Skip to main content

Advertisement

Log in

Preoperative imaging evaluation of pancreatic pathologies for the objective prediction of pancreatic fistula after pancreaticoduodenectomy

  • Review Article
  • Published:
Surgery Today Aims and scope Submit manuscript

Abstract

In performing pancreaticoduodenectomy (PD) or when conducting clinical trials involving PD procedure, a universal platform for predicting the risk of postoperative pancreatic fistula (POPF) is indispensable. In this article, the most significant imaging studies that focused on the objective preoperative assessment of pancreatic pathologies in association with the occurrence of POPF after PD were reviewed. Several recently developed imaging modalities can objectively predict the occurrence of POPF after PD by assessing the elasticity, fibrosis, and fatty infiltration of the pancreas. These valuable imaging modalities include: (1) acoustic radiation force impulse ultrasound (US) electrography which provides information about the elastic properties of the pancreas; (2) contrast-enhanced computed tomography (CT) and magnetic resonance imaging (MRI) with/without contrast-enhancement which reflect the histological degree of pancreatic fibrosis; and (3) multi-detector row CT and/or MRI which reflects the microscopic fatty infiltration of the pancreas. The precise and objective preoperative risk assessment of POPF enables surgeons to customize appropriate management strategies for individual patients undergoing PD. This would be also beneficial for stratifying patients for enrolment in relevant studies that involve pancreatic head resection, as objective criteria could be set for the definitive evaluation of collected data related to surgical outcomes across different institutions and surgeons.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, et al. Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery. 2005;138(1):8–13.

    Article  PubMed  Google Scholar 

  2. Winter JM, Cameron JL, Campbell KA, Arnold MA, Chang DC, Coleman J, et al. 1423 pancreaticoduodenectomies for pancreatic cancer: a single-institution experience. J Gastrointest Surg. 2006;10(9):1199–210.

    Article  PubMed  Google Scholar 

  3. Cameron JL, Riall TS, Coleman J, Belcher KA. One thousand consecutive pancreaticoduodenectomies. Ann Surg. 2006;244(1):10–5.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Daskalaki D, Butturini G, Molinari E, Crippa S, Pederzoli P, Bassi C. A grading system can predict clinical and economic outcomes of pancreatic fistula after pancreaticoduodenectomy: results in 755 consecutive patients. Langenbecks Arch Surg. 2011;396(1):91–8.

    Article  PubMed  Google Scholar 

  5. Niedergethmann M, Farag Soliman M, Post S. Postoperative complications of pancreatic cancer surgery. Minerva Chir. 2004;59(2):175–83.

    CAS  PubMed  Google Scholar 

  6. Tani M, Kawai M, Hirono S, Hatori T, Imaizumi T, Nakao A, et al. Use of omentum or falciform ligament does not decrease complications after pancreaticoduodenectomy: nationwide survey of the Japanese Society of Pancreatic Surgery. Surgery. 2012;151(2):183–91.

    Article  PubMed  Google Scholar 

  7. Katayama H, Kurokawa Y, Nakamura K, Ito H, Kanemitsu Y, Masuda N, et al. Extended Clavien-Dindo classification of surgical complications: Japan Clinical Oncology Group postoperative complications criteria. Surg Today. 2016;46(6):668–85.

    Article  PubMed  Google Scholar 

  8. Callery MP, Pratt WB, Vollmer CM Jr. Prevention and management of pancreatic fistula. J Gastrointest Surg. 2009;13(1):163–73.

    Article  PubMed  Google Scholar 

  9. Riall TS, Reddy DM, Nealon WH, Goodwin JS. The effect of age on short-term outcomes after pancreatic resection: a population-based study. Ann Surg. 2008;248(3):459–67.

    PubMed  PubMed Central  Google Scholar 

  10. Veillette G, Dominguez I, Ferrone C, Thayer SP, McGrath D, Warshaw AL, et al. Implications and management of pancreatic fistulas following pancreaticoduodenectomy: the Massachusetts General Hospital experience. Arch Surg. 2008;143(5):476–81.

    Article  PubMed  PubMed Central  Google Scholar 

  11. House MG, Fong Y, Arnaoutakis DJ, Sharma R, Winston CB, Protic M, et al. Preoperative predictors for complications after pancreaticoduodenectomy: impact of BMI and body fat distribution. J Gastrointest Surg. 2008;12(2):270–8.

