Abstract
Backgrounds/Aims
Pancreaticoduodenectomy (PD) is the standard treatment for resectable tumors of the pancreatic head, ampulla, distal bile duct, and duodenum. Despite advances, delayed gastric emptying (DGE) remains a common complication. Feeding jejunostomy (FJ) is often used during PD, though its necessity and association with increased morbidity, particularly DGE, remain controversial. This study aimed to evaluate early postoperative outcomes in PD patients with or without FJ, focusing on DGE and related complications.
Methods
This prospective observational study was conducted from August 2022 to April 2024 and included 56 patients (28 with FJ, 28 without). Primary outcomes were DGE, postoperative pancreatic fistula (POPF), and hospital stay. Secondary outcomes included FJ-related complications, surgical site infections, and time to tolerate solid food. Statistical analysis was performed using SPSS v28.
Results
DGE was significantly more frequent in the FJ group (78.6% vs. 39.3%, p = 0.006). Clinically relevant DGE (grades B/C) was also higher with FJ (60.7% vs. 21.4%, p = 0.008). FJ-related complications, including intestinal obstruction requiring reoperation, occurred in 10.7% of patients. Time to tolerate solid food and hospital stay were longer in the FJ group. Multivariate analysis identified FJ use and perioperative blood transfusion as independent risk factors for DGE.
Conclusions
Routine FJ placement in PD is associated with increased DGE and tube-related complications. A selective approach to FJ may improve postoperative outcomes. Larger multicenter randomized trials are needed to validate these findings and develop clear guidelines for FJ use in PD.
Keywords: Pancreaticoduodenectomy, Delayed gastric emptying, Feeding jejunostomy, Whipple procedure
INTRODUCTION
Pancreaticoduodenectomy (PD) is considered the treatment of choice for resectable tumors located in the head of the pancreas, ampulla, distal common bile duct and duodenum [1]. Surgical mortality following PD is reduced to 1% in high volume centers in the current decade [2]. However, morbidities following the procedure remain as high as 30% to 45% [3] Complications commonly seen after PD include delayed gastric emptying (DGE), pancreatic fistula, and surgical site infection (SSI). It is evident from the literature that early enteral feeding in the postoperative period can reduce infectious complications, improve wound healing, and shorten the length of hospital stay [4,5].
Early oral feeding is the simplest and the best natural way to start enteral nutrition. It has become feasible in most of Whipple’s procedures. DGE following PD is a hindrance to early oral feeding that needs to be addressed. Insertion of FJ intraoperatively is routinely practiced in many centers around the world to combat DGE. However, in the last decade, a few studies have raised questions regarding routine FJ insertion and given evidence that it is associated with increased morbidity following PD [6-8]. Using American College of Surgeons-National Surgical Quality Improvement Program (ACS-NSQIP) data from 15,154 PD patients, Werba et al. [9] have identified feeding jejunostomy (FJ) as a key independent risk factor among others for clinically significant DGE in the PrEDICT-DGE scoring model.
In a recent survey done among Indian hepato-pancreato-biliary surgeons (n = 110) who routinely perform PD, the majority (94.5%) of them prefer to create feeding access during operation while early oral feeding is favored only by 37.3% of surgeons [10]. Studies that favor routine use of FJ and those that do not favor FJ are mostly retrospective. Prospective studies on the use of FJ in PD are also observational studies without randomization. Hence, the evidence is not sufficient to give strong recommendations regarding routine placement of FJ in PD. Additionally, data on patients undergoing Whipple procedure without FJ is sparse in the Indian subcontinent.
Thus, the aim of this study was to analyze early surgical outcomes following PD among patients with FJ and those without FJ. The choice of placing FJ is at the surgeon’s discretion in our institute. We have two groups of surgeons. One group performs FJ routinely while the other does not perform any routine operative enteral access such as FJ or NJ. Hence, we decided to perform a prospectively study of postoperative outcomes between these two groups of patients.
