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Benign hepaticojejunostomy strictures after pancreatoduodenectomy

BMC Gastroenterology volume 24, Article number: 293 (2024) Cite this article

Abstract

Purpose

To determine the causes of benign hepaticojejunostomy strictures (BHSs) after pancreaticoduodenectomy (PD) and the outcome of endoscopic retrograde cholangiography (ERC) treatment for BHSs.

Methods

A total of 175 patients who underwent PD between January 2013 and December 2020 and who were followed up for at least 1 year were included. Preoperative data, operative outcomes, and postoperative courses were compared between the BHS group and the group of patients who did not develop stenosis during follow-up (non-BHS group). The course of treatment in the BHS group was also examined.

Results

BHS occurred in 13 of 175 patients (7.4%). Multivariate analysis of the BHS and non-BHS groups revealed that male sex (OR; 3.753, 95% CI; 1.029–18.003, P = 0.0448) and a preoperative bile duct diameter less than 8.8 mm (OR; 7.51, 95% CI; 1.75–52.40, P = 0.0053) were independent risk factors for the development of BHS. In the BHS group, all patients underwent ERC using enteroscopy. The success rate of the ERC approach to the bile duct was 92.3%. Plastic stents were inserted in 6 patients, and metallic stents were inserted in 3 patients. The median observation period since the last ERC was 17.9 months, and there was no recurrence of stenosis in any of the 13 patients.

Conclusions

Patients with narrow bile ducts are at greater risk of BHS after PD. Recently, BHS after PD has been treated with ERC-related procedures, which may reduce the burden on patients.

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Introduction

Pancreatoduodenectomy (PD) is the standard procedure for treating pancreatic head neoplasms, distal bile duct cancer, and ampullary cancer. PD is a highly invasive procedure that had a high mortality rate of approximately 5% until the 2000s [1, 2]. However, in recent years, the mortality rate for PD has decreased to approximately 1% [3, 4]. Although mortality has decreased, various complications still occur after PD and remain common [5]. Among post-PD complications, pancreatic fistula, delayed gastric emptying, and surgical site infection, which occur relatively early in the postoperative period, have been extensively studied, and the incidence rate of these complications has decreased due to research on preventive measures [6,7,8]. On the other hand, the incidence and causes of benign hepaticojejunostomy strictures (BHSs), which are late-onset complications, are unclear. However, BHS is an important complication because it can cause recurrent cholangitis, intrahepatic stones, jaundice and liver abscesses [9] and, in some cases, requires invasive treatment, resulting in patient suffering [10, 11]. Recent advances in endoscopic retrograde cholangiography (ERC) techniques and the development of endoscopic equipment and devices have improved the outcomes of endoscopic treatment among patients with biliary tract disease. Previously, ERC was found to be difficult in patients who underwent abdominal surgery in which the alignment of the gastrointestinal tract was altered; however, ERC was recently made possible even after upper gastrointestinal surgery [12]. In institutions with skilled endoscopists, endoscopic procedures are also being performed for hepaticojejunostomy strictures after PD [13]. The purpose of this study was to investigate the causes of BHS after PD and to determine the outcome of treatment with ERC for BHS.

Materials and methods

The institutional review board of the St. Marianna University School of Medicine approved this observational, retrospective, single-center study prior to the commencement of data collection and analysis (IRB no. 5617) and waived the informed consent requirement.

Patients and data collection

Patients who underwent PD at the St. Marianna University School of Medicine over 8 years from January 2013 to December 2020 and were able to be followed up for more than 1 year after surgery were retrospectively examined. Patients with incidents of BHS requiring treatment during follow-up were classified as the BHS group, and those without incidents of BHS were classified as the non-BHS group. Patient characteristics, blood test findings, preoperative biliary stenting, preoperative and postoperative bile duct diameters, and surgical outcomes were compared between the BHS and non-BHS groups. The bile duct diameter was measured using CT coronal images. For the preoperative bile duct diameter, CT before ERC (before treatment in jaundice patients) was used. The maximum bile duct diameter of the common hepatic duct immediately below the right hepatic artery was measured (Fig. 1A). The postoperative bile duct diameter was obtained by CT on the 4th day after surgery. The maximum diameter of the bile duct just above the hepaticojejunostomy was measured (Fig. 1B). The cutoff values for preoperative and postoperative bile duct diameters that cause BHS were calculated using receiver operating characteristic (ROC) curves. Furthermore, risk factors for BHS development were examined using multivariate analysis. We also tabulated the content of treatment for hepaticojejunostomy strictures in the BHS group and the course after treatment.