    Article  PubMed  Google Scholar 

  12. Roberts KJ, Sutcliffe RP, Marudanayagam R, Hodson J, Isaac J, Muiesan P, et al. Scoring system to predict pancreatic fistula after pancreaticoduodenectomy: a UK Multicenter Study. Ann Surg. 2015;261(6):1191–7.

    Article  PubMed  Google Scholar 

  13. DeOliveira ML, Winter JM, Schafer M, Cunningham SC, Cameron JL, Yeo CJ, et al. Assessment of complications after pancreatic surgery: a novel grading system applied to 633 patients undergoing pancreaticoduodenectomy. Ann Surg. 2006;244(6):931–7.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Lermite E, Pessaux P, Brehant O, Teyssedou C, Pelletier I, Etienne S, et al. Risk factors of pancreatic fistula and delayed gastric emptying after pancreaticoduodenectomy with pancreaticogastrostomy. J Am Coll Surg. 2007;204(4):588–96.

    Article  PubMed  Google Scholar 

  15. Heinrich S, Schäfer M, Weber A, Hany TF, Bhure U, Pestalozzi BC, et al. Neoadjuvant chemotherapy generates a significant tumor response in resectable pancreatic cancer without increasing morbidity: results of a prospective phase II trial. Ann Surg. 2008;248(6):1014–22.

    Article  PubMed  Google Scholar 

  16. Cheng TY, Sheth K, White RR, Ueno T, Hung CF, Clary BM, et al. Effect of neoadjuvant chemoradiation on operative mortality and morbidity for pancreaticoduodenectomy. Ann Surg Oncol. 2006;13(1):66–74.

    Article  PubMed  Google Scholar 

  17. Tomihara H, Eguchi H, Yamada D, Gotoh K, Kawamoto K, Wada H, et al. Preoperative chemoradiotherapy does not compromise the feasibility of adjuvant chemotherapy for patients with pancreatic ductal adenocarcinoma. Surg Today. 2017;47(2):218–26.

    Article  CAS  PubMed  Google Scholar 

  18. Tajima Y, Kuroki T, Tsutsumi R, Fukuda K, Kitasato A, Adachi T, et al. Risk factors for pancreatic anastomotic leakage: the significance of preoperative dynamic magnetic resonance imaging of the pancreas as a predictor of leakage. J Am Coll Surg. 2006;202(5):723–31.

    Article  PubMed  Google Scholar 

  19. Akamatsu N, Sugawara Y, Komagome M, Shin N, Cho N, Ishida T, 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.

    Article  PubMed  Google Scholar 

  20. Gaujoux S, Cortes A, Couvelard A, Noullet S, Clavel L, Rebours V, et al. Fatty pancreas and increased body mass index are risk factors of pancreatic fistula after pancreaticoduodenectomy. Surgery. 2010;148(1):15–23.

    Article  PubMed  Google Scholar 

  21. Mathur A, Pitt HA, Marine M, Saxena R, Schmidt CM, et al. Fatty pancreas: a factor in postoperative pancreatic fistula. Ann Surg. 2007;246(6):1058–64.

    Article  PubMed  Google Scholar 

  22. Kanda M, Fujii T, Suenaga M, Takami H, Hattori M, Inokawa Y, et al. Estimated pancreatic parenchymal remnant volume accurately predicts clinically relevant pancreatic fistula after pancreatoduodenectomy. Surgery. 2014;156(3):601–10.

    Article  PubMed  Google Scholar 

  23. Hashimoto Y, Traverso LW. Pancreatic anastomotic failure rate after pancreaticoduodenectomy decreases with microsurgery. J Am Coll Surg. 2010;211(4):510–21.

    Article  PubMed  Google Scholar 

  24. Yamashita Y, Yoshida Y, Kurihara T, Tsujita E, Takeishi K, Ishida T, et al. Surgical loupes at 5.0× magnification and the VIO soft-coagulation system can prevent postoperative pancreatic fistula in duct-to-mucosa pancreaticojejunostomy. Anticancer Res. 2015;35(3):1691–6.

    PubMed  Google Scholar 

  25. Ho V, Heslin MJ. Effect of hospital volume and experience on in-hospital mortality for pancreaticoduodenectomy. Ann Surg. 2003;237(4):509–14.

    PubMed  PubMed Central  Google Scholar 

  26. Schmidt CM, Turrini O, Parikh P, House MG, Zyromski NJ, Nakeeb A, et al. Effect of hospital volume, surgeon experience, and surgeon volume on patient outcomes after pancreaticoduodenectomy: a single-institution experience. Arch Surg. 2010;145(7):634–40.

