Sage Journals: Discover world-class research

Abstract

Background:

There is controversy regarding which is the best reconstruction technique after the pancreatoduodenectomy. Currently, there are no studies comparing the three most frequent reconstruction techniques: Whipple + Roux-en-Y gastrojejunostomy (WRYGJ), pyloric-preserving + Billroth II (PPBII), and Whipple + BII (WBII).

Methods:

Between 2012 and March 2023, 246 patients underwent pancreaticoduodenectomy with the following type of reconstruction techniques: (1) WRYGJ: 40 patients; (2) PPBII: 118 patients; and (3) WBII: 88 patients. A retrospective comparative study among these groups was performed.

Results:

No significant differences were found among the groups regarding duration of the surgery, the blood volume transfused, or caliber of the Wirsung duct. The size and types of tumors, the degree of differentiation and tumor invasion of the peripancreatic tissue, vascular and neural structures, and lymph nodes were similar among the groups. The rate of R0 resection was lower in WBII (62.5% [55/88]) than in WRYGJ (75% [30/40]) and PPBII (72% [85/118]), but statistically insignificant among the groups (p = 0.232). The incidences of relevant B/C postoperative pancreatic fistula (POPF) were similar among the groups: 7.5% (7/40) in WRYGJ, 17% (20/118) in PPBI, and 26.2% (23/88) in WBII (p = 0.292). In addition, the incidence of B/C delayed gastric emptying (DGE) was higher in WBII (27.3% [24/88]) than in WRYGJ (20% [8/40]) and PPBII (19.5% [23/118]) but statistically insignificance among the groups (p = 0.381). The incidence of medical and surgical complications, intensive care unit and hospital stays, morbimortality at 90 days, and 5-year survival were similar among the groups. Multivariate analysis revealed that POPF grade B/C was a risk factor for DGE grade B/C (odds ratio (OR) = 9.903, 95% confidence interval (CI) = 4.829–20.310; p < 0.001), and a <3-mm Wirsung duct was a risk factor for POPF (OR = 3.604, 95% CI = 1.791–7.254; p < 0.001).

Conclusion:

No technique was superior to the others. Only relevant POPF B/C was a risk factor for DGE B/C, and <3 mm Wirsung for a POPF.

Keywords

Pancreatic head cancer pancreatoduodenectomy reconstruction techniques postpancreatoduodenectomy Roux-en-Y gastrojejunostomy postoperative pancreatic fistula delayed gastric emptying

Context and Relevance

Regarding the controversy over the best reconstruction technique after pancreatoduodenectomy, we compared three reconstruction techniques (classical Whipple with isolated Roux-en-Y gastrojejunostomy (WRYGJ; n = 40), pyloric-preserving with B-II (PPBII; n = 118), and Whipple with Billroth II (WBII; n = 88). No significant differences were found among the groups regarding operative time, blood transfusion, tumoral invasion of lymph nodes, R0, hospital stay, 90-day morbimortality, and long-term survival. Relevant postoperative pancreatic fistula (POPF) was a risk factor for relevant delayed gastric emptying, and Wirsung duct <3 mm was a risk factor for POPF. Thus, neither reconstructive technique was superior to the other, but the prevention of POPF and the improvement in the management of pancreatojejunostomy with a <3-mm Wirsung duct could improve the results.

Introduction

Pancreatoduodenectomy (PD) has been universally accepted as therapy for pancreatic head and periampullary tumors due to the low rates of postoperative mortality in specialized centers, ranging from 0% to 3.8% in several recent series.^1
–5 On the contrary, the rates of post-PD complications such as POPF, intra-abdominal abscesses, intra-abdominal hemorrhage, and delayed gastric emptying (DGE) remain unchanged. Thus, POPF is the most serious complication with an overall incidence between 19.5% and 33.5% according to several researchers.^1
–3,5,6 DGE is a less severe, although it is the most frequent complication that develops in between 9.1% and 50% of patients and has been associated with a prolonged hospital stay, increased costs, and a decreased in quality of life.^2,5
–8 With the objective to reduce the rate of POPF and DGE, several modifications have been performed over the classical Billroth II (BII) reconstructive technique after PD, with or without pyloric-preserving, such as the use of an isolated Roux-en-Y pancreatojejunostomy,^6,9
–13 an isolated Roux-en-Y gastrojejunostomy,^14
–17 and a more recently isolated Roux-en-Y draining pancreatojejunostomy and gastrojejunostomy.¹⁸ However, the choice of the best reconstruction technique, based on achieving the lesser incidence of morbimortality and hospital length of stay, remains controversial. Therefore, many studies have been performed comparing BII versus Roux-en-Y reconstruction techniques after classical Whipple PD,^14
–17,19 pylorus-preserving versus classical Whipple PD using BII reconstruction,^8,20 and pylorus-preserving versus pylorus-resecting PD.^21
–24

The aim of this study was to compare the three most common techniques of PD and subsequent gastrointestinal reconstruction, such as classical Whipple with isolated Roux-en-Y gastrojejunostomy (WRYGJ), pyloric-preserving with Billroth II (PPBII), and Whipple with Billroth II (WBII). To our knowledge, this type of study has not been previously reported.

Patients and methods

Study design and patient recruitment

Between January 2012 and March 2023, 262 patients underwent PD at our institution for tumors located in the pancreatic head and periampullary regions.

