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Simple Preoperative Imaging Measurements Predict Postoperative Pancreatic Fistula After Pancreatoduodenectomy

  • Pancreatic Tumors
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Abstract

Objective

Postoperative pancreatic fistula is a potentially devastating complication after pancreatoduodenectomy (PD). The purpose of this study was to identify features on preoperative computed tomography (CT) imaging that correlate with an increased risk of postoperative pancreatic fistula (POPF).

Methods

Patients who underwent PD at our high-volume pancreatic surgery center from 2019 to 2021 were included if CT imaging was available within 8 weeks of surgical intervention. Pancreatic neck thickness (PNT), abdominal wall thickness (AWT), and intra-abdominal distance from pancreas to peritoneum (PTP) were measured by two board-certified radiologists who were blinded to the clinical outcomes. Radiographic measurements, as well as preoperative patient characteristics and intraoperative data, were assessed with univariate and multivariable analysis (MVA) to determine risk for clinically relevant POPF (CR-POPF, grades B and C).

Results

A total of 204 patients met inclusion criteria. Median PTP was 5.8 cm, AWT 1.9 cm, and PNT 1.3 cm. CR-POPF occurred in 33 of 204 (16.2%) patients. MVA revealed PTP > 5.8 cm (odds ratio [OR] 2.86, p = 0.023), PNT > 1.3 cm (OR 2.43, p = 0.047), soft pancreas consistency (OR 3.47, p = 0.012), and pancreatic duct size ≤ 3.0 mm (OR 4.55, p = 0.01) as independent risk factors for CR-POPF after PD. AWT and obesity were not associated with increased risk of CR-POPF. Patients with PTP > 5.8 cm or PNT > 1.3 cm were significantly more likely to suffer a major complication after PD (39.6% vs. 22.3% and 40% vs. 22.1%, p < 0.008).

Conclusions

Patients with a thick pancreatic neck and increased intra-abdominal girth have a heightened risk of CR-POPF after pancreatoduodenectomy, and they experience more serious postoperative complications. We defined a simple CT scan-based measurement tool to identify patients at increased risk of CR-POPF.

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References

  1. McMillan MT, Soi S, Asbun HJ, et al. Risk-adjusted outcomes of clinically relevant pancreatic fistula following pancreatoduodenectomy: a model for performance evaluation. Ann Surg. 2016;264(2):344–52. https://doi.org/10.1097/SLA.0000000000001537.

    Article  PubMed  Google Scholar 

  2. McMillan MT, Vollmer CM Jr, Asbun HJ, et al. The characterization and prediction of ISGPF Grade C fistulas following pancreatoduodenectomy. J Gastrointest Surg. 2016;20(2):262–76. https://doi.org/10.1007/s11605-015-2884-2.

    Article  PubMed  Google Scholar 

  3. 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):1–14. https://doi.org/10.1016/j.jamcollsurg.2012.09.002.

    Article  PubMed  Google Scholar 

  4. Bassi C, Marchegiani G, Dervenis C, 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. https://doi.org/10.1016/j.surg.2016.11.014.

    Article  PubMed  Google Scholar 

  5. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Ma LW, Dominguez-Rosado I, Gennarelli RL, et al. The cost of postoperative pancreatic fistula versus the cost of pasireotide: results from a prospective randomized trial. Ann Surg. 2017;265(1):11–6. https://doi.org/10.1097/SLA.0000000000001892.

    Article  PubMed  Google Scholar 

  7. Mungroop TH, Klompmaker S, GrootKoerkamp B, Besselink MG, Dutch Pancreatic Cancer G. Added value of body fat distribution in predicting clinically significant pancreatic fistula in the a-FRS following pancreatoduodenectomy currently unclear. Ann Surg. 2019;269(1):e23. https://doi.org/10.1097/SLA.0000000000002831

  8. Mungroop TH, van Rijssen LB, van Klaveren D, et al. Alternative fistula risk score for pancreatoduodenectomy (a-FRS): design and international external validation. Ann Surg. 2019;269(5):937–43. https://doi.org/10.1097/SLA.0000000000002620.

