Retrograde installation of percutaneous transhepatic negative-pressure biliary drainage stabilizes pancreaticojejunostomy after pancreaticoduodenectomy: a retrospective cohort study

Pancreaticoduodenectomy (PD) is a standard procedure for treating malignancy in the pancreatic head and periampullary area. Because PD includes anastomoses, which requires an advanced surgical technique, the mortality rates associated with this procedure in the past few decades have been reported to be approximately 25–30% [1]. Although the mortality rate of patients undergoing PD has recently decreased owing to improvements in surgical techniques and perioperative management strategies, the postoperative morbidity rate is still as high as 40–50% [2]. One of the major complications of PD has been leakage from pancreaticoenteric anastomosis.

This morbidity frequently leads to a fatal course, because the leaked pancreatic juice may affect the surrounding structures. Digestive enzymes in the leaked fluid can also disrupt the other anastomoses (i.e., gastroenterostomy, enteroenterostomy, or choledochoenterostomy) and sometimes cause massive hemorrhage by eroding the vessels. These conditions delay the initiation of adjuvant chemotherapy, and eventually yielding poor long-term results, even though recent technologies provide effective interventions for controlling diverse complications. Thus, several procedures associated with PD have been investigated, with a focus on leakage prevention.

Strategies for preventing the incidence of pancreatic fistulas are divided into two categories. The first category includes procedures that reinforce the consistency of anastomosis. These are related to the methodology of anastomosis or pathway of pancreatic juice. There is no consensus regarding the clinical effectiveness of this category of strategies. For example, whether the dunking technique is superior or inferior to duct-to-mucosa anastomosis during pancreaticojejunostomy (PJ) cannot be concluded [3]. In addition, although recent studies showed the advantage of pancreaticogastrostomy (PG) over PJ in reducing the incidence of pancreatic fistula, no consensus has been reached regarding the issues of morbidity and mortality [4, 5].

Meanwhile, the second category includes several procedures that reduce the burden of pancreaticoenteric anastomosis. Some of these procedures are associated with the preoperative or intraoperative conditioning of the biliary tree, and others with stabilizing the anastomoses by special reconstruction methods. Still, others involve pancreatic or biliary decompression using the external drainage. In this regard, in June 2012, we introduced retrograde installation of percutaneous transhepatic negative-pressure biliary drainage (RPTNBD) for biliopancreatic decompression in patients who had undergone PD for malignant disease (i.e., duodenal cancer, pancreatic cancer, bile duct cancer, and other malignant conditions requiring PD for R0 resection). Preoperatively, endoscopic nasobiliary drainage (ENBD) was applied for biliary decompression. This novel procedure could minimize the leakage rates of pancreaticoenterostomy and decompress both PJ and choledochojejunostomy (CJ) simultaneously.

The aim of this study was to investigate the feasibility of RPTNBD by comparing clinical outcomes before and after the introduction of this technique.

Twenty-one patients underwent RPTNBD during PD for a malignant disease of the duodenum, common bile duct, or pancreas. The patients’ demographics are presented in Table 1. The mean age and BMI of the enrolled patients were 65.5 ± 11.2 years (range, 36–82 years) and 22.6 ± 4.1 kg/m² (range, 15.3–33.3 kg/m²), respectively. Among the 21 enrolled patients, 13 (61.9%) underwent PPPD. The operation time was 412.0 ± 92.8 min (range, 240–600 min), and the duration of hospital stay was 39.4 ± 26.4 days (range, 13–105 days). The time to the first semi-blend diet was 8.4 ± 5.6 days (range, 3–31 days). The tumor size was 3.1 ± 1.2 cm (range, 1.1–5.4 cm). The numbers of retrieved and metastatic lymph nodes were 18.0 ± 8.1 (range, 2–36) and 1.6 ± 2.8 (range, 0–8), respectively. Thirteen patients showed postoperative morbidities. Among the 13 cases, 10 (47.6%) corresponded to a morbidity of Clavien-Dindo grade III or higher (Table 2). Four patients underwent radiological interventions for fluid collection around the PJ or CJ sites (cases 7, 11, 14, and 16); however, tubographic images acquired via the RPTNBD pathway showed no association between PJ and the fluid collection. All the patients recovered with conservative treatment.

The demographics of the internal control are presented in Table 3. The mean age and BMI of the enrolled patients were 62.6 ± 11.4 years (range, 30–78 years) and 22.6 ± 3.5 kg/m² (range, 17.2–32.4 kg/m²), respectively. Among the 31 patients in the internal control group, 20 (64.5%) underwent PPPD. The operation time was 420.2 ± 170.4 min (range, 267–1,015 min) and the duration of hospital stay was 30.3 ± 22.5 days (range, 9–118 days). The time to the first semi-blend diet was 12.0 ± 12.4 days (range, 4–61 days). The tumor size was 3.2 ± 1.4 cm (range, 0.8–5.8 cm). The numbers of retrieved and metastatic lymph nodes were 19.7 ± 6.7 (range, 4–36) and 1.5 ± 2.4 (range, 0–8), respectively. Twenty-two patients had postoperative morbidities. Among the 22 cases, 10 (52.4%) corresponded to a morbidity of Clavien-Dindo grade III or higher (Table 4). As shown in Table 5, the incidence of postoperative complications did not differ between the study participants and the internal controls (P = 0.494). However, the internal controls showed a higher incidence of PJ complications than the study participants (P = 0.020). Mortality occurred in the internal controls, although 12 (38.7%) patients with PJ complication underwent radiological interventions of PAD to remove the digestive juice leaked from the anastomoses. The internal control group showed higher morbidity and mortality rates than the RPTNBD group (Additional file 1).