After the exclusion of 16 patients who underwent PD with different reconstruction techniques, a sample of 246 patients was divided into three groups according to the following PD and gastrointestinal reconstruction techniques: (1) patients with classical Whipple PD and reconstruction with Roux-en-Y gastrojejunostomy in an isolated loop (WRYGJ [n = 40; 16.3%]); (2) patients with pylorus-preserving PD and Billroth II reconstruction (PPBII [n = 118; 47.9%]), and (3) patients with classical Whipple PD and BII reconstruction (WBII [n = 88; 35.8%]). A flowchart of the patient selection process is shown in Fig. 1.

Fig. 1.

Flowchart of patient selection. Reconstruction techniques after pancreatoduodenectomy (PD): Whipple + Roux-en-Y-gastrojejunostomy (WRYGJ), Pyloric-preserving + Billroth II (PPBII), and Whipple + Billroth II (WBII).

A comparative analysis concerning of preoperative, intraoperative, and postoperative variables was performed among the three groups of patients.

Study endpoints

The primary endpoint was to analyze the incidence and risk factors of relevant B/C POPF and DGE. Secondary endpoints comprised the analysis of the remaining postoperative complications, length of hospital stay, hospital and 90-day mortality, and 1-, 3-, and 5-year survival. The last outpatient review of patients was carried out until December 2023.

Surgical techniques

The surgical details of PD have been previously described.²⁵ Pylorus-preserving PD was carried out in patients with tumor distant from the duodenum, and antrectomy was performed when the tumor was close to the proximal portion of the duodenum. During pylorus-preserving PD, the proximal duodenum was preserved 2–3 cm distal to the pylorus, dividing the right gastric artery and the pyloric branch of the vagus nerve. In classical Whipple PD, an antrectomy of 20%–30% without truncal vagotomy was performed.

The variation of pancreatojejunostomy was selected based on the surgeon’s experience and the presence of risk factors, such as a <3 mm Wirsung duct diameter and/or a soft consistency of the pancreas. Pancreatojejunostomy was usually performed with an end-to-side duct-to-mucosa anastomosis using the two-layer technique. The pancreatojejunostomy was performed using an external, internal, or non-ductal stent depending on the caliber of the Wirsung duct, pancreatic texture, and surgeon’s preference. The external stent was closed at discharge and removed 6 weeks after surgery at the outpatient clinic. Non-ductal stent was performed using either duct-to-mucosa pancreatojejunostomy or invagination pancreatojejunostomy. An end-to-side hepaticojejunostomy was performed 10–15 cm distal to the pancreatojejunostomy. An end-to-side gastrojejunostomy or duodenojejunostomy (in PPBII) was routinely performed in the antecolic position, approximately 60–65 cm distal to the hepaticojejunostomy. The Roux-en-Y reconstruction after classical Whipple PD was tailored using two jejunal loops. Sixty centimeters afar from the bilio-jejunostomy, a proximal jejunal loop was anastomosed end-to-side to the foot of the jejunal loop. The 60-cm-long distal jejunal loop, that comes from antecolic gastrojejunostomy, was brought downward to perform the referred foot of the loop jejunojejunostomy (Fig. 2). Two drains were placed superior and inferior to the pancreatojejunostomy.

Fig. 2.

Reconstruction procedures after pancreaticoduodenectomy (PD): (A) Pyloric-preserving PD and Billroth II (PPBII; n = 118 cases); (B) Whipple resection and Billroth II (WBII; n = 88 cases); and (C) Whipple resection and Roux-en-Y gastrojejunostomy (WRYGJ; n = 40 cases).

Postoperative management

Postoperative parenteral nutrition was administered to all patients. Antibiotic prophylaxis was given with 2 g of iv cefazolin, and in patients with biliary stents, jaundice, or cholangitis, iv therapy with piperacillin + tazobactam 4/0.5 was administered every 6 h for 5 days.

Intra-abdominal drains were usually removed on the fifth or sixth postoperative day (POD) in the absence of a fistula, hemorrhage, or infection with amylase levels of abdominal drainage <400 IU.

In the absence of POPF, the nasogastric tube was usually removed on POD 3, and sips of water were progressively administered thereafter, administering a regular diet on POD 7. Prokinetics, such as octreotide (100 mg/mL every 8 h), erythromycin or metoclopramide, were often administered postoperatively if the patient had DGE, and octreotide (100 mg/mL every 8 h) was administered in patients with POPF.

Definitions

DGE was classified according to the definition approved by the ISGPS: grade A (mild), inability to tolerate solid oral intake by POD 7 and usually no vomiting; grade B (moderate), inability to tolerate solid oral intake by POD 14 with or without vomiting; and grade C (severe), inability to tolerate solid oral intake by POD 21 with or without vomiting. Grade A is not considered clinically relevant.²⁶

Pancreatic fistulas were classified according to the definition formulated by the ISGPS: grade A, biochemical fistulas; grade B, requirement of change in therapy or percutaneous drainage of collections; and grade C, clinical instability requiring drainage of collections or reoperations, leading to organ failure and/or mortality.²⁷ Postpancreatoduodenectomy hemorrhage (PPH) was classified according to the ISGPS definition.²⁸ Complications were reported using the Clavien classification.²⁹

Statistical analysis

Qualitative variables are expressed as absolute numbers, and relative frequencies are expressed as percentages. Associations were analyzed using the chi-square test or Fisher’s exact test, as appropriate. Most quantitative variables did not have a normal distribution according to the Kolmogorov–Smirnov test; therefore, all quantitative variables are expressed as medians and percentiles. The relationships between quantitative variables were analyzed using the Mann–Whitney U test.