MATERIALS AND METHODS
This prospective observational comparative study was conducted between August 2022 and April 2024, with the aim of evaluating early postoperative outcomes in patients undergoing PD with or without FJ. A sample size of a minimum 50 patients (25 patients in each group) was proposed. The decision to place a FJ was at the discretion of the surgeon. In our institute, we have two groups of surgeons. One group routinely places FJ for all PD patients and the other group does not do FJ along with PD. FJ was done by the Witzel technique using a 12-Fr feeding tube. Patients were enrolled from the day of surgery. Their postoperative progress was monitored until discharge, with a 90-day follow-up either physically or virtually.
Primary outcomes included DGE, postoperative pancreatic fistula (POPF), duration of hospital stay, and FJ tube-related complications. Complications following PD were graded according to the ISGPS (International Study Group of Pancreatic Surgery) guidelines. Details are mentioned in the Supplementary Table 1 and 2. Secondary outcomes encompassed deep and superficial SSIs, hemorrhage, time to tolerate solid food, need for total parenteral nutrition (TPN) post-surgery, and mortality. Patients over 18 years of age who underwent PD during the study period with or without FJ placement were included. Those undergoing additional procedures such as hepato-pancreatoduodenectomy were excluded.
The sample size was determined based on the following formula (N = z2pq/d2; Z = standard normal variant = 1.96, p = 0.093, Q = 1-p = 0.907 based on a prior study [6], d = clinically allowable error, 8%), ensuring a minimum of 50 patients. Statistical analyses were performed using SPSS software (ver. 28.0, IBM Corp.). Descriptive statistics (mean ± standard deviation, frequency, and percentage) was used for continuous and categorical variables. For non-normally distributed data, median and interquartile range (interquartile range) are presented. Student’s t-test or Mann–Whitney U test was used to compare continuous variables. Chi-square or Fisher’s exact test was used for categorical comparisons. A p-value < 0.05 was considered statistically significant.
RESULTS
A total of 56 patients underwent PD during the study period. FJ was placed in 28 patients. Demographically, age, BMI, glycaemic status, pancreatic duct size, pancreatic texture, and pathological diagnosis showed no significant differences between the two groups (Table 1). Clinical outcomes were similar, including 90-day mortality (3.57%), postoperative pancreaticoduodenal hemorrhage (7.1%), reoperation (7.1% vs. 3.57%, p > 0.99), and TPN usage (17.9% vs. 21.4%) for both groups (Table 2). Although length of stay was longer at 13.6 ± 6.7 days for the FJ group and 11.6 ± 6.3 days for the non-FJ group, the difference was not statistically significant (p = 0.1). However, the incidence of clinically significant DGE (grade B/C) was significantly higher in the FJ group (60.7% vs. 21.4%, p = 0.008). FJ tube related morbidities were seen in three patients, with 2 of them requiring reoperations. Patients in the non-FJ arm were free from tube-related morbidities.
Table 1.
Demographics of patients in FJ and non-FJ groups
| Demography | FJ (n = 28) | Non-FJ (n = 28) | p value |
|---|---|---|---|
| Age | 0.312 | ||
| < 60 | 13 (46.4) | 16 (57.1) | |
| ≥ 60 | 15 (53.6) | 12 (42.9) | |
| Sex | 0.582 | ||
| Male | 16 (57.1) | 19 (67.9) | |
| Female | 12 (42.9) | 9 (32.1) | |
| Body mass index | 0.545 | ||
| Underweight | - | 1 (3.6) | |
| Normal | 16 (57.1) | 17 (60.7) | |
| Overweight | 12 (42.9) | 10 (35.7) | |
| Diabetes mellitus | 14 (50.0) | 14 (50.0) | > 0.99 |
| Pancreatic duct size | 0.375 | ||
| Diameter ≤ 3 mm | 6 (21.4) | 10 (35.7) | |
| Diameter > 3 mm | 22 (78.6) | 18 (64.3) | |
| Pancreatico gastrostomy | 7 (25.0) | - | - |
| Pancreatico jejunostomy | 21 (75.0) | 28 (100) | |
| Pancreatic texture | 0.423 | ||
| Soft | 12 (42.9) | 16 (57.1) | |
| Firm | 16 (57.1) | 12 (42.9) | |
| Preoperative biliary drainage | 6 (21.4) | 9 (32.1) | 0.547 |
| Pathological diagnosis | 0.781 | ||
| Malignancy | 25 (89.2) | 23 (82.1) | |
| Benign | 3 (10.8) | 5 (17.9) |
Values are presented as number (%).