Fig. 1
figure 1

CT coronal images: The preoperative bile duct diameter was measured as the maximum diameter (arrow) of the common hepatic duct just below the right hepatic artery (arrowhead) using CT before ERC was performed (A). The postoperative bile duct diameter was measured as the maximum diameter (arrow) of the bile duct at the anastomotic jejunum using CT on the fourth postoperative day (B)

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Preoperative endoscopic retrograde biliary stenting

Even in patients without jaundice, preoperative ERC was performed when bile duct stenosis was suspected, and endoscopic retrograde biliary drainage was performed when bile duct stenosis was confirmed by cholangiography. In patients with jaundice (for whom the serum total bilirubin concentration was greater than 4 mg/mL), endoscopic nasobiliary drainage (ENBD) or endoscopic biliary stenting (EBS) was performed until the serum total bilirubin concentration was less than 4 mg/mL before surgery.

Pancreatoduodenectomy

In all patients with distal bile duct cancer, the #12a, #12b, #12p, and #12 h lymph nodes were dissected. Dissection up to #12a, #12b, and #12p was performed for pancreatic cancer, IPMN, and papillary cancer, and dissection of the hepatoduodenal ligament was performed as needed for other diseases. When the bile duct was dissected, the bile duct on the hepatic side was clamped, and the bile duct on the resected side was ligated to prevent bile from leaking into the abdominal cavity. Bile duct clamping on the hepatic side continued until subsequent hepaticojejunostomy was performed.

In the cancer patients, bile duct stumps were submitted for rapid intraoperative pathology. If the samples were positive for cancer, additional resections were performed until they became negative for cancer. In all patients, modified Child reconstruction was performed after resection (Fig. 2). Pancreatic anastomosis after PD was performed by duct-to-mucosa and end-to-side pancreatojejunostomy in all patients. Hepaticojejunostomy was performed by end-to-side anastomosis using a 5 − 0 Maxon (Covidien Japan Co, Tokyo, Japan) in all subjects. In cases where the diameter of the bile duct was less than 10 mm in the surgical findings, interrupted suturing was performed at intervals of 2 mm, and in cases where the diameter of the bile duct was greater than 10 mm, continuous suturing was performed. The distance from the bile duct jejunal anastomosis to the gastrointestinal anastomosis was 30–40 cm because a long anastomotic jejunal loop makes it difficult to perform ERC. A silicon tube thinner than the bile duct diameter was cut into strips and fixed as an internal tube in the hepaticojejunostomy anastomosis using 5 − 0 Maxon. Duodenal (or gastric) jejunostomy was performed with Albert–Lembert anastomosis. A 6-mm silicone tube drain (Kaneka Medix Corp., Osaka Japan) was inserted at the superior border of the site of pancreaticojejunostomy, and one 6.3-mm Blake silicone drain (Johnson & Johnson K. K., Tokyo, Japan) was inserted behind the site of hepaticojejunostomy.

Fig. 2
figure 2

Modified child reconstruction was performed after resection

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Definitions of BHS

Regarding postoperative follow-up for each disease, a computed tomography (CT) examination was performed every 3 months after surgery for cancer patients, and a CT examination was performed every 6 months after surgery for noncancer patients. Additional CT scans were performed whenever cholangitis occurred. Magnetic resonance cholangiopancreatography (MRCP) was performed when dilatation of the intrahepatic bile ducts or stones in the bile ducts was suspected in the regular CT examinations or in the CT examinations performed when cholangitis developed. Endoscopic retrograde cholangiography (ERC) was also performed when local strictures of the hepaticojejunostomy were suspected by MRCP. Among patients with hepaticojejunostomy strictures on the ERC, BHS was defined as occurring in those patients without malignant findings on biopsy (Fig. 3).