    Article  PubMed  Google Scholar 

  9. Joo I, Lee JM, Lee ES, et al. Preoperative CT classification of the resectability of pancreatic cancer: interobserver agreement. Radiology. 2019;293(2):343–9. https://doi.org/10.1148/radiol.2019190422.

    Article  MathSciNet  PubMed  Google Scholar 

  10. Zins M, Matos C, Cassinotto C. Pancreatic adenocarcinoma staging in the era of preoperative chemotherapy and radiation therapy. Radiology. 2018;287(2):374–90. https://doi.org/10.1148/radiol.2018171670.

    Article  PubMed  Google Scholar 

  11. Clavien PA, Barkun J, de Oliveira ML, et al. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg. 2009;250(2):187–96. https://doi.org/10.1097/SLA.0b013e3181b13ca2.

    Article  PubMed  Google Scholar 

  12. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240(2):205–13. https://doi.org/10.1097/01.sla.0000133083.54934.ae.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Wu W, He J, Cameron JL, et al. The impact of postoperative complications on the administration of adjuvant therapy following pancreaticoduodenectomy for adenocarcinoma. Ann Surg Oncol. 2014;21(9):2873–81. https://doi.org/10.1245/s10434-014-3722-6.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Hank T, Sandini M, Ferrone CR, et al. Association between pancreatic fistula and long-term survival in the era of neoadjuvant chemotherapy. JAMA Surg. 2019;154(10):943–51. https://doi.org/10.1001/jamasurg.2019.2272.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Neoptolemos JP, Kleeff J, Michl P, Costello E, Greenhalf W, Palmer DH. Therapeutic developments in pancreatic cancer: current and future perspectives. Nat Rev Gastroenterol Hepatol. 2018;15(6):333–48. https://doi.org/10.1038/s41575-018-0005-x.

    Article  PubMed  Google Scholar 

  16. De Pastena M, van Bodegraven EA, Mungroop TH, et al. Distal pancreatectomy fistula risk score (D-FRS): development and international validation. Ann Surg. 2022. https://doi.org/10.1097/SLA.0000000000005497.

    Article  PubMed  Google Scholar 

  17. He C, Zhang Y, Li L, Zhao M, Wang C, Tang Y. Risk factor analysis and prediction of postoperative clinically relevant pancreatic fistula after distal pancreatectomy. BMC Surg. 2023;23(1):5. https://doi.org/10.1186/s12893-023-01907-w.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Okano K, Oshima M, Kakinoki K, et al. Pancreatic thickness as a predictive factor for postoperative pancreatic fistula after distal pancreatectomy using an endopath stapler. Surg Today. 2013;43(2):141–7. https://doi.org/10.1007/s00595-012-0235-4.

    Article  PubMed  Google Scholar 

  19. Sugimoto M, Kendrick ML, Farnell MB, et al. Relationship between pancreatic thickness and staple height is relevant to the occurrence of pancreatic fistula after distal pancreatectomy. HPB (Oxford). 2020;22(3):398–404. https://doi.org/10.1016/j.hpb.2019.07.010.

    Article  PubMed  Google Scholar 

  20. Maeda K, Kuriyama N, Yuge T, et al. Risk factor analysis of postoperative pancreatic fistula after distal pancreatectomy, with a focus on pancreas-visceral fat CT value ratio and serrated pancreatic contour. BMC Surg. 2022;22(1):240. https://doi.org/10.1186/s12893-022-01650-8.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Mungroop TH, van der Heijde N, Busch OR, et al. Randomized clinical trial and meta-analysis of the impact of a fibrin sealant patch on pancreatic fistula after distal pancreatectomy: CPR trial. BJS Open. 2021. https://doi.org/10.1093/bjsopen/zrab001.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Akamatsu N, Sugawara Y, Komagome M, et al. Risk factors for postoperative pancreatic fistula after pancreaticoduodenectomy: the significance of the ratio of the main pancreatic duct to the pancreas body as a predictor of leakage. J Hepatobiliary Pancreat Sci. 2010;17(3):322–8. https://doi.org/10.1007/s00534-009-0248-6.