Considering the results, we believe that RPTNBD might contribute to the salvage treatment of a morbidity after PD. Because the present study included far advanced cases that required some challenging procedures (i.e., major vessel reconstruction or simultaneous hepatectomy) to accomplish R0 resection, several cases carried a high risk of morbidity or mortality. However, most postoperative complications were managed with intravenous antibiotics and additional PAD. One patient who underwent portal vein and right hepatic artery reconstructions did not show any postoperative morbidity. It was remarkable that no mortality occurred even in the advanced cases that required technically demanding procedures.

Because the corrosive property of pancreatic juice might cause secondary catastrophes in the surgical field, several strategies have been designed to prevent pancreaticoenteric leakage after the introduction of PD. Although many strategies have been established for the postoperative safety of PD, biliary tract decompression is one of the most traditional methods that reduces the morbidity rate of PD. In 1935, Whipple et al. first proposed preoperative biliary drainage (PBD), by which obstructive jaundice could be corrected in patients with periampullary lesions [7]. Preoperative correction of jaundice could be related to the clinical outcomes of patients undergoing PD, because hyperbilirubinemia is associated with impaired liver function, coagulation disorder, compromised immunity, accumulation of circulating endotoxin, and wound problems [8‐11]. Currently, PBD has been facilitated by the technical advancement of radiological interventions (i.e., PTBD) and endoscopic procedures. With regard to the clinical outcomes of patients undergoing PD, some studies showed the benefits of PBD, including improved resection rate, morbidity, and mortality rates [12, 13]. However, other reports indicated drawbacks of this procedure. Several researchers reported the possibility of hyperamylasemia after radiological or endoscopic procedures [14, 15]. In addition, some comparative studies revealed that PBD caused certain morbidities rather than advantages in patients who underwent PD [16, 17]. Therefore, the benefit of performing PBD before PD is not yet established.

Biliary drainage can be performed intraoperatively. Doi et al. reported an intraoperative biliary decompression technique in which a newly developed curved drainage clamp (Mizuho Co., Tokyo, Japan) was used for the drainage of the common hepatic duct stump [18]. However, it was difficult to determine the effect of this technique on anastomosis, despite the possibility that this technique reduces the risk of hepatic complications. As part of another biliary decompression technique, the special structures are added after PD. Two strategies were used for adding these special structures over the last few decades. Braun anastomosis is one of these two strategies; it reduces the pressure in the biliopancreatic limb to avoid the afferent loop syndrome. The result of a randomized clinical trial showed that Braun anastomosis might decrease the pressure in the biliopancreatic limb after standard Whipple’s operation [19]. Separating anastomoses is the other strategy. Isolated Roux loop PJ was performed to lower the incidence rate of pancreatic fistula [20]. Double Roux-en-Y reconstruction was proposed to isolate pancreaticoenteric, choledochoenteric, or gastroenteric anastomosis [21]. However, all these modified structures rendered no significant protection against pancreaticoenteric leakage [19‐21].

When PJ failures are diagnosed postoperatively, several radiological interventions can be helpful in maintaining the conservative treatment. PTBD and PAD are the representative procedures that have been widely accepted in the clinical field. These interventions can minimize anastomotic soling. PTBD reduces biliary flow into the afferent loop, which effectively decreases pressure in the disrupted anastomosis. PAD, on the contrary, may remove the digestive juice that has already leaked from the PJ or CJ site. Currently, the conservative strategy for the management of PJ or CJ failure is usually composed of PTBD or PAD, when radiological interventions can be performed under the guidance of real-time imaging techniques. Although PTBD heals the failed anastomosis by reducing the leakage, this intervention depends on biliary imaging. If the biliary ducts are not dilated, postoperative PTBD is technically demanding. Therefore, we performed RPTNBD intraoperatively. Our novel method was designed by incorporating the advantages of the previous procedures. The biliary decompression effect of RPTNBD may be equal to that of PTBD; however, the former does not require radiological guidance. As RPTNBD is intraoperatively performed during PD, surgeons can insert the drainage tube into the biliary duct.

RPTNBD has a protective effect against anastomotic leakage in both PJ and CJ sites. Similar to PTBD, RPTNBD decreases the high pressure of the afferent loop resulting from the accumulation of bile or pancreatic juice, which inevitably occurs during the paralytic ileus period after PD. When a minor leakage occurs in the PJ or CJ site, RPTNBD can reduce the risk of anastomotic failure. Although PAD had to be applied for fluid collection around the PJ or CJ site in several cases (cases 7, 11, 14, and 16) in the present study, these morbidities did not lead to the fulminant failure of PJ or CJ. Their drain amylase levels did not exceed three times the serum amylase levels. Tubography is also possible via the RPTNBD route, which can facilitate making a critical decision in the postoperative course (Additional file 2). For example, although computed tomography implied complicated fluid collection around the pancreas in two cases (cases 7 and 11), in our study, we could confirm no connection between the fluid collection and PJ using tubography via RPTNBD. In such cases, tubography via RPTNBD could provide an important clue to avoid unnecessary delay of the clinical decision.

One limitation of RPTNBD is that the surgeon should have reliable knowledge regarding the hepato-biliary anatomy. This is also an important precondition for performing RPTNBD. Although we did not encounter any accidental hemorrhage, introducing a probe into the intrahepatic bile duct may harbor a risk of injury to the hepatic structures.

In conclusion, if a skilled surgeon performs RPTNBD, pancreaticoenteric anastomosis may be stabilized after PD. RPTNBD is expected to be effective in minimizing PJ or CJ anastomotic failure, which can arise in compromised patients.