Skip to main content
Download PDF

Subtotal gastrectomy pancreaticoduodenectomy versus conventional pancreaticoduodenectomy in the incidence of delayed gastric emptying: single-center retrospective cohort study

BMC Surgery volume 22, Article number: 376 (2022) Cite this article

Abstract

Background

Delayed gastric emptying (DGE) is one of the most common complications after pancreaticoduodenectomy (PD). There is currently no widely accepted procedure for PD to reduce the incidence of DGE. Our institution attempts to perform subtotal gastrectomy in patients undergoing PD to reduce DGE. Here we aimed to evaluate the effectiveness and safety of PD with subtotal gastric resection.

Methods

Patients who underwent PD between January 2014 and December 2021 were reviewed. They were stratified by extent of gastrectomy into a conventional PD group (PD that resected approximately 1/3 of the distal stomach) and a subtotal gastrectomy PD group (PD that resected approximately 3/4 of the distal stomach), which were compared in terms of intraoperative and postoperative parameters.

Result

From January 2014 to December 2021, a total of 512 patients underwent PD in the Department of Hepatobiliary Surgery, Peking University People’s Hospital. Nineteen patients were excluded from this study due to benign disease. A total of 493 patients were included, with 378 in the conventional PD group and 115 in the subtotal gastrectomy PD group. Compared with the conventional PD group, the subtotal gastrectomy PD group had a lower incidence of DGE (8.7% vs. 17.7%, p = 0.019), and a shorter hospital stay. Multivariate analysis showed that conventional PD and higher body mass index were independent risk factors for grade B/C DGE.

Conclusion

This study showed that, compared with conventional PD, subtotal gastrectomy PD can reduce the incidence of DGE and shorten the length of hospital stay. At the same time, subtotal gastrectomy PD is comparable to conventional PD in terms of surgical safety. Furthermore, high BMI is an independent risk factor for postoperative DGE.

Peer Review reports

Introduction

Pancreaticoduodenectomy (PD) is used for the treatment of pancreatic head cancer, cholangiocarcinoma, ampullary carcinoma and duodenal carcinoma [1]. Despite advances in surgical techniques for PD, there is a high rate of postoperative complications, including delayed gastric emptying (DGE), pancreatic fistula, hemorrhage, biliary fistula and abdominal infection [2]. DGE is one of the most common complications after PD, with an incidence of approximately 17.5–56.0% [3, 4]. DGE does not directly cause the death of patients. However, prolonged feeding difficulty after surgery increases the patients’ hospital stay and medical costs.

The mechanism of DGE is currently not fully understood. Researchers attempted to explain DGE from different perspectives, such as smooth muscle dysfunction, enteric nervous system damage, pyloric sphincter disorder, oxidative distress and inflammation [5].

Surgeons have been working to improve surgical techniques for PD to reduce the incidence of postoperative gastric emptying disorders. However, it is currently unclear which surgical approach can reduce the incidence of DGE. In the past, surgeons believed that the incidence of DGE was related to the method for digestive tract reconstruction and whether the pylorus was preserved [6,7,8]. Few studies have investigated the association between the extent of gastrectomy and the incidence of DGE after PD. Since 2014, our institution has performed subtotal gastrectomy in some patients undergoing PD. Here we aimed to evaluate the effectiveness and safety of PD with subtotal gastric resection.

Materials and methods

Population

Patients who underwent PD at the Department of Hepatobiliary Surgery, Peking University People’s Hospital from January 2015 to December 2021 were reviewed. Patients who underwent PD for benign disease were excluded. According to the extent of distal gastrectomy, the subjects were divided into a conventional PD group (PD that resected approximately 1/3 of the distal stomach) and a subtotal gastrectomy PD group (PD that resected approximately 3/4 of the distal stomach). Surgical notes in the medical record system describe the extent of distal gastrectomy in PD. The following parameters were included as possible confounders: age, sex, body mass index (BMI), American Society of Anesthesiologists (ASA) grade, preoperative comorbidities, and site of lesion. The following parameters were compared: operative time, blood loss, incidence of complications, hospital stay and number of in-hospital deaths.