All clinically significant variables and variables with p < 0.05 in a univariate analysis were subsequently investigated using a binary logistic regression model to evaluate the association between variables at baseline and 90-day mortality. We also investigated their relationship with grade B and C DGE. Results are expressed as odds ratios and 95% confidence intervals. Survival analysis was performed using the Kaplan–Meier estimator and log-rank test. A p-value < 0.05 was considered statistically significant. Statistical analyses were performed using the SPSS Statistics version 25 (SPSS Inc., Chicago, IL, USA).

Ethical aspects

This retrospective cohort study was approved by our institutional review board (approval no. 24/034) and conducted in accordance with the Helsinki Declaration of 1975 and revision in 1983. The need for local clinical research ethics committee approval was waived due to the retrospective nature of the study. This study was registered in a retrospective research registry (UIN researchregistry9298). Informed consent for surgical treatment was obtained from all patients before surgery. No funding was received for this study.

Results

In the comparison of the preoperative characteristics among the groups, the patients of the WRYGJ group were more frequently submitted to neoadjuvant chemotherapy, and patients of group WBII showed significantly higher values of serum bilirubin (p = 0.022). No significant differences were found in the comparison of the remaining variables among the groups (Table 1).

Table 1.

Preoperative characteristics of the patients.

	WRYGJ (n = 40)	PPBII (n = 118)	WBII (n = 88)	p
Age (years)	65 (28-89)	65 (16-86)	69 (40-86)	0.686
Age >75	8 (20%)	36 (30.5%)	27 (30.7%)	0.401
Sex (male/female)	22/18 (55%/45%)	62/56 (52.5%/47.5%)	47/41 (53.4%/46.6%)	0.964
ASA score				0.564
I	3 (7.5%)	11 (9.3%)	6 (6.8%)
II	18 (45%)	51 (43.2%)	37 (42%)
III	17 (42.5%)	51 (43.2%)	43 (48.9%)
IV	2 (5%)	5 (4.2%)	2 (2.3%)
Body mass index, kg/m²	25 (18-36)	24 (16-43.3)	25 (14-42)	0.615
Comorbidities
Smoking	9 (22.5%)	23 (19.5%)	22 (25%)	0.391
Alcohol consumption	10 (25%)	12 (10.2%)	12 (13.6%)	0.110
Diabetes mellitus	12 (30%)	29 (27.5%)	24 (27.3%)	0.829
Hypertension	14 (35%)	52 (44.1%)	43 (48.9%)	0.135
Cardiovascular	13 (32.5%)	44 (37.3%)	33 (37.5%)	0.635
Pulmonary	9 (22.5%)	26 (22%)	16 (18.2%)	0.430
Tumor	9 (22.5%)	18 (15.3%)	10 (11.4%)	0.072
Neoadjuvant chemotherapy	10 (25%)	11 (9.3%)	8 (9.1%)	0.018
Clinical features
Jaundice	26 (65%)	75 (63.6%)	54 (61.4%)	0.860
Abdominal pain	16 (40%)	50 (42.4%)	40 (45.4%)	0.965
Weight loss	19 (47.5%)	57 (48.3%)	48 (54.5%)	0.447
Duodenal obstruction	5 (12.5%)	3 (2.5%)	5 (5.7%)	0.051
Gastrointestinal bleeding	3 (7.5%)	5 (4.2%)	5 (5.7%)	0.722
Preoperative pancreatitis	7 (17.5%)	14 (11.9%)	8 (9.1%)	0.281
Preoperative cholangitis	10 (25%)	22 (18.6%)	17 (19.3%)	0.675
Diagnostic procedures/findings
CT	39 (97.5%)	117 (98.3%)	88 (100%)	0.849
MRI	32 (80%)	85 (72%)	63 (70.5%)	0.515
Endoscopic ultrasonography	28 (70%)	73 (61.9%)	51 (58%)	0.429
ERCP	18 (45%)	70 (59.8%)	40 (45.5%)	0.076
PTHC	8 (20%)	14 (11.9%)	9 (10.2%)	0.287
Tumor size (cm)	2.4 (0.1-6)	2 (0.3-7)	2.4 (0-5.9)	0.085
Bile duct size (cm)	1.1 (0-2.4)	1.2 (0-3)	1.3 (0.2-3.1)	0.052
Preoperative biliary stent	15 (37.5%)	59 (50%)	36 (40.9%)	0.615
Laboratory findings
Hemoglobin (g/dL)	13.1 (11.2-15.8)	12.6 (10.3-16)	12.9 (9-17.2)	0.406
Creatinine (mg/dL)	0.8 (0.48-1.9)	0.78 (0.4-2.5)	0.73 (0.4-1.32)	0.222
Glycemia (mg/dL)	107 (72-211)	108 (56-290)	116 (70-304)	0.087
Albumin (g/dL)	3.9 (2.8-4.5)	3.9 (2.6-4.8)	3.8 (2.5-4.8)	0.292
Bilirubin (mg/dL)	0.6 (0.2-21)	0.9 (0.2-24)	1 (0.2-28.9)	0.022
CA 19-9 (U/mL)	15 (0.3-6713)	18 (0-1698)	40 (0-1125)	0.101

Data are presented as n (%) or median (range).