    Article  PubMed  Google Scholar 

  23. Barbier L, Mege D, Reyre A, Moutardier VM, Ewald JA, Delpero JR. Predict pancreatic fistula after pancreaticoduodenectomy: ratio body thickness/main duct. ANZ J Surg. 2018;88(5):E451–5. https://doi.org/10.1111/ans.14048.

    Article  PubMed  Google Scholar 

  24. Roberts KJ, Storey R, Hodson J, Smith AM, Morris-Stiff G. Preoperative prediction of pancreatic fistula: is it possible? Pancreatology. 2013;13(4):423–8. https://doi.org/10.1016/j.pan.2013.04.322.

    Article  PubMed  Google Scholar 

  25. 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. https://doi.org/10.1007/s11605-017-3356-7.

    Article  PubMed  Google Scholar 

  26. Pratt WB, Callery MP, Vollmer CM Jr. Risk prediction for development of pancreatic fistula using the ISGPF classification scheme. World J Surg. 2008;32(3):419–28. https://doi.org/10.1007/s00268-007-9388-5.

    Article  PubMed  Google Scholar 

  27. Hashimoto Y, Sclabas GM, Takahashi N, et al. Dual-phase computed tomography for assessment of pancreatic fibrosis and anastomotic failure risk following pancreatoduodenectomy. J Gastrointest Surg. 2011;15(12):2193–204. https://doi.org/10.1007/s11605-011-1687-3.

    Article  PubMed  Google Scholar 

  28. Kawai T, Autieri MV, Scalia R. Adipose tissue inflammation and metabolic dysfunction in obesity. Am J Physiol Cell Physiol. 2021;320(3):C375–91. https://doi.org/10.1152/ajpcell.00379.2020.

    Article  CAS  PubMed  Google Scholar 

  29. Coelho M, Oliveira T, Fernandes R. Biochemistry of adipose tissue: an endocrine organ. Arch Med Sci. 2013;9(2):191–200. https://doi.org/10.5114/aoms.2013.33181.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Jia SH, Li Y, Parodo J, et al. Pre-B cell colony-enhancing factor inhibits neutrophil apoptosis in experimental inflammation and clinical sepsis. J Clin Invest. 2004;113(9):1318–27. https://doi.org/10.1172/JCI19930.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Li Y, Yang Q, Cai D, et al. Resistin, a novel host defense peptide of innate immunity. Front Immunol. 2021;12:699807. https://doi.org/10.3389/fimmu.2021.699807.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Stoffel NU, El-Mallah C, Herter-Aeberli I, et al. The effect of central obesity on inflammation, hepcidin, and iron metabolism in young women. Int J Obes (Lond). 2020;44(6):1291–300. https://doi.org/10.1038/s41366-020-0522-x.

    Article  CAS  PubMed  Google Scholar 

  33. Tilg H, Moschen AR. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat Rev Immunol. 2006;6(10):772–83. https://doi.org/10.1038/nri1937.

    Article  CAS  PubMed  Google Scholar 

  34. Zhao H, Wu L, Yan G, et al. Inflammation and tumor progression: signaling pathways and targeted intervention. Signal Transduct Target Ther. 2021;6(1):263. https://doi.org/10.1038/s41392-021-00658-5.

    Article  MathSciNet  CAS  PubMed  PubMed Central  Google Scholar 

  35. Greten FR, Grivennikov SI. Inflammation and cancer: triggers, mechanisms, and consequences. Immunity. 2019;51(1):27–41. https://doi.org/10.1016/j.immuni.2019.06.025.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Singh N, Baby D, Rajguru JP, Patil PB, Thakkannavar SS, Pujari VB. Inflammation and cancer. Ann Afr Med. 2019;18(3):121–6. https://doi.org/10.4103/aam.aam_56_18.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Nagai N, Kudo Y, Aki D, Nakagawa H, Taniguchi K. Immunomodulation by inflammation during liver and gastrointestinal tumorigenesis and aging. Int J Mol Sci. 2021. https://doi.org/10.3390/ijms22052238.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Liu J, Lin PC, Zhou BP. Inflammation fuels tumor progress and metastasis. Curr Pharm Des. 2015;21(21):3032–40. https://doi.org/10.2174/1381612821666150514105741.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Mathur A, Hernandez J, Shaheen F, et al. Preoperative computed tomography measurements of pancreatic steatosis and visceral fat: prognostic markers for dissemination and lethality of pancreatic adenocarcinoma. HPB (Oxford). 2011;13(6):404–10. https://doi.org/10.1111/j.1477-2574.2011.00304.x.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Sandini M, Bernasconi DP, Ippolito D, et al. Preoperative computed tomography to predict and stratify the risk of severe pancreatic fistula after pancreatoduodenectomy. Medicine (Baltimore). 2015;94(31):e1152. https://doi.org/10.1097/MD.0000000000001152.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Tajima Y, Kawabata Y, Hirahara N. Preoperative imaging evaluation of pancreatic pathologies for the objective prediction of pancreatic fistula after pancreaticoduodenectomy. Surg Today. 2018;48(2):140–50. https://doi.org/10.1007/s00595-017-1529-3.