    Article  PubMed  Google Scholar 

  27. Laugier R, Camatte R, Sarles H. Chronic obstructive pancreatitis after healing of a necrotic pseudocyst. Am J Surg. 1983;146(5):551–7.

    Article  CAS  PubMed  Google Scholar 

  28. Sarles H, Cambon P, Choux R, Payan MJ, Odaira S, Laugier R, et al. Chronic obstructive pancreatitis due to tiny (0.6–8 mm) benign tumors obstructing pancreatic ducts: report of three cases. Pancreas. 1988;3(2):232–7.

    Article  CAS  PubMed  Google Scholar 

  29. Ophir J, Céspedes I, Ponnekanti H, Yazdi Y, Li X. Elastography: a quantitative method for imaging the elasticity of biological tissues. Ultrason Imaging. 1991;13:111–34.

    Article  CAS  PubMed  Google Scholar 

  30. Hoyt K, Parker KJ, Rubens DJ. Real-time shear velocity imaging using sonoelastographic techniques. Ultrasound Med Biol. 2007;33(7):1086–97.

    Article  PubMed  Google Scholar 

  31. Nightingale K, Bentley R, Trahey G. Observations of tissue response to acoustic radiation force: opportunities for imaging. Ultrason Imaging. 2002;24(3):129–38.

    Article  PubMed  Google Scholar 

  32. Toshima T, Shirabe K, Takeishi K, Motomura T, Mano Y, Uchiyama H, et al. New method for assessing liver fibrosis based on acoustic radiation force impulse: a special reference to the difference between right and left liver. J Gastroenterol. 2011;46(5):705–11.

    Article  PubMed  Google Scholar 

  33. Son CY, Kim SU, Han WK, Choi GH, Park H, Yang SC, et al. Normal liver elasticity values using acoustic radiation force impulse imaging: a prospective study in healthy living liver and kidney donors. J Gastroenterol Hepatol. 2012;l27:130–136.

  34. Itoh Y, Itoh A, Kawashima H, Ohno E, Nakamura Y, Hiramatsu T, et al. Quantitative analysis of diagnosing pancreatic fibrosis using EUS-elastography (comparison with surgical specimens). J Gastroenterol. 2014;49:1183–92.

    Article  PubMed  Google Scholar 

  35. Lee TK, Kang CM, Park MS, Choi SH, Chung YE, Choi JY, et al. Prediction of postoperative pancreatic fistulas after pancreatectomy: assessment with acoustic radiation force impulse elastography. J Ultrasound Med. 2014;33:781–6.

    Article  PubMed  Google Scholar 

  36. Harada N, Ishizawa T, Inoue Y, Aoki T, Sakamoto Y, Hasegawa K, et al. Acoustic radiation force impulse imaging of the pancreas for estimation of pathologic fibrosis and risk of postoperative pancreatic fistula. J Am Coll Surg. 2014;219:887–94.

    Article  PubMed  Google Scholar 

  37. Hashimoto Y, Sclabas GM, Takahashi N, Kirihara Y, Smyrk TC, Huebner M, 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.

    Article  PubMed  Google Scholar 

  38. Sugimoto M, Takahashi S, Kobayashi T, Kojima M, Gotohda N, Satake M, et al. Pancreatic perfusion data and post-pancreaticoduodenectomy outcomes. J Surg Res. 2015;194:441–9.

    Article  PubMed  Google Scholar 

  39. Rosso E, Casnedi S, Pessaux P, Oussoultzoglou E, Panaro F, Mahfud M, et al. The role of “fatty pancreas” and of BMI in the occurrence of pancreatic fistula after pancreaticoduodenectomy. J Gastrointest Surg. 2009;13(10):1845–51.

    Article  PubMed  Google Scholar 

  40. Tranchart H, Gaujoux S, Rebours V, Vullierme MP, Dokmak S, Levy P, et al. Preoperative CT scan helps to predict the occurrence of severe pancreatic fistula after pancreaticoduodenectomy. Ann Surg. 2012;256(1):139–45.

    Article  PubMed  Google Scholar 

  41. Kirihara Y, Takahashi N, Hashimoto Y, Sclabas GM, Khan S, Moriya T, et al. Prediction of pancreatic anastomotic failure after pancreatoduodenectomy: the use of preoperative, quantitative computed tomography to measure remnant pancreatic volume and body composition. Ann Surg. 2013;257(3):512–9.