ASA: American Society of Anesthesiologists; CA 19-9: carbohydrate antigen 19-9; CT: computed tomography; DGE: delayed gastric emptying; ERCP: endoscopic retrograde cholangiopancreatography.

Regarding perioperative variables, duration of surgery, frequency and blood volume transfused, and caliber of the Wirsung duct did not show significant differences among the groups. No significant differences were detected among the different groups regarding the rate of consistency (hard or soft) of the pancreas (p = 0.130). The rate of vascular resection because of tumor invasion and use of octreotide in patients with POPF were similar among the groups. No significant differences were found among the groups about the size and types of tumors and tumor invasion of the peripancreatic tissue and around the celiac axis or superior mesenteric artery. The number of resected lymph nodes was significantly less in the PPBII group (p < 0.001). However, the frequency and number of lymph nodes invaded by the tumor were similar among the groups, as it occurs with macrovascular and neural invasion. The rate of R0 resection was lower in WBII but without statistically significance among the groups. Tumor staging (TNM) did not show significant differences between the groups (p = 0.514) (Table 2).

Table 2.

Perioperative variables and histological features.

	WRYGJ (n = 40)	PPBII (n = 118)	WBII (n = 88)	p
Duration of surgery (min)	383 (240-570)	380 (230-680)	412 (190-630)	0.116
Transfusion required	5 (12.5%)	15 (12.7%)	19 (21.6%)	0.222
Blood transfused (units)	0 (0-3)	0 (0-7)	0 (0-7)	0.386
Surgical findings/techniques
Caliber of Wirsung duct (mm)				0.094
>3 mm	15 (37.5%)	60 (50.8%)	52 (59.1%)
<3 mm	25 (62.5%)	58 (49.2%)	36 (30.9%)
Consistency of the pancreas				0.130
Hard	15 (37.5%)	50 (42.4%)	46 (52.3%)
Soft	25 (62.5%)	68 (57.6%)	42 (47.7%)
Vascular resection	4 (10%)	11 (9.3%)	9 (10.2%)	0.975
Use of octreotide	2 (5%)	17 (14.4%)	16 (18.2%)	0.312
Histological features
Type of tumor				0.136
Adenocarcinoma	25 (62.5%)	71 (60.2%)	73 (82.9%)
Cholangiocarcinoma	2 (5%)	13 (11%)	3 (3.4%)
Neuroendocrine	3 (7.5%)	9 (7.6%)	2 (2.3%)
Other	10 (25%)	25 (21.2%)	10 (11.4%)
Tumor invasion				0.058
In situ	0 (0%)	4 (3.4%)	2 (2.3%)
<2 cm	5 (12.5%)	31 (26.3%)	8 (9.1%)
>2 cm limited to pancreas	15 (37.5%)	35 (29.7%)	28 (31.8%)
Peripancreatic invasion	13 (32.5%)	31 (26.3%)	37 (42%)
Invasion at CA or SMA	0 (0%)	2 (1.7%)	4 (4.5%)
Lymph node invasion	20 (50%)	63 (53.3%)	55 (62.5%)	0.276
Number of resected nodes	18 (10-38)	13 (9-53)	17 (8-78)	<0.001
Number of positive nodes	1 (1-8)	1 (1-12)	1 (1-14)	0.240
Macrovascular invasion	7 (17.5%)	26 (22%)	11 (12.5%)	0.067
Neural invasion	18 (45%)	51 (43.2%)	45 (51.1%)	0.565
R0 resection	30 (75%)	85 (72%)	55 (62.5%)	0.232
Tumor staging (TNM)				0.514
IA	3 (7.5%)	19 (16.1%)	3 (3.4%)
IB	5 (12.5%)	10 (8.5%)	8 (9.1%)
IIA	3 (7.5%)	10 (8.5%)	13 (14.7%)
IIB	13 (32.5%)	33 (27.9%)	28 (31.8%)
III	6 (15%)	24 (20.3%)	21 (23.9%)
IV	2 (5%)	4 (3.4%)	2 (2.3%)

Data are presented as n (%) or median (range).

CA: celiac artery; DGE: delayed gastric emptying; PD: pancreatoduodenectomy; SMA: superior mesenteric artery.

No significant differences in the incidence of medical complications were recorded. The incidence of postoperative pancreatitis did not show significant differences among the groups (p = 0.561). The incidence of relevant B/C POPF and relevant B/C DGE was higher in the group WBII, but these differences did not reach statistical significance. The incidence of relevant B/C PPH was lower in the WRYGJ, but no statistical difference was found between the groups. The incidence of complications according to Clavien classification was similar among the groups. Intensive care unit stay was similar among the groups, although hospital stay was lower in WRYGJ, yet not showing significant differences. Throughout the follow-up, complications and morbimortality at 90 days were similar among the patients, except for the significantly higher incidence of de novo exocrine insufficiency in WBII (p = 0.049). No significant differences were seen regarding 1-, 3-, and 5-year actuarial patient survival among the groups, both in patients with malignant (p = 0.339) and non-malignant tumors (p = 0.271) (Table 3 and Fig. 3).

Table 3.

Morbimortality after PD and long-term survival.

