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Estimation of pancreatic fibrosis and prediction of postoperative pancreatic fistula using extracellular volume fraction in multiphasic contrast-enhanced CT

  • Gastrointestinal
  • Published:
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Abstract

Objective

To investigate the diagnostic performance of the extracellular volume (ECV) fraction in multiphasic contrast-enhanced computed tomography (CE-CT) for estimating histologic pancreatic fibrosis and predicting postoperative pancreatic fistula (POPF).

Methods

Eighty-five patients (49 men; mean age, 69 years) who underwent multiphasic CE-CT followed by pancreaticoduodenectomy with pancreaticojejunal anastomosis between January 2012 and December 2018 were retrospectively included. The ECV fraction was calculated from absolute enhancements of the pancreas and aorta between the precontrast and equilibrium-phase images, followed by comparisons among histologic pancreatic fibrosis grades (F0‒F3). The diagnostic performance of the ECV fraction in advanced fibrosis (F2‒F3) was evaluated using receiver operating characteristic curve analysis. Multivariate logistic regression analysis was used to evaluate the associations of the risk of POPF development with patient characteristics, histologic findings, and CT imaging parameters.

Results

The mean ECV fraction of the pancreas was 34.4% ± 9.5, with an excellent intrareader agreement of 0.811 and a moderate positive correlation with pancreatic fibrosis (r = 0.476; p < 0.001). The mean ECV fraction in advanced fibrosis was significantly higher than that in no/mild fibrosis (44.4% ± 10.8 vs. 31.7% ± 6.7; p < 0.001), and the area under the receiver operating characteristic curve for the diagnosis of advanced fibrosis was 0.837. Twenty-two patients (25.9%) developed clinically relevant POPF. Multivariate logistic regression analysis demonstrated that the ECV fraction was a significant predictor of POPF.

Conclusions

The ECV fraction can offer quantitative information for assessing pancreatic fibrosis and POPF after pancreaticojejunal anastomosis.

Key Points

• There was a moderate positive correlation of the extracellular volume (ECV) fraction of the pancreas in contrast-enhanced CT with the histologic grade of pancreatic fibrosis (r = 0.476; p < 0.001).

• The ECV fraction was higher in advanced fibrosis (F2‒F3) than in no/mild fibrosis (F0‒F1) (p < 0.001), with an AUC of 0.837 for detecting advanced fibrosis.

• The ECV fraction was an independent risk factor for predicting subclinical (odds ratio, 0.81) and clinical (odds ratio, 0.80) postoperative pancreatic fistula.

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Abbreviations

AUC:

Area under the receiver operating characteristic curve

BL:

Biochemical leak

CE-CT:

Contrast-enhanced computed tomography

ECV:

Extracellular volume

ICC:

Intraclass correlation coefficient

IPMN:

Intraductal papillary mucinous neoplasm

ISGPS:

International Study Group for Pancreatic Surgery

MPD:

Main pancreatic duct

POPF:

Postoperative pancreatic fistula

ROI:

Region of interest

References

  1. Suda K (2000) Pathogenesis and progression of human pancreatic fibrosis. Med Electron Microsc 33:200–206

    Article  CAS  PubMed  Google Scholar 

  2. Klöppel G, Detlefsen S, Feyerabend B (2004) Fibrosis of the pancreas: the initial tissue damage and the resulting pattern. Virchows Arch 445:1–8

    Article  PubMed  Google Scholar 

  3. Masamune A, Watanabe T, Kikuta K, Shimosegawa T (2009) Roles of pancreatic stellate cells in pancreatic inflammation and fibrosis. Clin Gastroenterol Hepatol 7:S48-54

    Article  CAS  PubMed  Google Scholar 

  4. Poon RT, Lo SH, Fong D, Fan ST, Wong J (2002) Prevention of pancreatic anastomotic leakage after pancreaticoduodenectomy. Am J Surg 183:42–52

    Article  PubMed  Google Scholar 

  5. Ansorge C, Strömmer L, Andrén-Sandberg Å, Lundell L, Herrington MK, Segersvärd R (2012) Structured intraoperative assessment of pancreatic gland characteristics in predicting complications after pancreaticoduodenectomy. Br J Surg 99:1076–1082