    Article  PubMed  Google Scholar 

  42. Shen W, Punyanitya M, Wang Z, Gallagher D, St-Onge MP, Albu J, et al. Total body skeletal muscle and adipose tissue volumes: estimation from a single abdominal cross-sectional image. J Appl Physiol. 2004;97(6):2333–8.

    Article  PubMed  Google Scholar 

  43. Watanabe H, Kanematsu M, Tanaka K, Osada S, Tomita H, Hara A, et al. Fibrosis and postoperative fistula of the pancreas: correlation with MR imaging findings-preliminary results. Radiology. 2014;270(3):791–9.

    Article  PubMed  Google Scholar 

  44. Kim Z, Kim MJ, Kim JH, Jin SY, Kim YB, Seo D, et al. Prediction of post-operative pancreatic fistula in pancreaticoduodenectomy patients using pre-operative MRI: a pilot study. HPB (Oxford). 2009;11(3):215–21.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Tanaka K, Tomita H, Osada S, Watanabe H, Imai H, Sasaki Y, et al. Significance of histopathological evaluation of pancreatic fibrosis to predict postoperative course after pancreatic surgery. Anticancer Res. 2015;35(3):1749–56.

    PubMed  Google Scholar 

  46. Tajima Y, Matsuzaki S, Furui J, Isomoto I, Hayashi K, Kanematsu T. Use of the time-signal intensity curve from dynamic magnetic resonance imaging to evaluate remnant pancreatic fibrosis after pancreaticojejunostomy in patients undergoing pancreaticoduodenectomy. Br J Surg. 2004;91(5):595–600.

    Article  CAS  PubMed  Google Scholar 

  47. Tajima Y, Kuroki T, Kitasato A, Adachi T, Isomoto I, Uetani M, et al. Patient allocation based on preoperative assessment of pancreatic fibrosis to secure pancreatic anastomosis performed by trainee surgeons: a prospective study. J Hepatobiliary Pancreat Sci. 2010;17(6):831–8.

    Article  PubMed  Google Scholar 

  48. Tajima Y, Kuroki T, Tsuneoka N, Adachi T, Isomoto I, Uetani M, et al. Monitoring fibrosis of the pancreatic remnant after a pancreaticoduodenectomy with dynamic MRI. J Surg Res. 2010;158(1):61–8.

    Article  PubMed  Google Scholar 

  49. Dinter DJ, Aramin N, Weiss C, Singer C, Weisser G, Schoenberg SO, et al. Prediction of anastomotic leakage after pancreatic head resections by dynamic magnetic resonance imaging (dMRI). J Gastrointest Surg. 2009;13(4):735–44.

    Article  PubMed  Google Scholar 

  50. Schwenzer NF, Machann J, Martirosian P, Stefan N, Schraml C, Fritsche A, et al. Quantification of pancreatic lipomatosis and liver steatosis by MRI: comparison of in/opposed-phase and spectral-spatial excitation techniques. Invest Radiol. 2008;43(5):330–7.

    Article  PubMed  Google Scholar 

  51. Lee SE, Jang JY, Lim CS, Kang MJ, Kim SH, Kim MA, et al. Measurement of pancreatic fat by magnetic resonance imaging: predicting the occurrence of pancreatic fistula after pancreatoduodenectomy. Ann Surg. 2010;251(5):932–6.

    Article  PubMed  Google Scholar 

  52. Hu HH, Kim HW, Nayak KS, Goran MI. Comparison of fat-water MRI and single-voxel MRS in the assessment of hepatic and pancreatic fat fractions in humans. Obesity (Silver Spring). 2010;18(4):841–7.

    Article  PubMed  Google Scholar 

  53. Shi Y, Glaser KJ, Venkatesh SK, Ben-Abraham EI, Ehman RL. Feasibility of using 3D MR elastography to determine pancreatic stiffness in healthy volunteers. J Magn Reson Imaging. 2015;41(2):369–75.

    Article  PubMed  Google Scholar 

  54. Sugimoto M, Takahashi S, Kojima M, Gotohda N, Kato Y, Kawano S, et al. What is the nature of pancreatic consistency? Assessment of the elastic modulus of the pancreas and comparison with tactile sensation, histology, and occurrence of postoperative pancreatic fistula after pancreaticoduodenectomy. Surgery. 2014;156(5):1204–11.