	WRYGJ (n = 40)	PPBII (n = 118)	WBII (n = 88)	p
Medical complications	12 (30%)	44 (37.3%)	26 (29.5%)	0.710
Surgical complications
Wound infection	6 (15%)	17 (14.5%)	13 (14.8%)	0.897
Postoperative pancreatitis	5 (12.5%)	20 (16.9%)	17 (19.3%)	0.561
POPF				0.292
Grade A	9 (22.5%)	19 (16.1%)	20 (22.7%)
Grade B	6 (15%)	12 (10.2%)	16 (18.2%)
Grade C	1 (2.5%)	8 (6.8)	7 (8%)
Non-POPF	24 (60%)	79 (66.9%)	45 (51.1%)
DGE				0.381
Grade A	6 (15%)	19 (16.1%)	17 (19.3%)
Grade B	6 (15%)	21 (17.8%)	18 (20.5%)
Grade C	2 (5%)	2 (1.7%)	6 (6.8%)
Non-PPH	26 (65%)	76 (64.4%)	47 (53.4%)
PPH				0.869
Grade A	2 (5%)	6 (5.1%)	4 (4.5%)
Grade B	1 (2.5%)	6 (5.1%)	7 (8%)
Grade C	1 (2.5%)	5 (4.2%)	5 (5.7%)
Non-PPH	36 (90%)	101 (85.6%)	72 (81.8%)
Reoperation	2 (5%)	20 (16.9%)	13 (14.8%)	0.112
Hemoperitoneum	1 (2.5%)	5 (4.3%)	5 (5.7%)
POPF	1 (2.5%)	8 (6.8%)	7 (7.9%)
Other	0 (0%)	7 (5.9%)	1 (1.1%)
Complications (Clavien-Dindo)				0.712
No complications	12 (30%)	37 (31.3%)	20 (22.7%)
Grade I-II	20 (50%)	51 (43.2%)	46 (52.3%)
Grade III-IV	8 (20%)	30 (25.4%)	22 (25%)
ICU stay (d)	2 (1-13)	2 (2-30)	2 (1-28)	0.136
Hospital stay (d)	14 (5-78)	17 (7-91)	20 (7-97)	0.107
Follow-up
Mortality (90-d)	1 (2.5%)	4 (3.4%)	3 (3.4%)	0.791
Morbidity (90-d)	25 (62.5%)	73 (61.2%)	63 (71.6%)	0.487
De novo diabetes	5 (12.5%)	25 (21.2%)	16 (18.2%)	0.804
De novo exocrine insufficiency	13 (32.5%)	47 (39.8%)	43 (48.9%)	0.049
Venous thrombosis	0 (0%)	6 (5.1%)	5 (5.7%)	0.492
Pulmonary embolism	0 (0%)	4 (3.4%)	2 (2.3%)	0.618
Adjuvant chemotherapy	18 (45%)	59 (50%)	43 (48.9%)	0.516
Patient survival (malignancy)				0.339
1 year	80.6%	85.9%	80.3%
3 years	44%	44.7%	54.5%
5 years	14.7%	25.7%	29.6%
Patient survival (non-malignancy)				0.271
1 year	100%	90.9%	90%
3 years	100%	90.9%	77.1%
5 years	66.7%	90.9%	77.1%

Data presented as n (%) or median (range).

DGE: delayed gastric emptying; ICU: intensive care unit; PD: pancreatoduodenectomy; POPF: postoperative pancreatic fistula; PPH: postpancreatoduodenectomy hemorrhage.

Fig. 3.

The 1-, 3-, and 5-year patient survival in the three groups of reconstruction after pancreatoduodenectomy (WRYGJ, PPBII, and WDII). (A) Patients with malignant tumor: no significant differences among the groups (p = 0.339). (B) Patients with non-malignant tumor: no significant differences among the groups (p = 0.271).

Binary multivariate analysis revealed that POPF-relevant grade B/C was a risk factor for DGE-relevant grade B/C (Table 4). In addition, another binary multivariate analysis demonstrated that the presence of a Wirsung duct with a <3-mm diameter was a risk factor for POPF (Table 5).

Table 4.

Binary multivariate analysis: risk factors for post-PD DGE grades B/C.

	p	OR	95% CI		p	OR	95% CI
WBII	0.294	1.498	0.704	3.187
PPBII	0.880	0.908	0.257	3.205
WRYGJ	0.856	1.098	0.401	3.009
Wirsung duct <3 mm	0.889	1.057	0.486	2.297
Hard pancreas	0.271	0.655	0.308	1.393
Relevant POPF B/C	<0.001	9.084	4.291	19.229	<0.001	9.903	4.829	20.310

POPF: postoperative pancreatic fistula.

Table 5.

Binary multivariate analysis: risk factors for post-PD POPF grades B/C.

	p	OR	95% CI		p	OR	95% CI
WBII	0.141	1.729	0.835	3.581
PPBII	0.260	1.692	0.653	2.917
WRYGJ	0.811	0.887	0.334	2.361
Wirsung duct <3 mm	0.001	3.518	1.648	7.509	<0.001	3.604	1.791	7.254
Hard pancreas	0.442	0.749	0.359	1.565

Discussion

A variety of research has been published comparing two gastrointestinal reconstruction techniques after PD; such as three randomized clinical trials,^6,12,17 four retrospective comparative studies,^10,14
–16 and two meta-analyses.^13,19 The outcomes of the different reconstructive techniques after PD are very discordant. The argument to use an isolated Roux-en-Y pancreatojejunostomy versus BII reconstruction has been to divert the biliary secretion away from the pancreatic secretion to prevent activation of pancreatic enzymes by biliary secretion³⁰ with the intention to reduce the incidence of POPF and its subsequent risk of mortality,³¹ whereas the reason to use an isolated Roux-en-Y gastrojejunostomy after PD is to reduce the biliary and pancreatic reflux that can theoretically minimize the rate of DGE.^14
–17

