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A preserved pancreatic exocrine function after pancreatectomy may be a crucial cause of pancreatic fistula: paradoxical results of the 13C-trioctanoin breath test in the perioperative period

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Abstract

Purpose

The aim of this study was to elucidate the association between pancreatic fistula (PF) and the sequential changes in the perioperative exocrine function after pancreatectomy.

Methods

The subjects were 96 patients who underwent a 13C-trioctanoin breath test before and 1 month after pancreatectomy, between 2006 and 2018. We retrospectively compared the pre- and postoperative fat absorption levels between patients with PF (PF group; n = 17) and without PF (non-PF group; n = 79) using the breath test.

Results

The preoperative level of 13C-trioctanoin absorption (%dose/h) was comparable between the non-PF and PF groups (36.5 vs. 36.9). In the non-PF group, 13C-trioctanoin absorption was significantly decreased after surgery in comparison to the preoperative setting (post-operative 28.5; pre-operative 36.5; p < 0.0001), whereas these values were comparable (post-operative 36.9; pre-operative 34.5; p = 0.129) in the PF group. Moreover, postoperative absorption in the PF group was significantly better than that in the non-PF group (34.5 vs. 28.5%, p = 0.0003). The maximum drain amylase level was significantly higher in patients with a 13C-trioctanoin absorption level (%dose/h) of ≥ 30 in comparison to patients with levels of < 30 (2502 vs. 398 U/L, p = 0.001).

Conclusion

PF did not exacerbate the pancreatic exocrine function in the early postoperative period, and the acceleration or preservation of the exocrine function after surgery may be an important cause of PF.

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Data availability

All the data generated or analyzed during this study are included within the article.

References

  1. Kawai M, Kondo S, Yamaue H, Wada K, Sano K, Motoi F, et al. Predictive risk factors for clinically relevant pancreatic fistula analyzed in 1239 patients with pancreaticoduodenectomy: multicenter data collection as a project study of pancreatic surgery by the Japanese Society of Hepato-Biliary-Pancreatic Surgery. J Hepatobiliary Pancreat Sci. 2011;18(4):601–8.

    Article  Google Scholar 

  2. Kusafuka T, Kato H, Iizawa Y, Noguchi D, Gyoten K, Hayasaki A, et al. Pancreas-visceral fat CT value ratio and serrated pancreatic contour are strong predictors of postoperative pancreatic fistula after pancreaticojejunostomy. BMC Surg. 2020;20(1):129.

    Article  Google Scholar 

  3. Sugimoto M, Takahashi S, Kojima M, Kobayashi T, Gotohda N, Konishi M. In patients with a soft pancreas, a thick parenchyma, a small duct, and fatty infiltration are significant risks for pancreatic fistula after pancreaticoduodenectomy. J Gastrointest Surg. 2017;21(5):846–54.

    Article  Google Scholar 

  4. Yasuda H, Takada T, Toyota N, Amano H, Yoshida M, Takada Y, et al. Limited pancreatectomy: significance of postoperative maintenance of pancreatic exocrine function. J Hepatobiliary Pancreat Surg. 2000;7(5):466–72.

    Article  CAS  Google Scholar 

  5. Horiguchi A, Miyakawa S, Ishihara S, Ito M, Asano Y, Furusawa K, et al. Surgical design and outcome of duodenum-preserving pancreatic head resection for benign or low-grade malignant tumors. J Hepatobiliary Pancreat Sci. 2010;17(6):792–7.

    Article  Google Scholar 

  6. Ito K. Duodenum preservation in pancreatic head resection to maintain pancreatic exocrine function (determined by pancreatic function diagnostant test and cholecystokinin secretion). J Hepatobiliary Pancreat Surg. 2005;12(2):123–8.

    Article  Google Scholar 

  7. Yamaguchi K, Yokohata K, Nakano K, Ohtani K, Ogawa Y, Chijiiwa K, et al. Which is a less invasive pancreatic head resection: PD, PPPD, or DPPHR? Dig Dis Sci. 2001;46(2):282–8.

    Article  CAS  Google Scholar 

  8. Kato H, Nakao A, Kishimoto W, Nonami T, Harada A, Hayakawa T, et al. 13C-labeled trioctanoin breath test for exocrine pancreatic function test in patients after pancreatoduodenectomy. Am J Gastroenterol. 1993;88(1):64–9.