Surgery

Except for the extent of gastrectomy, conventional PD and subtotal gastrectomy PD have the same surgical procedures. Roux-en-y or child surgery was used to reconstruct the digestive tract. Conventional PD surgery removes approximately 1/3 of the distal end of the stomach. The resection line for the stomach is located just above the gastric antrum. Subtotal gastrectomy PD removes the distal 3/4 of the stomach. The resection line crosses the second branch of the left gastric artery and the avascular area on the left side of the stomach (Fig. 1)

Fig. 1
figure 1

Illustration of the two PD. a Conventional PD removes approximately 1/3 of the distal end of the stomach. The resection line for the stomach is located just above the gastric antrum. b Subtotal gastrectomy PD removes the distal 3/4 of the stomach. The resection line crosses the second branch of the left gastric artery and the avascular area on the left side of the stomach

Full size image

Definition of DGE

According to the definition by the International Study Group of Pancreatic Surgery [9], grade A DGE was defined as a patient requiring retention of the nasogastric tube for 4–7 days after surgery, 8–14 days for grade B DGE, and more than 14 days for grade C DGE.

Postoperative management

After surgery, when the drainage volume of gastrointestinal decompression was less than 150 ml per day, the nasogastric tube was removed. Abdominal drainage fluid amylase was regularly monitored daily for 5 days after surgery. After the patient’s gastrointestinal tract recovered peristalsis, liquid food would be admitted. Semi-liquid and solid foods would be gradually allowed according to patient tolerance.

Statistical analysis

Data were analyzed in Statistical Package for the Social Sciences version 21.0. When a continuous variable conformed to a normal distribution, the variable was expressed as mean ± standard deviation. Otherwise, the variable was expressed with the median and interquartile range. Continuous variables between groups were compared by Student’s t-test and Mann–Whitney U test according to whether they were normally distributed. Categorical variables were analyzed by chi-square test. Univariate and multivariable logistic regression was used to assess the risk factor on outcome. Variables with p values less than 0.05 were included in the multivariable logistic regression analysis. P values less than 0.05 were considered significant.

Results

Baseline characteristics

From January 2015 to December 2019, a total of 512 patients underwent PD at the Department of Hepatobiliary Surgery, Peking University People’s Hospital. Nineteen patients were excluded from the study due to postoperative pathology confirmed to be benign. A total of 493 patients were included in this study.

The baseline information of the patients is shown in Table 1. Of the 493 patients, 378 patients underwent conventional PD with distal 1/3 gastric resection, and 115 patients underwent subtotal gastrectomy PD with distal 2/3 gastric resection. There were no significant differences in any baseline information between the conventional PD group and the subtotal gastrectomy PD group (Table 1).

Table 1 Baseline characteristics
Full size table

Intraoperative and postoperative parameters

The intraoperative and postoperative parameters are shown in Table 2. Compared with the conventional PD group, the subtotal gastrectomy PD group had a lower incidence of grade B/C DGE and a shorter hospital stay. There were no differences in other parameters (Table 2). No patient died intraoperatively. Nineteen patients (3.7%) died during postoperative hospitalization. Four patients died of pneumonia; four patients died of abdominal infection; and five patients died of gastrointestinal bleeding or intra-abdominal bleeding. Four patients died of pancreatic fistula. One patient died of biliary fistula; one person died of thromboembolism.

Table 2 Intraoperative and postoperative parameters
Full size table

Univariate and multivariate logistic regression analysis of the risk factors for DGE

To identify the risk factors for DGE, we performed univariate and multivariate logistic regression analyses. The univariate analysis identified conventional PD and high BMI as risk factors for grade B or C DGE. In the multivariate logistic regression, conventional PD and high BMI were independent risk factors for grade B/C DGE (Table 3).

Table 3 univariate and multivariate analyses of risk factors for delayed DGE (B/C)
Full size table

Discussion

Previous study reported that subtotal gastrectomy has a lower incidence of DGE of only 3.1% [10]. Thus, we hypothesized that a less remnant stomach might lead to a lower incidence of DGE and attempted subtotal gastrectomy for PD. Conventional PD surgery requires removal of approximately 1/3 of the distal stomach. Compared with conventional PD, subtotal gastrectomy PD removes approximately 3/4 of the stomach. Several investigators have reported that the subtotal gastrectomy in PD surgery may reduce the incidence of postoperative DGE. Yusuke et al. compared the incidence of DGE between subtotal stomach-preserving PD and antrectomy-combined PD and finally concluded that antrectomy-combined PD leads to a lower incidence of DGE. Philip et al. [11] reported that 4/5 gastrectomy in patients undergoing PD reduces the incidence of DGE. Toshihiko et al. [12]. reported that Roux-en-Y reconstruction following gastric cancer was more frequently followed by Roux stasis in the antrum than in the midstomach.