The pathophysiology of DGE is not clearly known, being attributed to a multifactorial origin, including duodenal resection associated with reduced plasma motilin concentration, vagotomy, extended lymphadenectomy, antroduodenal ischemia, intra-abdominal collections or abscesses, and relevant grade B/C POPF as the main surgical causes for that complication.^{7,14,21,26,32} On the contrary, several perioperative risk factors, such as duodenal or ampullary tumors, <3 mm Wirsung duct, soft texture of the pancreas, pancreatic steatosis, significant transfusion, prolonged operation, and no use of Wirsung stent, have been associated with the development of POPF.^33
–36

Several studies have been carried out comparing WBII with WRYGJ reconstruction to analyze the incidence of POPF and DGE as the most common and severe complication.^14
–17,19 Concerning the surgical technique of WRYGJ, a jejunal loop has been used for the pancreatic and biliary anastomoses, joining at 40–60 cm from the bilio-jejunostomy to the 30–40 cm isolated jejunal loop that comes from the gastrojejunostomy.^14,15,17 Our WRYGJ technique differs from the previously mentioned, measuring 60 cm for both jejunal loops. In agreement with other authors, we always use an antecolic position for the gastrojejunostomy because it has been associated with a significantly decreased incidence of DGE as opposed to the use of a retrocolic gastrojejunostomy position.^14,17,32 It seems that gastric emptying is favored by the straight passage of the gastric content into the jejunum under the action of gravity¹⁵ and the use of a Braun jejunojejunostomy.³⁷

In comparative studies analyzing PPBII and WBII techniques, the pancreas duct, bile duct, and duodenum or stomach are subsequently anastomosed with a jejunal loop, maintaining a jejunal length of 60–70 cm from biliary to gastric anastomosis.^17,25

Several studies comparing WRYGJ with WBII or pyloric resection-BII have shown similarity of the preoperative variables between the groups,^14,15,17 also finding no significant differences regarding operation time, blood transfusion,¹⁴ and postoperative mortality.^14,16,17 However, the overall and clinically relevant incidence of DGE was significantly higher in two series of WBII patients,^15,16 lower in one,¹⁴ and equal in the remaining.¹⁷ In regard to the incidence of POPF, there was only one study that showed significantly lower incidence in patients with WRYGJ versus BII reconstruction,¹⁵ being the incidence similar in three other studies.^14,16,17 Two recent meta-analyses did not show statistically significant differences between both reconstruction techniques in terms of the incidence of POPF, bile leak, intra-abdominal abscess, and the length of hospital stay,^19,38 except for the significantly lower incidence of relevant grade B/C DGE and shorter operation time in BII reconstruction.³⁸ Moreover, no significant differences between the groups were demonstrated regarding the incidence of DGE, operative time, blood transfusion, and overall morbimortality in one of those meta-analyses.¹⁹

Controversial results are also seen in comparative studies between PPBII and WBII reconstruction techniques. Thus, PPBII has been associated with a significant reduction in surgery time and intraoperative bleeding,²² although other authors did not find significant differences.^20,23

Nevertheless, as has been previously referred,^14,17,19 the duration of surgery and blood transfusion were similar among our three groups. In addition, the rates of soft pancreas and <3 mm Wirsung duct were higher in group WRYGJ, but without statistically significance. Nevertheless, both characteristics have been confirmed by several authors as risk factors for POPF.^35,36 In line with the results of other authors,¹ our multivariate analysis showed that a <3-mm Wirsung duct was a risk factor for POPF grade B/C.

A theoretical advantage of WBII over PPBII has been suggested due to a better oncological resection that also avoids duodenal ischemia.²⁰ Our study did not reveal significant differences among the groups regarding histological features, except for the lower number of lymph nodes resected in PPBII, although the degree of tumoral invasion of lymph nodes was similar among the groups, demonstrating that the Whipple technique does not add any oncological advantages over the remaining techniques. Nevertheless, in the presence of massive pancreatic tumors, the choice of WBII over PPBII technique can be justified by getting a more extended resection yet having similar morbimortality for both techniques.²⁰

No significant differences were observed among the groups concerning TNM-staging. In three comparative studies, the incidence of DGE has been significantly higher in PPBII than in WBII,^21,22,24 although the other three studies did not find significant differences.^8,20,23 However, the presence of relevant POPF grade B/C has been pointed out as a risk factor for DGE.^7,32 According to previous reports comparing PPBII with WBII techniques, there have not been observed significant differences concerning the incidence of POPF,^20,23,24 postoperative morbidity, hospital stay,^22,23,37 and long-term survival.^20,22,39 Similarly, our study also revealed no significant differences among the groups concerning postoperative medical and surgical complications. The most severe complications such as relevant B/C POPF and relevant B/C DGE were higher but insignificant in the group WBII. In addition, no significant differences were observed among our groups regarding hospital stay, morbimortality at 90 days, and long-term survival, both in malignant and non-malignant tumors. In addition, a recent review of five reconstruction techniques following PD for pancreatic tumors after Roux-en-Y gastric bypass did not find evidence for the best technique of resection and reconstruction technique.⁴⁰

The retrospective nature of this study shows some limitations and is consequently subject to bias. Future prospective randomized studies with large sample sizes are necessary to demonstrate the best reconstruction technique after PD.

