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.
Similar content being viewed by others
References
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.
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.
Cameron JL, Riall TS, Coleman J, Belcher KA. One thousand consecutive pancreaticoduodenectomies. Ann Surg. 2006;244(1):10–5.
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.
Niedergethmann M, Farag Soliman M, Post S. Postoperative complications of pancreatic cancer surgery. Minerva Chir. 2004;59(2):175–83.
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.
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.
Callery MP, Pratt WB, Vollmer CM Jr. Prevention and management of pancreatic fistula. J Gastrointest Surg. 2009;13(1):163–73.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Hashimoto Y, Traverso LW. Pancreatic anastomotic failure rate after pancreaticoduodenectomy decreases with microsurgery. J Am Coll Surg. 2010;211(4):510–21.
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.
Ho V, Heslin MJ. Effect of hospital volume and experience on in-hospital mortality for pancreaticoduodenectomy. Ann Surg. 2003;237(4):509–14.
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.
Laugier R, Camatte R, Sarles H. Chronic obstructive pancreatitis after healing of a necrotic pseudocyst. Am J Surg. 1983;146(5):551–7.
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.
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.
Hoyt K, Parker KJ, Rubens DJ. Real-time shear velocity imaging using sonoelastographic techniques. Ultrasound Med Biol. 2007;33(7):1086–97.
Nightingale K, Bentley R, Trahey G. Observations of tissue response to acoustic radiation force: opportunities for imaging. Ultrason Imaging. 2002;24(3):129–38.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Gurusamy KS, Koti R, Fusai G, Davidson BR. Somatostatin analogues for pancreatic surgery. Cochrane Database Syst Rev. 2013;4:CD008370.
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.
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
We have no conflicts of interest to declare.
Rights and permissions
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00595-017-1529-3