Our study compared the short-term outcomes of subtotal gastrectomy PD and conventional PD. Compared with conventional PD, subtotal gastrectomy PD resulted in a lower incidence of DGE B/C (17.7% vs. 8.7%) and a shorter hospital stay. This result is similar to previous studies. Due to the lower incidence of DGE, subtotal gastrectomy PD had a shorter hospital stay. Subtotal gastrectomy PD was similar to conventional PD in terms of intraoperative bleeding, operative time and in-hospital mortality. This means that although PD removed more stomach, it did not increase the morbidity and mortality of patients.

Currently, DGE is thought to be mainly caused by pyloric dysfunction and impairment of the propulsive action of the stomach [13]. Some publications have reported that pylorus-resecting PD results in a lower incidence of DGE than pylorus-preserving PD [6, 14]. The elimination of pyloric dysfunction caused by pyloric resection may be the reason for the lower incidence of DGE in pyloric-resecting PD. Additionally, the smaller remnant stomach volume increases the mechanical stimulation of the stomach by food, which can promote the vago-vagal reflex and the local reflex of the intramural plexus, thereby enhancing gastric peristalsis and promoting gastric emptying [15].

Our study did not analyze the long-term quality of life of patients after PD. Yusuke et al. compared the nutritional status after PD between the antrectomy-combined PD group and the subtotal stomach-preserving PD group. The nutritional status of the two groups at 3, 6, and 12 months after surgery was comparable. Santoro et al. reported that most patients who underwent subtotal gastrectomy showed no significant difference in long-term quality of life after surgery compared with preoperative patients [16]. Philip et al. reported that subtotal gastrectomy PD patients with subtotal gastrectomy lost more body weight 1.5 months after surgery than conventional PD patients. However, there was no significant difference in weight loss between the two groups at 3 months and 6 months after surgery. Additionally, most of the patients who received PD in our center did not complain of obvious discomfort in the postoperative outpatient follow-up. Therefore, our center initially believes that subtotal gastrectomy PD has little adverse effect on the long-term quality of life of patients.

In the multivariate regression analysis, conventional PD and elevated BMI were risk factors for DGE. Previous studies have also confirmed that high BMI is associated with an increased risk of DGE [17, 18]. A high BMI can lead to the accumulation of fat around the patient’s organs, which increases the difficulty of PD surgery.

In addition to conventional PD and subtotal gastrectomy PD, pylorus-preserving PD is the standard of care in many institutions. Many studies have reported that pylorus-preserving PD can reduce operating time, intraoperative blood loss and postoperative hospital stay compared with conventional PD [19, 20]. However, some studies reported that pylorus-preserving PD increased the incidence of postoperative complications, DGE21, 22]. Which surgical approach maximizes patient benefit may require further research.

This study preliminarily confirmed that subtotal gastric resection of PD can effectively reduce the incidence of postoperative DGE, and the level of safety is similar to that of conventional PD. However, the study still has some limitations, as it was a single-center, retrospective cohort study. Further multicenter prospective studies are needed in the future. Additionally, further long-term quality of life assessments should be conducted in future investigations.

Conclusion

This study showed that, compared with conventional PD, subtotal gastrectomy PD can reduce the incidence of DGE and shorten the length of hospital stay. At the same time, subtotal gastrectomy PD is comparable to conventional PD in terms of surgical safety. Furthermore, high BMI is an independent risk factor for postoperative DGE. The long-term quality of life in patients who undergo subtotal gastrectomy PD requires further study.

Availability of data and materials

The datasets analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

PD:

Pancreaticoduodenectomy

DGE:

Delayed gastric emptying

BMI:

Body mass index

ASA:

American Society of Anesthesiologists

References

  1. Ausania F, Landi F, Martínez-Pérez A, Fondevila C. A meta-analysis of randomized controlled trials comparing laparoscopic vs open pancreaticoduodenectomy. HPB (Oxford). 2019;21(12):1613–20. https://doi.org/10.1016/j.hpb.2019.05.017.

    Article  Google Scholar 

  2. Simon R. Complications after pancreaticoduodenectomy. Surg Clin North Am. 2021;101(5):865–74. https://doi.org/10.1016/j.suc.2021.06.011.