Fig. 3
figure 3

Endoscopic examination of the ERC revealed a pinhole-shaped bile duct jejunal anastomosis (A). Cholangiography revealed stenosis at the bile duct jejunal anastomosis (B). BHS was defined as no malignant findings on biopsy of the stenosis

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ERC for suspected BHS

ERC was performed when BHS was suspected by CT and MRCP. ERC was performed using enteroscopy, and the bile duct was contrasted from the hepaticojejunostomy. A guidewire was then inserted into the bile duct, and the cannula was further advanced into the bile duct through the guidewire. When the degree of stenosis was weak, temporary dilation was performed using a balloon. In cases of concurrent cholangitis, a 7 Fr plastic stent was inserted after balloon dilation of the stenosis. If the stenosis remained when the stent was removed, it was dilated again using a balloon. When the stenosis was severe, a covering metallic stent was inserted. In addition, when cancer recurrence around the hepaticojejunostomy site was suspected by CT or MRCP or when stenosis due to a neoplastic lesion was suspected during ERC, a metallic stent was inserted after biopsy.

Definitions

Preoperative jaundice was defined as a serum level of total bilirubin greater than 4 mg/mL. Postoperative cholangitis was defined as a fever of 38 °C or higher with an elevated blood inflammatory reaction (white blood cells or CRP), a serum bilirubin concentration of 2 mg/mL or higher, or any ALP, γ-GTP, AST, or ALT levels above the reference values. In addition, CT scans revealed no cause of inflammation other than cholangitis. Pancreatic fistula was defined as grade B or higher by the International Study Group on Pancreatic Surgery (ISGPS) [14], and bile leakage was defined as grade B or higher by the International Study Group of Liver Surgery (ISGLS) [15].

Statistical analysis

There were no missing data in this study. All the statistical computations were performed using JMP 14 (SAS Institute Inc., Cary, NC, USA). Descriptive data are reported as the median (25th to 75th percentile) or count and proportion, as appropriate for the data type. Between-group differences were evaluated using the chi-squared test for categorical variables, with continuous variables evaluated using Student’s t test or the nonparametric Mann–Whitney U test, as appropriate for the data distribution. Receiver operating characteristic (ROC) curves were used to determine cutoff values for preoperative and postoperative bile duct diameters at which postoperative bile duct stricture occurred. The best cutoff value was defined as the value with the highest sum of sensitivity and specificity on the ROC curve. Multivariate logistic regression analyses were performed using a forward stepwise selection procedure. All the statistical tests were two-tailed, and P values less than 0.05 were considered to indicate statistical significance.

Results

Patient demographics

From January 2013 to December 2020, 259 PD procedures were performed at the St. Marianna University School of Medicine. Seven patients in whom two or more hepatic ducts and jejuna were anastomosed instead of the common hepatic duct and 9 patients in which more than one subsegmental hepatectomy was performed simultaneously were excluded from this study. Additionally, 10 patients whose bile duct diameter could not be accurately measured on preoperative CT images and 58 patients whose follow-up duration was less than 1 year were excluded. Ultimately, 175 patients were included in the current study. Since the purpose of this study was to investigate the cause of benign strictures as a complication of PD, hepaticojejunostomy strictures due to cancer recurrence were included in the non-BHS group. The non-BHS group also included patients who developed cholangitis and were suspected of having bile duct stenosis but whose stenosis was not proven by ERC (Fig. 4).

Fig. 4
figure 4

Study flow diagram

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The median follow-up period for the 175 patients was 35.7 (21.4–63.9) months. There were 36 patients with distal bile duct cancer, 18 patients with ampullary cancer, and 75 patients with pancreatic cancer. Biliary stenting was performed preoperatively in 60.6% of the 175 patients, and the median preoperative bile duct diameter was 11 mm (6.7–15). In 53.1% of the patients, hepaticojejunostomy was performed with continuous suturing (Table 1).

