DOI QR코드

DOI QR Code

Impact of soft pancreas on pancreaticoduodenectomy outcomes and the development of the preoperative soft pancreas risk score

  • Received : 2024.09.05
  • Accepted : 2024.11.04
  • Published : 2025.02.28

Abstract

Backgrounds/Aims: Pancreatic texture is difficult to predict without palpation. Soft pancreatic texture is associated with increased post-operative complications, including postoperative pancreatic fistula (POPF), cardiac, and respiratory complications. We aimed to develop a calculator predicting pancreatic texture using patient factors and to illustrate complications from soft pancreatic texture following pancreaticoduodenectomy. Methods: Data was collected from the 2016 to 2021 American College of Surgeons National Surgical Quality Improvement database including 17,706 pancreaticoduodenectomy cases. Patients were categorized into two cohorts based on pancreatic texture (9,686 hard, 8,020 soft). Multivariable modeling assessed the impact of patient factors on complications, mortality, and pancreatic texture. These preoperative factors were integrated into a risk calculator (preoperative soft pancreas risk score [PSPRS]) that predicts pancreatic texture. Results: Patients with a soft pancreas had higher rates of postoperative complications compared to those with a hard pancreas (56.5% vs 42.2%; p < 0.001), particularly a threefold increase in POPF rate, and at least a twofold increase in rates of acute kidney injury, deep organ space infection, septic shock, and prolonged length of stay. Female sex (odds ratio [OR]: 1.14, confidence interval [CI]: 1.06-1.22, p < 0.001) and higher body mass index (OR: 1.12, CI: 1.09-1.16, p < 0.001) were independently associated with a soft pancreas. PSPRS ≥6 correctly identified >40% of patients preoperatively as having a hard pancreas (68.9% specificity). Conclusions: A soft pancreas was independently associated with serious postoperative complications. Our results were integrated into a risk calculator predicting pancreatic texture from preoperative patient factors, potentially enhancing preoperative counseling and surgical decision-making.

Keywords

Acknowledgement

American College of Surgeons National Surgical Quality Improvement Program and the hospitals involved in the ACS NSQIP are sources of the data utilized in this study; they have neither verified nor bear responsibility for the statistical validity of the data analysis or the conclusions drawn by the authors. This research was exempt from ethics review.