    Article  PubMed  Google Scholar 

  42. Tranchart H, Gaujoux S, Rebours V, et al. Preoperative CT scan helps to predict the occurrence of severe pancreatic fistula after pancreaticoduodenectomy. Ann Surg. 2012;256(1):139–45. https://doi.org/10.1097/SLA.0b013e318256c32c.

    Article  PubMed  Google Scholar 

  43. Park CM, Park JS, Cho ES, Kim JK, Yu JS, Yoon DS. The effect of visceral fat mass on pancreatic fistula after pancreaticoduodenectomy. J Invest Surg. 2012;25(3):169–73. https://doi.org/10.3109/08941939.2011.616255.

    Article  PubMed  Google Scholar 

  44. Savin ML, Mihai F, Gheorghe L, et al. Proposal of a preoperative CT-based score to predict the risk of clinically relevant pancreatic fistula after cephalic pancreatoduodenectomy. Medicina (Kaunas). 2021. https://doi.org/10.3390/medicina57070650.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Kolbinger FR, Lambrecht J, Leger S, et al. The image-based preoperative fistula risk score (preFRS) predicts postoperative pancreatic fistula in patients undergoing pancreatic head resection. Sci Rep. 2022;12(1):4064. https://doi.org/10.1038/s41598-022-07970-2.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  46. Frozanpor F, Loizou L, Ansorge C, Lundell L, Albiin N, Segersvard R. Correlation between preoperative imaging and intraoperative risk assessment in the prediction of postoperative pancreatic fistula following pancreatoduodenectomy. World J Surg. 2014;38(9):2422–9. https://doi.org/10.1007/s00268-014-2556-5.

    Article  PubMed  Google Scholar 

  47. Menahem B, Guittet L, Mulliri A, Alves A, Lubrano J. Pancreaticogastrostomy is superior to pancreaticojejunostomy for prevention of pancreatic fistula after pancreaticoduodenectomy: an updated meta-analysis of randomized controlled trials. Ann Surg. 2015;261(5):882–7. https://doi.org/10.1097/SLA.0000000000000806.

    Article  PubMed  Google Scholar 

  48. Garg PK, Sharma J, Jakhetiya A, Chishi N. The role of prophylactic octreotide following pancreaticoduodenectomy to prevent postoperative pancreatic fistula: a meta-analysis of the randomized controlled trials. Surg J (N Y). 2018;4(4):e182–7. https://doi.org/10.1055/s-0038-1675359.

    Article  PubMed  Google Scholar 

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Acknowledgment

Research reported in this publication was supported by the National Cancer Institute of the National Institutes of Health under Award Number K12 CA237806 from the Emory K12 Clinical Oncology Training Program. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Additional support in part by the Contardi Research Fellowship and the Georgia CTSA UL1 Program (grant number UL1 TR002378). The acknowledged parties had no role in study design, data collection, analysis and interpretation of data, manuscript writing, and decision to submit the manuscript for publication.

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Sok, C., Sandhu, S., Shah, H. et al. Simple Preoperative Imaging Measurements Predict Postoperative Pancreatic Fistula After Pancreatoduodenectomy. Ann Surg Oncol 31, 1898–1905 (2024). https://doi.org/10.1245/s10434-023-14564-3

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