    Article  PubMed  Google Scholar 

  55. Belyaev O, Rosenkranz S, Munding J, Herzog T, Chromik AM, Tannapfel A, et al. Quantitative assessment and determinants of suture-holding capacity of human pancreas. J Surg Res. 2013;184(2):807–12.

    Article  PubMed  Google Scholar 

  56. Itoh A, Ueno E, Tohno E, Kamma H, Takahashi H, Shiina T, et al. Breast disease: clinical application of US elastography for diagnosis. Radiology. 2006;239(2):341–50.

    Article  PubMed  Google Scholar 

  57. D’Onofrio M, Crosara S, De Robertis R, Canestrini S, Demozzi E, Pozzi Mucelli R. Elastography of the pancreas. Eur J Radiol. 2014;83(3):415–9.

    Article  PubMed  Google Scholar 

  58. Xiong JJ, Altaf K, Mukherjee R, Huang W, Hu WM, Li A, et al. Systematic review and meta-analysis of outcomes after intraoperative pancreatic duct stent placement during pancreaticoduodenectomy. Br J Surg. 2012;99(8):1050–61.

    Article  CAS  PubMed  Google Scholar 

  59. Motoi F, Egawa S, Rikiyama T, Katayose Y, Unno M. Randomized clinical trial of external stent drainage of the pancreatic duct to reduce postoperative pancreatic fistula after pancreaticojejunostomy. Br J Surg. 2012;99(4):524–31.

    Article  CAS  PubMed  Google Scholar 

  60. Kawahara R, Akasu G, Ishikawa H, Yasunaga M, Kinoshita H. A questionnaire on the educational system for pancreatoduodenectomy performed in 1134 patients in 71 institutions as members of the Japanese Society of Pancreatic Surgery. J Hepatobiliary Pancreat Sci. 2013;20(2):173–85.

    Article  PubMed  Google Scholar 

  61. 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.

    Article  PubMed  Google Scholar 

  62. Xiong JJ, Tan CL, Szatmary P, Huang W, Ke NW, Hu WM, et al. Meta-analysis of pancreaticogastrostomy versus pancreaticojejunostomy after pancreaticoduodenectomy. Br J Surg. 2014;101(10):1196–208.

    Article  CAS  PubMed  Google Scholar 

  63. He T, Zhao Y, Chen Q, Wang X, Lin H, Han W. Pancreaticojejunostomy versus pancreaticogastrostomy after pancreaticoduodenectomy: a systematic review and meta-analysis. Dig Surg. 2013;30:56–69.

    Article  PubMed  Google Scholar 

  64. Keck T, Wellner UF, Bahra M, Klein F, Sick O, Niedergethmann M, et al. Pancreatogastrostomy versus pancreatojejunostomy for RECOnstruction after PANCreatoduodenectomy (RECOPANC, DRKS 00000767): perioperative and long-term results of a multicenter randomized controlled trial. Ann Surg. 2016;263(3):440–9.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Allen PJ, Gönen M, Brennan MF, Bucknor AA, Robinson LM, Pappas MM, et al. Pasireotide for postoperative pancreatic fistula. N Engl J Med. 2014;370(21):2014–22.

    Article  PubMed  Google Scholar 

  66. Gurusamy KS, Koti R, Fusai G, Davidson BR. Somatostatin analogues for pancreatic surgery. Cochrane Database Syst Rev. 2013;4:CD008370.

  67. Jin K, Zhou H, Zhang J, Wang W, Sun Y, Ruan C, et al. Systematic review and meta-analysis of somatostatin analogues in the prevention of postoperative complication after pancreaticoduodenectomy. Dig Surg. 2015;32(3):196–207.

    Article  CAS  PubMed  Google Scholar 

  68. Zeng Q, Zhang Q, Han S, Yu Z, Zheng M, Zhou M, et al. Efficacy of somatostatin and its analogues in prevention of postoperative complications after pancreaticoduodenectomy: a meta-analysis of randomized controlled trials. Pancreas. 2008;36(1):18–25.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yoshitsugu Tajima.

Ethics declarations

Conflict of interest

We have no conflicts of interest to declare.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tajima, Y., Kawabata, Y. & Hirahara, N. Preoperative imaging evaluation of pancreatic pathologies for the objective prediction of pancreatic fistula after pancreaticoduodenectomy. Surg Today 48, 140–150 (2018). https://doi.org/10.1007/s00595-017-1529-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00595-017-1529-3

Keywords

Navigation