References

  1. Hong TH, Choi JI, Park MY, Rha SE, Lee YJ, You YK, et al. Pancreatic hardness: Correlation of surgeon's palpation, durometer measurement and preoperative magnetic resonance imaging features. World J Gastroenterol 2017;23:2044-2051. https://doi.org/10.3748/wjg.v23.i11.2044
  2. Zhang JY, Huang J, Zhao SY, Liu X, Xiong ZC, Yang ZY. Risk factors and a new prediction model for pancreatic fistula after pancreaticoduodenectomy. Risk Manag Healthc Policy 2021;14:1897-1906. https://doi.org/10.2147/RMHP.S305332
  3. Mahvi DA, Pak LM, Urman RD, Gold JS, Whang EE. Discharge destination following pancreaticoduodenectomy: a NSQIP analysis of predictive factors and post-discharge outcomes. Am J Surg 2019;218:342-348. https://doi.org/10.1016/j.amjsurg.2018.11.043
  4. Luu AM, Olchanetski B, Herzog T, Tannapfel A, Uhl W, Belyaev O. Is primary total pancreatectomy in patients with high-risk pancreatic remnant justified and preferable to pancreaticoduodenectomy? -A matched-pairs analysis of 200 patients. Gland Surg 2021;10:618-628. https://doi.org/10.21037/gs-20-670
  5. Zhu F, Wang M, Wang X, Tian R, Shi C, Xu M, et al. Modified technique of pancreaticogastrostomy for soft pancreas with two continuous hemstitch sutures: a single-center prospective study. J Gastrointest Surg 2013;17:1306-1311. https://doi.org/10.1007/s11605-013-2183-8
  6. Kazantsev GB, Spitzer AL, Peng PD, Ramirez RM, Chang CK, Tsai S, et al. Pancreaticogastrostomy as a fistula mitigating strategy for a high-risk pancreatic anastomosis following pancreaticoduodenectomy. HPB (Oxford) 2023;25:124-135. https://doi.org/10.1016/j.hpb.2022.10.003
  7. Poon RT, Fan ST, Lo CM, Ng KK, Yuen WK, Yeung C, et al. External drainage of pancreatic duct with a stent to reduce leakage rate of pancreaticojejunostomy after pancreaticoduodenectomy: a prospective randomized trial. Ann Surg 2007;246:425-433; discussion 433-425. https://doi.org/10.1097/SLA.0b013e3181492c28
  8. Hallet J, Theodosopoulos E, Abou-Khalil J, Bertens K, Pelletier JS, Segedi M, et al. Prevention of postoperative pancreatic fistula after pancreatectomy: results of a Canadian RAND/UCLA appropriateness expert panel. Can J Surg 2022;65:E135-E142. https://doi.org/10.1503/cjs.001520
  9. Kambakamba P, Mannil M, Herrera P, Linecker M, Müller P, Kümmerli C, et al. Machine learning based texture analysis predicts postoperative pancreatic fistula in preoperative non-contrast enhanced computed tomography. HPB 2020;22(Suppl 2):S384. https://doi.org/10.1016/j.hpb.2020.04.432
  10. Tirkes T, Yadav D, Conwell DL, Territo PR, Zhao X, Venkatesh SK, et al. Magnetic resonance imaging as a non-invasive method for the assessment of pancreatic fibrosis (MINIMAP): a comprehensive study design from the consortium for the study of chronic pancreatitis, diabetes, and pancreatic cancer. Abdom Radiol (NY) 2019;44:2809-2821. https://doi.org/10.1007/s00261-019-02049-5
  11. Kolbinger FR, Lambrecht J, Leger S, Ittermann T, Speidel S, Weitz J, et al. The image-based preoperative fistula risk score (preFRS) predicts postoperative pancreatic fistula in patients undergoing pancreatic head resection. Sci Rep 2022;12:4064. https://doi.org/10.1038/s41598-022-07970-2
  12. Tang B, Lin Z, Ma Y, Zhang A, Liu W, Zhang J, et al. A modified alternative fistula risk score (a-FRS) obtained from the computed tomography enhancement pattern of the pancreatic parenchyma predicts pancreatic fistula after pancreatoduodenectomy. HPB (Oxford) 2021;23:1759-1766. https://doi.org/10.1016/j.hpb.2021.04.015
  13. American College of Surgeons (ACS). ACS NSQIP participant usedata file [Internet]. ACS 2022 [cited 2024 Feb 1]. Available from: https://www.facs.org/quality-programs/data-and-registries/acsnsqip/participant-use-data-file/.
  14. Pulvirenti A, Ramera M, Bassi C. Modifications in the International Study Group for Pancreatic Surgery (ISGPS) definition of postoperative pancreatic fistula. Transl Gastroenterol Hepatol 2017;2:107. https://doi.org/10.21037/tgh.2017.11.14
  15. Liu X. Classification accuracy and cut point selection. Stat Med 2012;31:2676-2686. https://doi.org/10.1002/sim.4509
  16. Kalayarasan R, Himaja M, Ramesh A, Kokila K. Radiological parameters to predict pancreatic texture: Current evidence and future perspectives. World J Radiol 2023;15:170-181. https://doi.org/10.4329/wjr.v15.i6.170
  17. Callery MP, Pratt WB, Kent TS, Chaikof EL, Vollmer CM, Jr. A prospectively validated clinical risk score accurately predicts pancreatic fistula after pancreatoduodenectomy. J Am Coll Surg 2013;216:1-14. https://doi.org/10.1016/j.jamcollsurg.2012.09.002
  18. Hayashibe A, Kameyama M. Duct-to-mucosa pancreaticojejunostomies with a hard pancreas and dilated pancreatic duct and duct-to-mucosa pancreaticojejunostomies with a soft pancreas and non-dilated duct. HPB (Oxford) 2008;10:54-57. https://doi.org/10.1080/13651820701883130
  19. Yang YM, Tian XD, Zhuang Y, Wang WM, Wan YL, Huang YT. Risk factors of pancreatic leakage after pancreaticoduodenectomy. World J Gastroenterol 2005;11:2456-2461. https://doi.org/10.3748/wjg.v11.i16.2456