    Article  PubMed  Google Scholar 

  3. Grossi S, Lin A, Wong A, Namm J, Senthil M, Gomez N, Reeves M, Garberoglio C, Solomon N. Costs and complications: delayed gastric emptying after pancreaticoduodenectomy. Am Surg. 2019;85(12):1423–8.

    Article  PubMed  Google Scholar 

  4. Cai X, Zhang M, Liang C, Xu Y, Yu W. Delayed gastric emptying after pancreaticoduodenectomy: a propensity score-matched analysis and clinical Nomogram study. BMC Surg. 2020;20(1):149. https://doi.org/10.1186/s12893-020-00809-5.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Camilleri M, Chedid V, Ford AC, Haruma K, Horowitz M, Jones KL, Low PA, Park SY, Parkman HP, Stanghellini V. Gastroparesis. Nat Rev Dis Primers. 2018;4(1):41. https://doi.org/10.1038/s41572-018-0038-z.

    Article  PubMed  Google Scholar 

  6. Lee YH, Hur YH, Kim HJ, Kim CY, Kim JW. Is delayed gastric emptying associated with pylorus ring preservation in patients undergoing pancreaticoduodenectomy? Asian J Surg. 2021;44(1):137–42. https://doi.org/10.1016/j.asjsur.2020.08.012.

    Article  PubMed  Google Scholar 

  7. Imamura M, Kimura Y, Ito T, Kyuno T, Nobuoka T, Mizuguchi T, Hirata K. Effects of antecolic versus retrocolic reconstruction for gastro/duodenojejunostomy on delayed gastric emptying after pancreatoduodenectomy: a systematic review and meta-analysis. J Surg Res. 2016;200(1):147–57. https://doi.org/10.1016/j.jss.2015.08.004.

    Article  PubMed  Google Scholar 

  8. Schorn S, Demir IE, Vogel T, Schirren R, Reim D, Wilhelm D, Friess H, Ceyhan GO. Mortality and postoperative complications after different types of surgical reconstruction following pancreaticoduodenectomy—a systematic review with meta-analysis. Langenbecks Arch Surg. 2019;404(2):141–57. https://doi.org/10.1007/s00423-019-01762-5.

    Article  PubMed  Google Scholar 

  9. Wente MN, Bassi C, Dervenis C, Fingerhut A, Gouma DJ, Izbicki JR, Neoptolemos JP, Padbury RT, Sarr MG, Traverso LW, 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):761–8. https://doi.org/10.1016/j.surg.2007.05.005.

    Article  PubMed  Google Scholar 

  10. Paik HJ, Choi CI, Kim DH, Jeon TY, Kim DH, Son GM, Lee SH, Hwang SH. Risk factors for delayed gastric emptying caused by anastomosis edema after subtotal gastrectomy for gastric cancer. Hepatogastroenterology. 2014;61(134):1794–800.

    PubMed  Google Scholar 

  11. Müller PC, Ruzza C, Kuemmerli C, Steinemann DC, Müller SA, Kessler U, Z’Graggen K. 4/5 Gastrectomy in patients undergoing pancreaticoduodenectomy reduces delayed gastric emptying. J Surg Res. 2020;249:180–5. https://doi.org/10.1016/j.jss.2019.12.028.

    Article  PubMed  Google Scholar 

  12. Masui T, Kubora T, Nakanishi Y, Aoki K, Sugimoto S, Takamura M, Takeda H, Hashimoto K, Tokuka A. The flow angle beneath the gastrojejunostomy predicts delayed gastric emptying in Roux-en-Y reconstruction after distal gastrectomy. Gastric Cancer. 2012;15(3):281–6. https://doi.org/10.1007/s10120-011-0107-4.

    Article  PubMed  Google Scholar 

  13. Camilleri M, Sanders KM. Gastroparesis. Gastroenterology. 2022;162(1):68–87. https://doi.org/10.1053/j.gastro.2021.10.028.

    Article  CAS  PubMed  Google Scholar 

  14. Hackert T, Hinz U, Hartwig W, Strobel O, Fritz S, Schneider L, Werner J, Büchler MW. Pylorus resection in partial pancreaticoduodenectomy: impact on delayed gastric emptying. Am J Surg. 2013;206(3):296–9. https://doi.org/10.1016/j.amjsurg.2012.10.042.