Conclusion

The present study did not find significant differences among the three compared reconstruction techniques after PD. Of note, we observed in multivariate analysis that relevant POPF B/C was a risk factor for DGE B/C and <3 mm Wirsung duct for a POPF. Prospective randomized studies are needed to demonstrate the superiority of one technique over the others, considering future studies to demonstrate a reconstruction technique with lesser bilio-gastric reflux that can improve the quality of life.

Footnotes

Acknowledgements

The authors acknowledge Dr Clara Fernández for the drawing of reconstruction procedures and Dr Paula Rioja for her contribution to the acquisition of data.

Author contributions

I.J.A. and C.J.-R. contributed to study conception and design, acquisition of data, analysis and interpretation of data, manuscript writing, drafting the work, and review and approval of the final version. All authors contributed to study conception and design, acquisition of data, drafting the work, and approval of the final version.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Ethical approval

The study was conducted according to the Helsinki Declaration and approved by the Institutional Review Board.

Informed consent

All study participants provided informed written consent before surgery.

ORCID iD

Iago Justo Alonso

Data statement

Data are available from the corresponding author upon request.

References

Wang

, et al: External versus internal pancreatic duct drainage for the early efficacy after pancreaticoduodenectomy: A retrospectively comparative study. J Invest Surg 2016;29(4):226–233.

Jang

Chang

Kim

, et al: Randomized multicentre trial comparing external and internal pancreatic stenting during pancreaticoduodenectomy. Br J Surg 2016;103(6):668–675.

Shin

Jang

Chang

, et al: Comparison of long-term clinical outcomes of external and internal pancreatic stents in pancreaticoduodenectomy: Randomized controlled study. HPB (Oxford) 2019;21(1):51–59.

Pessaux

Sauvanet

Mariette

, et al: External pancreatic duct stent decreases pancreatic fistula rate after pancreaticoduodenectomy: Prospective multicenter randomized trial. Ann Surg 2011;253(5):879–885.

Zhang

, et al: Internal versus external drainage with a pancreatic duct stent for pancreaticojejunostomy during pancreaticoduodenectomy for patients at high risk for pancreatic fistula: A comparative study. J Surg Res 2018;232:247–256.

Tani

Kawai

Hirono

, et al: Randomized clinical trial of isolated Roux-e-Y versus conventional reconstruction after pancreaticoduodenectomy. Br J Surg 2014;101:1084–1091.

Robinson

Marincola

Shelton

, et al: Peri-operative risk factors for delayed gastric emptying after a pancreaticoduodenectomy. HPB (Oxford) 2015;17(6):495–501.

Fahlbusch

Luu

Höhn

, et al: Impact of pylorus preservation on delayed gastric emptying after pancreaticoduodenectomy—analysis of 5,000 patients based on the German StuDoQ/Pancreas-Registry. Gland Surg 2022;11(1):67–76.

Machado

da Cunha

Bacchella

, et al: A modified technique for the reconstruction of the alimentary tract after pancreaticoduodenectomy. Surg Gynecol Obstet 1976;143:271–272.

10.

Kaman

Sanyal

Behera

, et al: Isolated Roux loop pancreaticojejunostomy vs single loop pancreaticojejunostomy after pancreaticoduodenectomy. Int J Surg 2008;6(4):306–310.

11.

Perwaiz

Singhal

Singh

, et al: Is isolated Roux loop pancreaticojejunostomy superior to conventional reconstruction in pancreaticoduodenectomy? HPB (Oxford) 200;11(4):326–331.

12.

Ding

Gao

, et al: A prospective, randomized trial of Roux-en-Y reconstruction with isolated pancreatic drainage versus conventional loop reconstruction after pancreatidoduodenectomy. Surgery 2013;153:743–752.

13.

Klaiber

Probst

Knebel

, et al: Meta-analysis of complication rates for single-loop versus dual-loop (Roux-en-Y) with isolated pancreaticojejunostomy reconstruction after pancreaticoduodenectomy. Br J Surg 2015;102(4):331–340.

14.

Shimoda

Kubota

Katoh

, et al: Effect of Billroth II or Roux-en-Y reconstruction for the gastrojejunostomy on delayed gastric emptying after pancreaticoduodenectomy: A randomized controlled study. Ann Surg 2013;257:938–942.

15.

Barakat

Cagigas

Bozorgui

, et al: Proximal Roux-en-Y gastrojejunal anastomosis with pyloric ring resection improves gastric emptying after pancreaticoduodenectomy. J Gastrointest Surg 2016;20(5):914–923.

16.

Ben-Ishay

Zhaya

Kluger

: Dual loop (Roux en Y) reconstruction with isolated gastric limb reduces delayed gastric emptying after pancreatico-duodenectomy. World J Gastrointest Surg 2019;11:93–100.

17.

Busquets

Martín

Fabregat

, et al: Randomized trial of two types of gastrojejunostomy after pancreatoduodenectomy and risk of delayed gastric emptying (PAUDA trial). Br J Surg 2019;106(1):46–54.

18.

Smyrniotis

Parasyris

Gemenetzis

, et al: Severity of pancreatic leak in relation to gut restoration after pancreaticoduodenectomy. Ann Surg Open 2022;3(2):e161.

19.