FJ, feeding jejunostomy.
Table 2.
Comparison of short-term outcomes between FJ and non-FJ groups
| Outcome | FJ (n = 28) | Non-FJ (n = 28) | p value |
|---|---|---|---|
| 90-day mortality | 1 (3.57) | 1 (3.57) | > 0.99 |
| DGE | 22 (78.6) | 11 (39.3) | 0.006* |
| Clinically significant DGE (grade B, C) | 17 (60.7) | 6 (21.4) | 0.008* |
| POPF | 11 (39.3) | 9 (32.2) | 0.59 |
| PPDH | 2 (7.1) | 2 (7.1) | > 0.99 |
| SSI | 9 (32.1) | 8 (28.6) | 0.99 |
| Length of stay (day) | 13.6 ± 6.7 | 11.6 ± 6.3 | 0.1 |
| Time to tolerate solid diet (day) | 14.9 ± 7.3 | 11.5 ± 7.3 | 0.07 |
| Reoperation | 2 (7.1) | 1 (3.57) | > 0.99 |
| FJ-related complications | 3 (10.6) | 0 (0) | - |
| TPN usage | 5 (17.9) | 6 (21.4) | > 0.99 |
| ICU stay | 3 (10.7) | 4 (14.3) | > 0.99 |
Values are presented as number (%) or mean ± standard deviation.
FJ, feeding Jejunostomy; DGE, delayed gastric emptying; POPF, postoperative pancreatic fistula; PPDH, post pancreato duodenectomy hemorrhage; SSI, surgical site infection; TPN, total parenteral nutrition; ICU, intensive care unit.
*Statistically significant (p < 0.05).
Since multiple factors are associated with DGE, a multivariate analysis of those factors was done in our study. We found that patients without FJ (odds ratio [OR]: 0.1, 95% confidence interval [95% CI]: 0.02–0.4, p = 0.002) and those did not receive perioperative blood transfusion (OR: 0.03, 95% CI: 0.03–0.3, p = 0.003) were associated with a significantly reduced risk of DGE. Multivariate analysis of all factors suspected to be associated with POPF showed that patients with firm pancreatic texture and main pancreatic duct diameter ≥ 3 mm had a lower chance of getting POPF (p = 0.01).
DISCUSSION
Does FJ increase DGE?
In our study, we found that the DGE rate was twice more common in the FJ group than in the non-FJ group (78.6% vs. 39.3%, p = 0.006). This result was similar to the study by Waliye et al. [7] showing that the DGE rate was twice as common among patients with jejunostomy tubes (66.7% vs. 33%, p = 0.003). The incidence of clinically significant DGE (grades B and C) was even higher in our study (60.7% vs. 21.4%) than in the study of Waliye et al. [7] (37.9% vs. 17.5%). The meta-analysis by Vasavada and Patel [11], the retrospective cohort study by Zeinalpour et al. [12], and the retrospective analysis of various enteral feeding routes following PD by Gerritsen et al. [13] also showed a higher DGE incidence among patients with FJ. However, the meta-analysis published in 2020 [14] and the prospective study by Hassan et al. [15] showed that enteral nutrition using FJ was not associated with an increased risk of DGE. The DGE incidence with naso-jejunal tube placement was very low (6%) in the data from the Tata Memorial Centre reported by Shrikhande et al. [16].