  20. Agalianos C, Paraskeva K, Gouvas N, Davides D, Dervenis C. Impact of biliary stenting on surgical outcome in patients undergoing pancreatectomy. A retrospective study in a single institution. Langenbecks Arch Surg 2016;401:55-61. https://doi.org/10.1007/s00423-015-1360-5
  21. Zechner D, Knapp N, Bobrowski A, Radecke T, Genz B, Vollmar B. Diabetes increases pancreatic fibrosis during chronic inflammation. Exp Biol Med (Maywood) 2014;239:670-676. https://doi.org/10.1177/1535370214527890
  22. Kopljar M, Čoklo M, Krstačić A, Krstačić G, Jeleč V, Zovak M, et al. Retrorenal fat predicts grade C pancreatic fistula after pancreaticoduodenectomy. ANZ J Surg 2020;90:2472-2477. https://doi.org/10.1111/ans.16147
  23. Shamali A, Shelat V, Jaber B, Wardak A, Ahmed M, Fontana M, et al. Impact of obesity on short and long term results following a pancreatico-duodenectomy. Int J Surg 2017;42:191-196. https://doi.org/10.1016/j.ijsu.2017.04.058
  24. Ramsey AM, Martin RC. Body mass index and outcomes from pancreatic resection: a review and meta-analysis. J Gastrointest Surg 2011;15:1633-1642. https://doi.org/10.1007/s11605-011-1502-1
  25. Lee JM, Kim HS, Lee M, Park HS, Kang S, Nahm JH, et al. Association between pancreatic fibrosis and development of pancreoprivic diabetes after pancreaticoduodenectomy. Sci Rep 2021;11:23538. https://doi.org/10.1038/s41598-021-02858-z
  26. Erstad DJ, Sojoodi M, Taylor MS, Jordan VC, Farrar CT, Axtell AL, et al. Fibrotic response to neoadjuvant therapy predicts survival in pancreatic cancer and is measurable with collagen-targeted molecular MRI. Clin Cancer Res 2020;26:5007-5018. https://doi.org/10.1158/1078-0432.CCR-18-1359
  27. Moten AS. Fibrosis following neoadjuvant treatment of PDAC: less is not always more. Am J Surg 2024;232:8. https://doi.org/10.1016/j.amjsurg.2023.12.001
  28. Mungroop TH, Klompmaker S, Wellner UF, Steyerberg EW, Coratti A, D'Hondt M, et al.; European Consortium on Minimally Invasive Pancreatic Surgery (E-MIPS). Updated alternative fistula risk score (ua-FRS) to include minimally invasive pancreatoduodenectomy: pan-european validation. Ann Surg 2021;273:334-340. https://doi.org/10.1097/SLA.0000000000003234
  29. Wang M, Gorelick F, Bhargava A. Sex differences in the exocrine pancreas and associated diseases. Cell Mol Gastroenterol Hepatol 2021;12:427-441. https://doi.org/10.1016/j.jcmgh.2021.04.005
  30. Schuh F, Mihaljevic AL, Probst P, Trudeau MT, Müller PC, Marchegiani G, et al. A simple classification of pancreatic duct size and texture predicts postoperative pancreatic fistula: a classification of the International Study Group of Pancreatic Surgery. Ann Surg 2023;277:e597-e608. https://doi.org/10.1097/SLA.0000000000004855
  31. Verdeyen N, Gryspeerdt F, Abreu de Carvalho L, Dries P, Berrevoet F. A comparison of preoperative predictive scoring systems for postoperative pancreatic fistula after pancreaticoduodenectomy based on a single-center analysis. J Clin Med 2024;13:3286. https://doi.org/10.3390/jcm13113286
  32. Balzano G, Zerbi A, Aleotti F, Capretti G, Melzi R, Pecorelli N, et al. Total pancreatectomy with islet autotransplantation as an alternative to high-risk pancreatojejunostomy after pancreaticoduodenectomy: a prospective randomized trial. Ann Surg 2023;277:894-903. https://doi.org/10.1097/SLA.0000000000005713
  33. Gueroult S, Parc Y, Duron F, Paye F, Parc R. Completion pancreatectomy for postoperative peritonitis after pancreaticoduodenectomy: early and late outcome. Arch Surg. 2004;139:16-19. https://doi.org/10.1001/archsurg.139.1.16
  34. Marchegiani G, Perri G, Burelli A, Zoccatelli F, Andrianello S, Luchini C, et al. High-risk pancreatic anastomosis versus total pancreatectomy after pancreatoduodenectomy: postoperative outcomes and quality of life analysis. Ann Surg 2022;276:e905-e913. https://doi.org/10.1097/SLA.0000000000004840
  35. Stoop TF, Ghorbani P, Scholten L, Bergquist E, Ateeb Z, van Dieren S, et al. Total pancreatectomy as an alternative to high-risk pancreatojejunostomy after pancreatoduodenectomy: a propensity score analysis on surgical outcome and quality of life. HPB (Oxford) 2022;24:1261-1270. https://doi.org/10.1016/j.hpb.2021.12.018
  36. Rykina-Tameeva N, Nahm CB, Mehta S, Gill AJ, Samra JS, Mittal A. Neoadjuvant therapy for pancreatic cancer changes the composition of the pancreatic parenchyma. HPB (Oxford) 2020;22:1631-1636. https://doi.org/10.1016/j.hpb.2020.03.007
  37. Deig CR, Sutton TL, Beneville B, Trone K, Stratton A, Gunesch AN, et al. Neoadjuvant therapy is associated with improved chemotherapy delivery and overall survival compared to upfront resection in pancreatic cancer without increasing perioperative complications. Cancers (Basel) 2022;14:609. https://doi.org/10.3390/cancers14030609
  38. Rompen IF, Merz DC, Alhalabi KT, Klotz R, Kalkum E, Pausch TM, et al. Perioperative drug treatment in pancreatic surgery-a systematic review and meta-analysis. J Clin Med 2023;12:1750. https://doi.org/10.3390/jcm12051750