    CAS  PubMed  Google Scholar 

  9. Giuliani T, Andrianello S, Bortolato C, Marchegiani G, De Marchi G, Malleo G, et al. Preoperative fecal elastase-1 (FE-1) adds value in predicting post-operative pancreatic fistula: not all soft pancreas share the same risk—a prospective analysis on 105 patients. HPB (Oxford). 2020;22(3):415–21.

    Article  Google Scholar 

  10. Wali PD, Loveridge-Lenza B, He Z, Horvath K. Comparison of fecal elastase-1 and pancreatic function testing in children. J Pediatr Gastroenterol Nutr. 2012;54(2):277–80.

    Article  CAS  Google Scholar 

  11. Kang JH, Park JS, Yu JS, Chung JJ, Kim JH, Cho ES, et al. Prediction of pancreatic fistula after pancreatoduodenectomy by preoperative dynamic CT and fecal elastase-1 levels. PLoS ONE. 2017;12(5):e0177052.

    Article  Google Scholar 

  12. Hirono S, Murakami Y, Tani M, Kawai M, Okada K, Uemura K, et al. Identification of risk factors for pancreatic exocrine insufficiency after pancreaticoduodenectomy using a 13C-labeled mixed triglyceride breath test. World J Surg. 2015;39(2):516–25.

    Article  Google Scholar 

  13. Bassi C, Marchegiani G, Dervenis C, Sarr M, Hilal MA, Adham M, 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):584–91.

    Article  Google Scholar 

  14. Miyakawa S, Hayakawa M, Horiguchi A, Mizuno K, Ishihara S, Niwamoto N, et al. Estimation of fat absorption with the 13C-trioctanoin breath test after pancreatoduodenectomy or pancreatic head resection. World J Surg. 1996;20(8):1024–8 (discussion 8-9).

    Article  CAS  Google Scholar 

  15. Miyakawa S, Niwamoto N, Horiguchi A, Hanai T, Mizuno K, Ishihara S, et al. Fat absorption after pylorus-preserving pancreatoduodenectomy reconstructed with Billroth II pancreaticojejunostomy or Billroth I pancreaticogastrostomy. Hepatogastroenterology. 2000;47(31):264–8.

    CAS  PubMed  Google Scholar 

  16. Mews P, Phillips P, Fahmy R, Korsten M, Pirola R, Wilson J, et al. Pancreatic stellate cells respond to inflammatory cytokines: potential role in chronic pancreatitis. Gut. 2002;50(4):535–41.

    Article  CAS  Google Scholar 

  17. Roshani R, McCarthy F, Hagemann T. Inflammatory cytokines in human pancreatic cancer. Cancer Lett. 2014;345(2):157–63.

    Article  CAS  Google Scholar 

  18. Hirono S, Kawai M, Okada KI, Miyazawa M, Kitahata Y, Hayami S, et al. Modified Blumgart mattress suture versus conventional interrupted suture in pancreaticojejunostomy during pancreaticoduodenectomy: randomized controlled trial. Ann Surg. 2019;269(2):243–51.

    Article  Google Scholar 

  19. Satoi S, Yamamoto T, Yanagimoto H, Yamaki S, Kosaka H, Hirooka S, et al. Does modified Blumgart anastomosis without intra-pancreatic ductal stenting reduce post-operative pancreatic fistula after pancreaticojejunostomy? Asian J Surg. 2019;42(1):343–9.

    Article  Google Scholar 

  20. Fujii T, Yamada S, Murotani K, Sugimoto H, Hattori M, Kanda M, et al. Modified Blumgart suturing technique for remnant closure after distal pancreatectomy: a propensity score-matched analysis. J Gastrointest Surg. 2016;20(2):374–84.

    Article  Google Scholar 

  21. Fujii T, Sugimoto H, Yamada S, Kanda M, Suenaga M, Takami H, et al. Modified Blumgart anastomosis for pancreaticojejunostomy: technical improvement in matched historical control study. J Gastrointest Surg. 2014;18(6):1108–15.

    Article  Google Scholar 

  22. Wallace CL, Georgakis GV, Eisenberg DP, Macaulay WP, Jimenez RE. Further experience with pancreatic stump closure using a reinforced staple line. Conn Med. 2013;77(4):205–10.

    PubMed  Google Scholar 

  23. Ferrone CR, Warshaw AL, Rattner DW, Berger D, Zheng H, Rawal B, et al. Pancreatic fistula rates after 462 distal pancreatectomies: staplers do not decrease fistula rates. J Gastrointest Surg. 2008;12(10):1691–7 (discussion 7-8).