The available literature stands divided with respect to the usage of FJ tube and its association with DGE. In patients with severe DGE (grade C) who require prolonged nutrition support, using FJ tube has an advantage of providing nutrition via the enteral route, which is of vital importance in these select groups of patients. However, due to reduced complications following PD in the last two decades with enhanced recovery plan, routine placement of FJ tube is a dilemma. Preoperatively defined set criteria are currently not set for FJ placement. It was at the surgeon’s discretion in our study. Data comparing DGE rates and time to tolerate a solid diet orally between our study and recent studies in the literature were compared. Results are presented in Table 3.
Table 3.
Comparison of DGE rates and time to tolerate solid diet between FJ and non-FJ groups among various studies
| Study | DGE (FJ) | DGE (non-FJ) | Time to solid diet (FJ) | Time to solid diet (non-FJ) |
|---|---|---|---|---|
| Waliye et al., 2016 [7] | 102/153 (66.7) | 34/103 (33%) | 9.4 ± 6.3 | 7.3 ± 5.8 |
| Li et al., 2019 [22] | 8/33 (24.2) | 7/36 (22.2%) | NA | NA |
| Vasavada and Patel, meta-analysis 2021 [11] | 117/222 (52.7) | 44/175 (25.1%) | Time to solid diet was more in FJ group. Weighted mean difference of 2.4 days. (p < 0.0001) | |
| Zeinalpour et al., 2022 [12] | 14/20 (70.0) | 23/28 (82.1%) | 6.4 ± 3.8 | 5.4 ± 2.0 |
| Current study 2024 | 22/28 (78.6) | 11/28 (39.3%) | 14.9 ± 7.3 | 11.5 ± 7.3 |
Values are presented as number (%) or mean ± standard deviation.
FJ, feeding jejunostomy; NA, not available.
The recent meta-analysis on early oral feeding after PD with a total of 553 patients concluded that it reduced the length of stay without increasing the risk of DGE or POPF. Rebelo et al. [17] in 2024 included 5,930 patients from 29 studies [18] for a meta-analysis and analyzed the impact of various interventions such as Enhanced Recovery After Surgery (ERAS), epidural anesthesia, pylorus preservation, and jejunal or nasojejunal feeding on the development of DGE. Their data showed that the DGE rate was lower in patients without a jejunal or nasojejunal tube (OR: 0.618, 95% CI: 0.39–0.84, p < 0.001). Other findings from their study, which were associated with lower DGE rates, were adherent to the ERAS strategy and pylorus resection [17]. Their meta-analysis suggests that FJ can be useful in highly selected cases while routine FJ placement may not be beneficial in PD. There was no available previous study from Indian subcontinent to compare with results of the present study.
Does diabetes mellitus increase DGE?
Diabetes mellitus is considered a risk factor associated with DGE among patients who undergo PD [19]. The proportion of patients with DM in our study was equally distributed between FJ and non-FJ groups. In our study, the overall DGE incidence among patients with DM was 53.6%, which was higher than that (16.8%) in the NSQIP study [20]. However, the incidence of clinically significant DGE (grades B and C) was less (35.7%, 10 out of 28) in our study. The NSQIP analysis published in 2020 showed that there was no difference in the rate of DGE between DM and non-DM patients after PD [20]. That study also showed that DGE had a different pathophysiology than gastroparesis in DM patients. There was no difference in DGE rate between DM and non-DM PD patients.
Can FJ itself cause problem?
Patients in the FJ arm are at risk of tube-related complications such as peri tubal infection, intraabdominal infection, tube block, and tube-related bowel obstruction [21]. FJ tube-related morbidity was seen in 10.7% (3 out of 28) of patients in the FJ arm. Two patients in this arm had intestinal obstruction secondary to the kinking of the jejunal loop around the FJ entry site, for which they had to be reoperated. Mechanical obstruction at the FJ site is very uncommon. However, the Witzel technique FJ may result in compromise of the lumen if tunneling is done by taking wide serosal sutures. The incidence of tube related complications among recent studies in the literature including our study is presented in Table 4.
Table 4.