Mobarak

Tarazi

Davé

, et al: Roux-en-Y versus single loop reconstruction in pancreaticoduodenectomy: A systematic review and meta-analysis. Int J Surg 2021;88:105923.

20.

Busquets

Martín

Secanella

, et al: Delayed gastric emptying after classical Whipple or pylorus-preserving pancreatoduodenectomy: A randomized clinical trial (QUANUPAD). Langenbecks Arch Surg 2022;407(6):2247–2258.

21.

Kawai

Tani

Hirono

, et al: Pylorus ring resection reduces delayed gastric emptying in patients undergoing pancreatoduodenectomy: A prospective, randomized, controlled trial of pylorus-resecting versus pylorus-preserving pancreatoduodenectomy. Ann Surg 2011;253(3):495–501.

22.

Yang

Chen

, et al: Pylorus-preserving versus pylorus-resecting pancreaticoduodenectomy for periampullary and pancreatic carcinoma: A meta-analysis. PLoS ONE 2014;9(3):e90316.

23.

Hackert

Probst

Knebel

, et al: Pylorus resection does not reduce delayed gastric emptying after partial pancreatoduodenectomy. A blinded randomized controlled trial (PROPP Study, DRKS00004191). Ann Surg 2018;217:1021–1027.

24.

Lee

Hur

Kim

, et al: Is delayed gastric emptying associated with pylorus ring preservation in patients undergoing pancreaticoduodenectomy? Asian J Surg 2021;44(1):137–142.

25.

Jiménez Romero

Alonso Murillo

Rioja Conde

, et al: Pancreaticoduodenectomy and external Wirsung stenting: Our outcomes in 80 cases. Cir Esp 2021;99(6):440–449.

26.

Wente

Bassi

Dervenis

, et al: Delayed gastric emptying (DGE) after pancreatic surgery: A suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 2007;142(5):761–768.

27.

Bassi

Marchegiani

Dervenis

, et al: The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 years after. Surgery 2017;161(3):584–591.

28.

Wente

Veit

Bassi

, et al: Postpancreatectomy hemorrhage (PPH)-An International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery 2007;142(1):20–25.

29.

Clavien

Barkun

de Oliveira

, et al: The Clavien-Dindo classification of surgical complications: Five-year experience. Ann Surg 2009;250(2):187–196.

30.

Nakamura

Okada

Higaki

, et al: Pancreatobiliary maljunction-associated pancreatitis: An experimental study on the activation of pancreatic phospholipase A2. World J Surg 1996;20:543–550.

31.

Kawamoto

Konomi

Kobayashi

, et al: Type of gastrointestinal reconstruction affects postoperative recovery after pancreatic head resection. J Hepatobiliary Pancreat Surg 2006;13(4):336–343.

32.

El Nakeeb

Askr

Mahdy

, et al: Delayed gastric emptying after pancreaticoduodenectomy. Risk factors, predictors of severity and outcome. A single center experience of 588 cases. J Gastrointest Surg 2015;19(6):1093–1100.

33.

Pratt

Callery

Vollmer

Jr : Risk prediction for development of pancreatic fistula using the ISGPF classification scheme. World J Surg 2008;32(3):419–428.

34.

Motoi

Egawa

Rikiyama

, et al: Randomized clinical trial of external stent drainage of the pancreatic duct to reduce postoperative pancreatic fistula after pancreaticojejunostomy. Br J Surg 2012;99(4):524–531.

35.

Callery

Pratt

Kent

, et al: A prospectively validated clinical risk score accurately predicts pancreatic fistula after pancreatoduodenectomy. J Am Coll Surg 2013;216(1):1–14.

36.

McMillan

Vollmer

Jr Asbun

, et al: The characterization and prediction of ISGPF grade C fistulas following pancreatoduodenectomy. J Gastrointest Surg 2016;20(2):262–276.

37.

Zhang

Yin

Liu

, et al: Does Braun enteroenterostomy reduce delayed gastric emptying after pancreaticoduodenectomy? Medicine (Baltimore) 2014;93(7):e48.

38.

Xiao

Hao

Yang

, et al: Effect of Billroth-II versus Roux-en-Y reconstruction for gastrojejunostomy after pancreaticoduodenectomy on delayed gastric emptying: A meta-analysis of randomized controlled trials. J Hepatobiliary Pancreat Sci 2021;28(5):397–408.

39.

Hüttner

Fitzmaurice

Schwarzer

, et al: Pylorus-preserving pancreaticoduodenectomy (pp Whipple) versus pancreaticoduodenectomy (classic Whipple) for surgical treatment of periampullary and pancreatic carcinoma. Cochrane Database Syst Rev 2016;2:CD006053.

40.

Morano

Shaikh

Gleeson

, et al: Reconstruction options following pancreaticoduodenectomy after Roux-en-Y gastric bypass: A systematic review. World J Surg Oncol 2018;16:168.

Comparison of reconstruction techniques after pancreatoduodenectomy: A single-center retrospective cohort study

Abstract

Background:

Methods:

Results:

Conclusion:

Keywords

Context and Relevance

Introduction

Patients and methods

Study design and patient recruitment

Study endpoints

Surgical techniques

Postoperative management

Definitions

Statistical analysis

Ethical aspects

Results

Discussion

Conclusion

Footnotes

Acknowledgements

Author contributions

Declaration of conflicting interests

Funding

Ethical approval

Informed consent

ORCID iD

Data statement

References