Table 1 Patient characteristics and surgical outcomes
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Comparison of the BHS and non-BHS groups

BHS occurred in 13 of 175 patients (7.4%) during the postoperative observation period (Table 2). There were significant differences in sex, preoperative biliary stenting, diameter of the bile duct, diameter of the postoperative bile duct, anastomosis procedure, and occurrence of postoperative and postdischarge cholangitis between the 13 patients in the BHS group and the 162 patients in the non-BHS group. The preoperative bile duct diameter was 7.2 (± 1.5) mm in the BHS group and 11.9 (± 0.4) mm in the non-BHS group (P = 0.0031). In addition, 84.6% of patients in the BHS group did not undergo preoperative biliary stenting, while 35.8% of patients in the non-BHS group did not undergo preoperative biliary stenting (P = 0.0005). Continuous suture hepaticojejunostomy was performed in 15.4% of the BHS group, whereas continuous suture hepaticojejunostomy was performed in 56.2% of the non-BHS group (P = 0.0046). An ROC curve of the preoperative bile duct diameter was generated for 13 patients in the BHS group and 162 patients in the non-BHS group (Fig. 5A). The cutoff value of the preoperative bile duct diameter determined from this ROC curve was 8.8 mm. An ROC curve was also generated for postoperative bile duct diameter (Fig. 5B). The AUC of the ROC curve was 0.78676, and the cutoff value of the preoperative bile duct diameter, which was determined from this ROC curve, was 8.6 mm. Multivariate analysis was performed for the BHS group and the non-BHS group (Table 3). As a result, male sex (OR; 4.05, 95% CI; 1.10-19.49, P = 0.0343) and a preoperative bile duct diameter of 8.8 mm or less (OR; 7.51, 95% CI; 1.75–52.40, P = 0.0053) were identified as independent risk factors for the development of BHS. BHS occurred in 13 (7.4%) of the 175 included patients. Eleven (84.6%) of the 13 patients in the BHS group had a bile duct diameter of 8.8 mm or less, and 10 (76.9%) were male. Patients with a preoperative bile duct diameter of 8.8 mm or less (11 in the BHS group and 56 in the non-BHS group) were then compared, with a median age of 68 (48–74) years in the BHS group and 72 (68–77) years in the non-BHS group (P = 0.019). Postdischarge cholangitis occurred in 63.6% of patients in the BHS group compared with 25% in the non-BHS group (P = 0.012) (Table 4).

Table 2 Univariate analysis of the BHS group and non-BHS group
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Fig. 5
figure 5

ROC curve of preoperative bile duct diameter in the BHS and non-BHS groups; the AUC was 0.76258 (OR: 0.781972; 95% CI: 0.656307–0.931699), P = 0.0059, and the cutoff value of preoperative bile duct diameter was 8.8 mm (A). The cutoff value of the postoperative bile duct diameter in the BHS and non-BHS groups was 8.6 mm (AUC: 0.78676; OR: 0.001708; 95% CI: 0.424105–0.807633; P = 0.0019) (B)

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Table 3 Multivariable analysis of the BHS group and non-BHS group
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Table 4 ; comparison of BHS and non-BHS in cases with bile duct diameter less than 8.8 mm
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Course of treatment for anastomotic stenosis in the BHS group

The median time to occurrence of BHS was 13.2 months (5.8–23.3) after PD (Table 5). BHS occurred at a minimum of 3.3 months and a maximum of 70.9 months after surgery. ERC was performed in all 13 patients with BHS, but hepaticojejunostomy could not be identified in 1 patient. In that case, percutaneous transhepatic biliary drainage (PTBD) was performed, followed by reattempting the ERC via a rendezvous procedure to approach the hepaticojejunostomy. Of the 13 patients in which BHS occurred, none underwent surgery for the treatment of BHS. In 12 patients (92.3%), the first ERC successfully approached hepaticojejunostomy. For treatment, only dilation by balloon was performed in 4 patients, plastic stents were inserted in 6 patients, and metal stents were inserted in 3 patients. In the 9 patients who had a stent inserted, the stent was removed in a median of 119 days (88–293).

Table 5 ; course of treatment for anastomotic stenosis in the BHS group
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Discussion

In this study, BHS occurred in 7.4% of patients after PD. In addition, the median time until the onset of BHS was 395 days after surgery, indicating the need for a relatively long-term follow-up after PD. On the other hand, endoscopists were able to approach the bile duct at the first ERC in 92.3% of the 13 patients in which BHS occurred. Stents were placed in 9 of the 13 patients, but the stents were removed after 119 days of placement, and BHS did not recur in any patients during the 539-day follow-up period. Minimally invasive treatment for BHS is possible at facilities where endoscopists conversant with ERC are enrolled.

