); median age: 51 years (32-71); median BMI: 19.8 (14.7-29.4); median weight loss: 9 kg (0-20); median percentage weight loss: 15.3% (0-35.2%)] underwent FP associated with biliary derivation (Fig. 2). Type 2 diabetes mellitus was present in 7 patients (46.7%), of whom 3 were receiving insulin therapy. Active smoking was recorded in 13 patients (86.7%). Preoperative exocrine pancreatic insufficiency was present in 6 patients (40.0%). All 15 patients had chronic abdominal pain and 4 were receiving morphine therapy (Table 1).

 

The etiology of CP was alcohol-related in all cases. The median time since onset of CP was 6.3 years (1-20). Preoperative abdominal CT scans showed pancreatic calcifications and CBD stricture in all cases. An inflammatory pancreatic head mass was observed in 86.7% of the patients (n=13). We also observed portal hypertension (1), duodenal stenosis (1), pancreatic pseudocysts with no repercussion on CBD stricture (6), and pancreatic duct stricture (10). Preoperative endoscopic treatment was performed in 9 patients (60.0%) with a median number of endoscopic procedures of 2 (0-5) for a total of 7 biliary prostheses and 4 pancreatic prostheses (Table 1).

 

The median serum total bilirubin level was 13 mg/dL (4-372) and the median serum alkaline phosphatase level was 302 U/L (152-1210). All patients had a CBD diameter ≥10 mm. Twelve patients (80.0%) had a short CBD stenosis (≤2 cm), whereas the three others had a long CBD stenosis (20.0%).

 

The FP was performed in all patients. Biliary derivation was performed via CD (8, 53.3%), CJ (4, 26.7%) and CBD reinsertion into the resection cavity (3, 20.0%). The CBD was performed prospectively in two cases and as a result of accidental injury to the CBD in the third case. Cholecystectomy was performed in all patients during the same surgical session. The median operating time was 387 minutes (320-590) and the median blood loss was 325 mL (100-1300) (Table 1).

 

In our period study, we first performed CD for our first patients (n=8) then we performed Roux-en-Y CJ for 4 patients and finally we performed reinsertion of the CBD into the resection cavity for the last three patients.

 

No postoperative deaths were observed. We recorded 11 postoperative complications in 11 patients (73.3%). The median length of hospital stay was 17 days (8-28). There was one major complication (Clavien ≥3): an abdominal collection necessitating radiologically-guided drainage. The remaining (minor) complications included three pancreatic fistulas (grade A), three lung infections, two chylous ascites and two scar infections. No bile leakage occurred. There was no significant difference between the three biliary derivation procedures (CD, CJ and CBD reinsertion) in terms of the frequency of major and minor postoperative complications (P=0.25) (Table 2).

 

The median follow-up time was 35.2 months (7.2-95.4). Sixty percent of the patients suffered from postoperative diabetes mellitus (n=9) and 55.6% of the latter were receiving insulin therapy (n=5). Postoperative exocrine pancreatic insufficiency was present in 73.3% (n=11) of the patients. All fifteen patients were free of chronic abdominal pain. Two of the patients having undergone an FP with CBD reinsertion into the resection cavity experienced recurrence of CBD stricture 29 and 7 months after surgery, respectively (Table 2). The third patient having undergone an FP and CBD reinsertion was stricture-free for 18 months after surgery. Of the 8 patients having undergone an FP with CD, three (37.5%) presented alkaline reflux gastritis, one (12.5%) presented cholangitis in the absence of CBD stricture (treated with antibiotics), and one (12.5%) experienced recurrence of CBD stricture 31 months after CD. Univariate analyses did not reveal any risk factors for secondary CBD stricture (P>0.05). Also, logistic regression analysis of our population was performed without significant results.

 

Patient 1: Twenty-nine months after surgery, the patient was admitted for cholangitis. Endoscopic treatment was performed because the patient refused revisional surgery. During the endoscopic procedure, the failure of papillary cannulation prompted us to perform percutaneous transhepatic biliary puncture to dilate an internal biliary stricture (Fig. 3). The outcome was favorable and the patient was stricture-free for 18 months after the dilatation procedure.

 

Patient 2: Seven months after primary surgery, the patient presented with recurrence of CBD stricture (in the absence of cholangitis) with jaundice and elevated serum total bilirubin level. The procedure described above for patient 1 was also performed in patient 2 but failed. An external biliary drain was left in place until revisional surgery was performed 7 days later (a biliary diversion with Roux-en-Y CJ) (Fig. 4). The external biliary drain was left in place for a further five days, in order to guide the biliary anastomosis. The outcome was favorable: 4 months after revisional surgery, the patient's clinical and biochemical status was normal.

 

Patient 3: Thirty-one months after biliary diversion via CD anastomosis, the patient presented jaundice and an elevated serum total bilirubin level (in the absence of cholangitis). Endoscopy revealed a CBD stricture with biliary dilatation. Installation of a coated biliary stent led to resolution of the jaundice and normalization of the serum total bilirubin level (Fig. 5). The stent was removed four weeks later. There has been no recurrence of the stricture in the eight months since removal.