    Article  Google Scholar 

  24. Azumi Y, Isaji S, Kato H, Nobuoka Y, Kuriyama N, Kishiwada M, et al. A standardized technique for safe pancreaticojejunostomy: pair-watch suturing technique. World J Gastrointest Surg. 2010;2(8):260–4.

    Article  Google Scholar 

  25. Azumi Y, Isaji S. Stented pancreaticojejunostomy (with video). J Hepatobiliary Pancreat Sci. 2012;19(2):116–24.

    Article  Google Scholar 

  26. Maemura K, Mataki Y, Kurahara H, Tanoue K, Kawasaki Y, Ijichi T, et al. The 1-year outcomes after pancreaticogastrostomy using vertical versus horizontal mattress suturing for gastric wrapping. Surg Today. 2020;51:511–9.

    Article  Google Scholar 

  27. Eguchi H, Iwagami Y, Matsushita K, Tomimaru Y, Akita H, Noda T, et al. Randomized clinical trial of pancreaticogastrostomy versus pancreaticojejunostomy regarding incidence of delayed gastric emptying after pancreaticoduodenectomy. Langenbecks Arch Surg. 2020;405(7):921–8.

    Article  Google Scholar 

  28. Kawai M, Yamaue H, Jang J-Y, Uesaka K, Unno M, Nakamura M, et al. Propensity score-matched analysis of internal stent vs external stent for pancreatojejunostomy during pancreaticoduodenectomy: Japanese-Korean cooperative project. Pancreatology. 2020;20(5):984–91.

    Article  Google Scholar 

  29. Tani M, Kawai M, Hirono S, Ina S, Miyazawa M, Shimizu A, et al. A prospective randomized controlled trial of internal versus external drainage with pancreaticojejunostomy for pancreaticoduodenectomy. Am J Surg. 2010;199(6):759–64.

    Article  Google Scholar 

  30. Casadei R, Ricci C, Ingaldi C, Alberici L, De Raffele E, Minni F. Comparison of Blumgart anastomosis with duct-to-mucosa anastomosis and invagination pancreaticojejunostomy after pancreaticoduodenectomy: a single-center propensity score matching analysis. J Gastrointest Surg. 2020;25:411–20.

    Article  Google Scholar 

  31. Schrempf M, Anthuber M. Pancreaticojejunostomy: duct-to-mucosa anastomosis or invagination anastomosis? Chirurg. 2019;90:68 (Suppl 2).

    Article  CAS  Google Scholar 

  32. Lyu Y, Li T, Wang B, Cheng Y, Zhao S. Selection of pancreaticojejunostomy technique after pancreaticoduodenectomy: duct-to-mucosa anastomosis is not better than invagination anastomosis: a meta-analysis. Medicine (Baltimore). 2018;97(40):e12621.

    Article  Google Scholar 

  33. Van Buren G, Vollmer CM. The landmark series: mitigation of the postoperative pancreatic fistula. Ann Surg Oncol. 2020;28:1052–9.

    Article  Google Scholar 

  34. Williams ST, Woltering EA, O’Dorisio TM, Fletcher WS. Effect of octreotide acetate on pancreatic exocrine function. Am J Surg. 1989;157(5):459–62.

    Article  CAS  Google Scholar 

Download references

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Authors and Affiliations

  1. Department of Gastroenterological Surgery, Bantane Hospital, Fujita Health University School of Medicine, Nagoya, Japan

    Takahiko Higashiguchi, Hiroyuki Kato, Hironobu Yasuoka, Masahiro Ito, Yukio Asano, Norihiko Kawabe, Satoshi Arakawa, Masahiro Shimura, Daisuke Koike, Chihiro Hayashi, Takayuki Ochi, Kenshiro Kamio, Toki Kawai, Toshiaki Utsumi, Hidetoshi Nagata, Yuka Kondo, Daisuke Tochii & Akihiko Horiguchi

Authors
  1. Takahiko Higashiguchi
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  2. Hiroyuki Kato
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Correspondence to Hiroyuki Kato.

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Takahiko Higashiguchi and the other co-authors declare no conflicts of interest in association with the present study.

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Higashiguchi, T., Kato, H., Yasuoka, H. et al. A preserved pancreatic exocrine function after pancreatectomy may be a crucial cause of pancreatic fistula: paradoxical results of the 13C-trioctanoin breath test in the perioperative period. Surg Today 52, 580–586 (2022). https://doi.org/10.1007/s00595-021-02371-w

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