The occurrence of BHS after PD has previously been reported to vary between 2.6% and 10.1% [16, 17]. There are differences in the observation period, the definition of BHS, the method of hepaticojejunostomy and the type of thread used; furthermore, in recent years, laparoscopic surgery has also been performed. This is thought to be the reason why the incidence of BHS varies among institutions. Recently, the incidence of BHS after PD has been reported to be approximately 5–8%, which is similar to our results [18, 19].

In this study, male sex and preoperative thin bile duct diameter were identified as risk factors for the development of BHS. Univariate analysis also revealed significant differences in preoperative biliary stenting, postoperative cholangitis and postdischarge cholangitis between the two groups. Biliary stenting was excluded as a factor in the multivariate analysis because biliary stenting was not performed preoperatively when there was no stenosis in the bile duct and the bile duct diameter was almost normal in the patients examined in this study. In addition, postdischarge cholangitis was not included as a factor in the multivariate analysis because it is likely to be a consequence of BHS rather than a cause of BHS. The normal bile duct diameter in elderly individuals was reported to be 8.5 mm by abdominal ultrasonography [20]. According to the results of this study, a bile duct diameter of 8.8 mm or less was a risk factor for the occurrence of BHS. This suggests that patients with a normal bile duct diameter should be considered at high risk for BHS. On the other hand, it is difficult to determine why BHS occurs more frequently in males, although Natsume et al. reported that being male is a risk factor for BHS after PD [21]. Malgras et al. also conducted a multivariate analysis of factors for the occurrence of early biliary complications after PD and found that male sex was an independent risk factor for biliary complications, including BHS, occurring within 90 days after PD [22]. It was thought that males have a deeper abdomen than females and that performing anastomotic manipulation in the deeper part of the abdomen may complicate the procedure and result in anastomotic stenosis, but this cannot be proven chemically and is considered a problem that needs further study with the accumulation of more cases. For narrow bile ducts, it may be possible to prevent the occurrence of BHS by making an incision in the bile duct and widening the anastomotic opening.

There are some reports that consider differences in hepaticojejunostomy procedures and laparotomy, laparoscopic surgery, and robotic surgery as factors for the development of BHS. Tatsuguchi et al. compared long-term outcomes after PD and total pancreatectomy between patients who received interrupted sutures and continuous sutures in hepaticojejunostomy [23]. There was no significant difference between the two groups regarding the incidence of BHS (interrupted suture, 8.6%; continuous suture, 6.2%; p = 0.563). Ito et al. also reported that the incidence of late biliary complications after PD was similar between interrupted suture and continuous suture groups (interrupted suture, 2.7%; continuous suture, 4.0%; p = 0.581) [24]. On the other hand, it has been reported that in patients with a bile duct diameter of 8 mm or less, BHS occurred in 15.6% of patients when hepaticojejunostomy after PD was performed with continuous sutures and in 1.8% of patients when interrupted sutures were performed (p = 0.006) [21]. Laparoscopic hepaticojejunostomy usually employs continuous sutures, and laparoscopic hepaticojejunostomy has been reported to be associated with a greater risk of postoperative BHS [25, 26]. In contrast, hepaticojejunostomy with robotic approaches has a lower incidence of BHS [27]. Bustos et al. evaluated 152 patients who underwent robot-assisted hepaticojejunostomy with interrupted sutures in the anterior wall and continuous sutures in the posterior wall, and they reported that the incidence of BHS was 3.3% [28]. In this study, when the bile duct diameter was less than 10 mm at the time of surgery, hepaticojejunostomy was performed with interrupted sutures, and when the bile duct diameter was 10 mm or more, continuous suture hepaticojejunostomy was performed. In patients with a small bile duct diameter (8.8 mm or less), stenosis occurred even with interrupted sutures. BHS is more likely to occur after hepaticojejunostomy with continuous sutures or with less dense suture techniques in patients with narrow bile duct diameters, but even if hepaticojejunostomy is performed with nodal sutures, BHS will occur at a certain rate in patients with narrow bile duct diameters. In patients with small bile duct diameters, hepaticojejunostomy with continuous sutures or with less dense suture techniques is likely to cause BHS; however, even if interrupted sutures are used, BHS can occur at a certain rate.