 

 

DPPHR is the gold standard for the treatment of CP and has a lower morbidity and mortality rate than pancreatico­duodenectomy.^[18] In a series of 514 DPPHRs (with or without CBD reinsertion), Cataldegirmen et al^[9] showed that patients operated with this technique gained greater postoperative weight compared with those who underwent pancreaticoduodenectomy. This weight gain can be blamed on the preservation of the duodenum tract. DPPHR is associated with an acceptable morbidity rate. It relieves chronic abdominal pain and enables morphine therapy to be withdrawn in the majority of cases.^[19] Indeed, the long-term follow-up in our series showed a nil morphine therapy rate. Furthermore, the recurrence rate requiring revisional surgery is quite low, with a value of 3% reported by Riediger et al.^[20] Hence, our surgical team tends to perform first-line DPPHR in view of its efficacy and low rate of recurrence (when compared with prosthetic treatment).^[3]

 

The FP is performed frequently because it is technically easier than the Beger procedure, which requires release of the mesenteric-portal axis; this can be complicated when CP has caused local inflammation.^[5] According to the series reported by Pessaux et al,^[8] the FP is associated with good outcomes in terms of chronic abdominal pain (with complete pain relief in 56% of cases, substantial pain relief in 32% and no use of narcotic analgesics over a mean follow-up period of 15 months). Furthermore, the FP is associated with a relatively short length of hospital stay (from 14 to 17 days in the literature^{[8, 19]} and 17 days in our present series).

 

In cases of CBD stricture associated with CP, surgery yields better results than endoscopy, with a lower recurrence rate and a higher success rate at 2 years (65% for surgery versus 12% for endoscopy).^[3] The choice between endoscopic and surgical therapy as treatment of CBD strictures related to CP should rely on local expertise, patient co-morbidities and expected patient compliance with repeat endoscopic procedures.^[21] Also, Chaudhary et al^[22] reported more complications (infections) with a longer hospital stay for patients undergoing first-line endoscopy before surgery. In other series,^[23-25] long-term success ranged from 10% to 28% when surgery was performed in 27.5% to 53% of cases (Table 3). However, a recent series^[26] showed good results because of the placement of covered self-expanding metal stents. This type of endoscopic procedures is very optimistic in case of biliary strictures related to CP with a higher success rate compared to plastic stent.^[27] Catalano et al^[28] reported that multiple metal stents (4 or 5 stents) can be used with good long-term results in 92% of cases over a mean treatment period of 14 months. The placement of multiple metal stents provides long-term dilation compared to the use of single stent with improvement of the mean diameter of the strictures in the multiple stent group, with 1.2 mm before treatment to 2.5 mm after procedure. In this series, an aggressive endoscopic protocol could be an alternative to surgical procedures. Finally, decision between first-line endoscopy and surgery must be based according to the experience of endoscopists and surgeons, and each case of CP with CBD stricture must be discussed at a multidisciplinary staff meeting as in our series.

 

There are three possible surgical treatments: CD, Roux-en-Y CJ and CBD reinsertion into the resection cavity.^[10] The more recent introduction of the latter technique means that it has not been as extensively studied as the other biliary bypass procedures.^{[29, 30]} Surgery for CBD stricture using different techniques^[31,32] is associated with a low rate of major complications and good results concerning long-term success (Table 4). In the present series, we used all three different types of biliary derivation. CD was performed in the first eight cases in our series but was then abandoned because of the late appearance of alkaline reflux gastritis in three patients (37.5%). This condition was highly disabling, as in the series described by Mihmanli et al.^[33] Another patient in the CD group presented cholangitis (in the absence of CBD stricture) and was treated with antibiotics. According to Malik et al's report,^[34] this type of long-term, post-CD complication has an incidence of between 3.8% and 6.8%. For these reasons, we replaced CD by Roux-en-Y CJ and CBD reinsertion into the resection cavity.

 

Two of the patients in the present series (both of whom had undergone CBD reinsertion into the resection cavity) presented recurrence of the CBD stricture. This is a rare complication that has only been described by Cataldegirmen et al^[9] as a secondary CBD stricture found in 18% (n=15) of 82 patients. The recurrence rate was 2.3% after DPPHR procedures and 4% after pancreaticoduodenectomy. We suggest that stricture recurrence may be due to the occurrence of ischemia of the distal CBD during pancreatic head resection or failure to remove enough inflamed pancreatic tissue. In our series, there was no difference in recurrence rate between three types of biliary anastomosis despite performing univariate, multivariate and logistic regression analysis due to the low effectiveness of our study.

 

As part of the treatment of CBD stricture after DPPHR with CBD reinsertion in the series described by Cataldegirmen et al,^[9] transhepatic dilatation was attempted but failed in all cases and required revisional procedures (pancreatic head excision with repeat reinsertion of the distal CBD or bilio-enteric anastomosis, depending on the presence or absence of pain and the size of the pancreatic head). In our series, the two recurrences of the CBD stricture were pain-free. Interestingly, we were able to relieve one of the strictures by transhepatic dilatation. The patient was still stricture-free 18 months after the procedure. To the best of our knowledge, our study is the first to describe the successful application of transhepatic dilatation in this context. Transhepatic dilatation is usually complicated by the pancreatic tissue inflammation and fibrosis around the CBD. Indeed, we were unable to perform this procedure in the second patient with stricture, who therefore requires revisional surgery. Given the absence of painful symptoms, we chose to perform of a biliary bypass using Roux-en-Y CJ.

 

In conclusion, the FP with biliary derivation gave good results (whatever the derivation procedure used) and had an acceptable complication rate. There were no complications specifically related to the surgical management of the CBD. However, longer-term recurrence of biliary anastomosis in the pancreatic head may be more frequent--requiring revisional surgery or radiologically-guided dilatation. Also, the FP with CD appeared to be associated with the more frequent occurrence of postoperative alkaline reflux gastritis. In our experience, reinsertion of the CBD into the resection cavity should be considered in the event of accidental injury to the duct during FP. In other cases, we prefer to perform a biliary derivation using Roux-en-Y CJ. We consider that this remains the "gold standard" for the surgical management of symptomatic CP with biliary stricture. Those results must be confirmed by larger prospective series evaluating in particular the results of biliary anastomosis in the pancreatic head.

 

 

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