FJ tube related complications in various studies
| Study | FJ tube related complications | Remarks from the study |
|---|---|---|
| Waliye et al., 2016 [7] | 11/153 (7.2) | FJ group had increased DGE, LOS, time to tolerate solid diet. |
| Li et al., 2019 [22] | 2/33 (6.1) | FJ may not be routinely necessary during PD. Consider it on a case by case basis |
| Vasavada and Patel, meta-analysis 2021 [11] | 23/187 (12.2) | FJ associated with increased DGE, SSI, LOS, and time to tolerate solid diet |
| Zeinalpour et al., 2022 [12] | 2/20 (10.0) | No difference with or without FJ |
| Current study 2024 | 3/28 (10.6) | FJ group had increased DGE |
Values are presented as number (%).
FJ, feeding jejunostomy; DGE, delayed gastric emptying; LOS, length of stay; SSI, surgical site infection.
This study showed chances of tube-related morbidity, which could hamper patient’s postoperative progress, result in reoperation and prolonged hospital stay, and ultimately increase the overall morbidity of the patient. Secondary outcomes such as pancreatic fistula, bleeding, and hospital stay were similar between both study groups. These were also similar in other studies [7,13,14,22].
Perioperative blood transfusion and its relation to DGE
Morris et al. performed a systematic review and meta-analysis regarding perioperative blood transfusion in major abdominal surgery and reported perioperative blood transfusion associated with increased morbidity, mortality, and infectious complications [23]. Blood transfusion was given intraoperatively or postoperatively to 28.7% of our study group. They had increased DGE (93.7% vs. 45%, p < 0.001), POPF (50% vs. 30%, p = 0.013), length of stay (16.7 ± 8.2 days vs. 10.9 ± 4.9 days, p = 0.002), and time to tolerate solid diet (16.9 ± 6.1 days vs 11.9 ± 6.3 days, p = 0.012). A retrospective data review from Johns Hopkins University has analyzed long-term outcomes following perioperative blood transfusion [24]. It was found that perioperative blood transfusion was associated with decreased median overall survival (17.2 vs. 27.4 months, p < 0.001). In the present study, we analyzed short-term outcomes alone following PD since this study was focused mainly on the role of FJ in postoperative outcomes. Intraoperative transfusion is an indirect measure of large-volume blood loss. It worsens both short-term and long-term outcomes of patients.
This study was done at a single center over 24 months without a long-term follow-up. Defined criteria for FJ placement are currently unavailable. FJ use was at the discretion of the surgeon. Variations in surgeon experience were not considered in this study. Being a non-randomized study, confounding factors might have affected study results. However, findings of this study were similar to many previous large volume studies including meta-analysis, although randomized controlled trials were not available.
Conclusions
Routine use of FJ in Whipple’s procedure might increase the risk of DGE, time to start solid food, and length of hospital stay. Tube-related complications such as peri tubal infection and intestinal obstruction could become additional burdens to patients’ postoperative courses. Perioperative blood transfusion may result in worse postoperative outcomes in terms of DGE, POPF, and length of stay. This study underscores the need for a more selective approach to FJ, guided by standardized criteria and patient-specific risk factors. However, a well-designed, multicenter RCT with a larger sample size is necessary to validate these findings and to recommend a selective approach for FJ placement.
SUPPLEMENTARY DATA
Supplementary data related to this article can be found at https://doi.org/10.14701/ahbps.25-035.
ACKNOWLEDGEMENTS
We acknowledge the department of Surgical Gastroenterology and department of anesthesiology of Apollo Hospitals, Chennai for their contribution in the management of these patients.
Funding Statement
FUNDING None.
Footnotes
CONFLICT OF INTEREST
No potential conflict of interest relevant to this article was reported.
AUTHOR CONTRIBUTIONS
Conceptualization: GSJ, SAKS, JKAJ, TGB, SKS. Data curation: GSJ, ST, JM, GC. Methodology: GSJ, SKS. Visualization: SKS. Writing - original draft: GSJ. Writing - review & editing: SAKS, JKAJ, TGB, SKS.
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