Treatment for BHS after PD includes surgery, percutaneous transhepatic biliary drainage, and biliary drainage using the ERC. A recently published meta-analysis of treatments for benign biliary strictures revealed that surgery was associated with fewer long-term recurrences [29]. However, the literature used in this meta-analysis is older and was published between 1997 and 2015. In this meta-analysis, the target disease of 3 articles examining the effects of single plastic stents was chronic pancreatitis, and most of the 6 articles on surgery targeted biliary tract injury after cholecystectomy. Comparing treatments for benign biliary strictures with different causes is not accurate. Performing ERC for BHS after PD poses some difficulties for beginners. For example, there is a problem of whether the endoscope can reach the hepaticojejunostomy site and whether hepaticojejunostomy can be confirmed. During stenting, it is often necessary to place stents in both lobes. In addition, since there are many cases in which a calculus is present upstream of the stenosis, it is necessary to remove the calculus. Therefore, conducting ERC after PD requires knowledge, experience, and procedural familiarity. BHS after PD can be treated minimally invasively in facilities where ERC experts are enrolled [30], and in fact, the number of facilities where post-PD BHS treatment is performed at the time of ERC has increased recently [19, 31]. The technical success rate of plastic stent placement at the anastomosis was reported to be 89.2%, and the stenosis improvement rate was 76.9%31; after 3 months of metal stent implantation, the stenosis improvement rate was 85%, and the stenosis recurrence rate was 5.9% [32].

A limitation of this study is that the preoperative diameter of the bile duct was not the diameter at the time of surgery after jaundice improved. In many patients in whom jaundice improved smoothly, surgery was performed without CT after ERC, so the diameter of the bile ducts could not be measured after jaundice improvement in all patients. Another limitation is the method of hepaticojejunostomy. In this study, the anastomotic method was changed according to the diameter of the bile duct at the time of surgery; therefore, the risk of bile duct stenosis due to differences in anastomotic methods could not be examined. It is necessary to examine whether BHS occurs due to differences in anastomotic methods, which are limited to patients with small bile duct diameters.

Conclusions

BHS after PD is a complication that is not infrequent and is a burden to the patient. BHS is more likely to occur in patients with small preoperative bile duct diameters and in men. For BHS occurring after PD, it has recently become possible to relieve stenosis by treatment using the ERC, which is less invasive.

Data availability

The datasets generated and/or analyzed during the current study are available from the corresponding author upon reasonable request.

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Acknowledgements

We would like to thank Springer Nature Author Services for English language editing.

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Authors and Affiliations

  1. Department of Gastroenterological and General Surgery, St. Marianna University School of Medicine, 2-16-1 Sugao, Miyamae-ku, Kanagawa, 216-8511, Japan

    Shinjiro Kobayashi, Saori Umezawa, Keisuke Ida, Atsuhito Tsuchihashi, Satoshi Koizumi & Takehito Otsubo

  2. Department of Gastroenterology, School of Medicine, St. Marianna University, Kawasaki, Japan

    Kazunari Nakahara, Junya Sato & Keisuke Tateishi

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  1. Shinjiro Kobayashi
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Contributions

Kobayashi S and Nakahara K designed the report; Nakahara K, Umezawa S, Tsuchihashi A, Ida K, Koizumi S, and Sato J contributed to the analysis and interpretation of the data and assisted in the preparation of the manuscript; Nakahara K, Tateishi K, and Otsubo T organized the report; and Kobayashi S wrote the report.

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Correspondence to Shinjiro Kobayashi.

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The institutional review board of St. Marianna University School of Medicine approved this observational, retrospective, single-center study prior to the commencement of data collection and analysis (IRB no. 5617) and waived the informed consent requirement. The study protocol conforms to the ethical guidelines of the 1957 Declaration of Helsinki.

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Kobayashi, S., Nakahara, K., Umezawa, S. et al. Benign hepaticojejunostomy strictures after pancreatoduodenectomy. BMC Gastroenterol 24, 293 (2024). https://doi.org/10.1186/s12876-024-03388-4

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BMC Gastroenterology

ISSN: 1471-230X

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