    Article  PubMed  Google Scholar 

  15. Travagli RA, Hermann GE, Browning KN, Rogers RC. Musings on the wanderer: what’s new in our understanding of vago-vagal reflexes? III. Activity-dependent plasticity in vago-vagal reflexes controlling the stomach. Am J Physiol Gastrointest Liver Physiol. 2003;284(2):G180–7. https://doi.org/10.1152/ajpgi.00413.2002.

    Article  CAS  PubMed  Google Scholar 

  16. Santoro R, Mancini P, Carboni F, Lepiane P, Ettorre GM, Santoro E. Subtotal gastrectomy for gastric cancer: long term outcomes of Billroth I reconstruction at a single European institute. Hepatogastroenterology. 2014;61(136):2448–54.

    CAS  PubMed  Google Scholar 

  17. Snyder RA, Ewing JA, Parikh AA. Delayed gastric emptying after pancreaticoduodenectomy: a study of the national surgical quality improvement program. Pancreatology. 2020;20(2):205–10. https://doi.org/10.1016/j.pan.2019.12.003.

    Article  PubMed  Google Scholar 

  18. Matsumoto S, Wakatsuki K, Migita K, Ito M, Nakade H, Kunishige T, Kitano M, Nakatani M, Sho M. Predictive factors for delayed gastric emptying after distal gastrectomy with Roux-en-Y reconstruction. Am Surg. 2018;84(6):1086–90.

    Article  PubMed  Google Scholar 

  19. Calderon E, Day RW, Stucky CC, Gray RJ, Pockaj BA, Chang YH, Wasif N. Comparative effectiveness of pylorus-preserving versus standard pancreaticoduodenectomy in clinical practice. Pancreas. 2020;49(4):568–73. https://doi.org/10.1097/mpa.0000000000001524.

    Article  PubMed  Google Scholar 

  20. Hüttner FJ, Fitzmaurice C, Schwarzer G, Seiler CM, Antes G, Büchler MW, Diener MK. Pylorus-preserving pancreaticoduodenectomy (pp Whipple) versus pancreaticoduodenectomy (classic Whipple) for surgical treatment of periampullary and pancreatic carcinoma. Cochrane Database Syst Rev. 2016;2(2):Cd006053. https://doi.org/10.1002/14651858.CD006053.pub6.

    Article  PubMed  Google Scholar 

  21. Lin PW, Shan YS, Lin YJ, Hung CJ. Pancreaticoduodenectomy for pancreatic head cancer: PPPD versus Whipple procedure. Hepatogastroenterology. 2005;52(65):1601–4.

    PubMed  Google Scholar 

  22. Zhou Y, Lin L, Wu L, Xu D, Li B. A case-matched comparison and meta-analysis comparing pylorus-resecting pancreaticoduodenectomy with pylorus-preserving pancreaticoduodenectomy for the incidence of postoperative delayed gastric emptying. HPB (Oxford). 2015;17(4):337–43. https://doi.org/10.1111/hpb.12358.

    Article  Google Scholar 

Download references

Acknowledgements

We thank all surgeons involved in the treatment of patients included in the study.

Funding

Supported by: Peking University People’s Hospital Scientific Research Development Funds (RDY2017-28).

Author information

Authors and Affiliations

  1. Department of Hepatobiliary Surgery, Peking University People’s Hospital, No. 11 Xizhimen South Street, Xicheng District, Beijing, 100044, China

    Jinzhu Zhang, Shu Li, Weihua Zhu, Xisheng Leng, Jie Gao & Dafang Zhang

Authors
  1. Jinzhu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Weihua Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xisheng Leng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jie Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dafang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JZ designed the study, acquired and analyzed the data, and drafted the work. DZ and JG designed the study, revised the paper, and supervised the study. SL, WZ and XL acquired and analyzed the data, and revised the paper. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Jie Gao or Dafang Zhang.

Ethics declarations

Ethics approval and consent to participate

This study was approved by the institutional review board of Peking University People’s hospital (Approval No. 2022PHB 197-001). We informed all patients included in the trial and obtained their informed consent. This study was conducted in accordance with the Declaration of Helsinki.

Consent for publication

Not applicable.

Competing interests

All authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, J., Li, S., Zhu, W. et al. Subtotal gastrectomy pancreaticoduodenectomy versus conventional pancreaticoduodenectomy in the incidence of delayed gastric emptying: single-center retrospective cohort study. BMC Surg 22, 376 (2022). https://doi.org/10.1186/s12893-022-01824-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12893-022-01824-4

Keywords

BMC Surgery

ISSN: 1471-2482

Contact us