    Article  CAS  PubMed  Google Scholar 

  6. Pulvirenti A, Marchegiani G, Pea A et al (2018) Clinical implications of the 2016 International Study Group on Pancreatic Surgery definition and grading of postoperative pancreatic fistula on 775 consecutive pancreatic resections. Ann Surg 268:1069–1075

    Article  PubMed  Google Scholar 

  7. Bassi C, Marchegiani G, Dervenis C et al (2017) The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 years after. Surgery 161:584–591

    Article  PubMed  Google Scholar 

  8. Brient C, Regenet N, Sulpice L et al (2012) Risk factors for postoperative pancreatic fistulization subsequent to enucleation. J Gastrointest Surg 16:1883–1887

    Article  PubMed  Google Scholar 

  9. Hu BY, Wan T, Zhang WZ, Dong JH (2016) Risk factors for postoperative pancreatic fistula: analysis of 539 successive cases of pancreaticoduodenectomy. World J Gastroenterol 22:7797–7805

    Article  PubMed  PubMed Central  Google Scholar 

  10. Harada N, Ishizawa T, Inoue Y et al (2014) Acoustic radiation force impulse imaging of the pancreas for estimation of pathologic fibrosis and risk of postoperative pancreatic fistula. J Am Coll Surg 219:887-894.e885

    Article  PubMed  Google Scholar 

  11. Yoon JH, Lee JM, Lee KB et al (2016) Pancreatic steatosis and fibrosis: quantitative assessment with preoperative multiparametric mr imaging. Radiology 279:140–150

    Article  PubMed  Google Scholar 

  12. Shi Y, Liu Y, Gao F et al (2018) Pancreatic stiffness quantified with MR elastography: relationship to postoperative pancreatic fistula after pancreaticoenteric anastomosis. Radiology 288:476–484

    Article  PubMed  Google Scholar 

  13. Hashimoto Y, Sclabas GM, Takahashi N et al (2011) Dual-phase computed tomography for assessment of pancreatic fibrosis and anastomotic failure risk following pancreatoduodenectomy. J Gastrointest Surg 15:2193–2204

    Article  PubMed  Google Scholar 

  14. Tranchart H, Gaujoux S, Rebours V et al (2012) Preoperative CT scan helps to predict the occurrence of severe pancreatic fistula after pancreaticoduodenectomy. Ann Surg 256:139–145

    Article  PubMed  Google Scholar 

  15. Sugimoto M, Takahashi S, Kojima M, Kobayashi T, Gotohda N, Konishi M (2017) 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 21:846–854

    Article  PubMed  Google Scholar 

  16. Jablonowski R, Wilson MW, Do L, Hetts SW, Saeed M (2015) Multidetector CT measurement of myocardial extracellular volume in acute patchy and contiguous infarction: validation with microscopic measurement. Radiology 274:370–378

    Article  PubMed  Google Scholar 

  17. Bandula S, Punwani S, Rosenberg WM et al (2015) Equilibrium contrast-enhanced CT imaging to evaluate hepatic fibrosis: initial validation by comparison with histopathologic sampling. Radiology 275:136–143

    Article  PubMed  Google Scholar 

  18. Yoon JH, Lee JM, Klotz E et al (2015) Estimation of hepatic extracellular volume fraction using multiphasic liver computed tomography for hepatic fibrosis grading. Invest Radiol 50:290–296

    Article  PubMed  Google Scholar 

  19. Guo SL, Su LN, Zhai YN et al (2017) The clinical value of hepatic extracellular volume fraction using routine multiphasic contrast-enhanced liver CT for staging liver fibrosis. Clin Radiol 72:242–246

    Article  CAS  PubMed  Google Scholar 

  20. Sofue K, Tsurusaki M, Mileto A et al (2018) Dual-energy computed tomography for non-invasive staging of liver fibrosis: accuracy of iodine density measurements from contrast-enhanced data. Hepatol Res 48:1008–1019

    Article  PubMed  Google Scholar 

  21. Yamada Y, Masuda A, Sofue K et al (2020) Prediction of pancreatic atrophy after steroid therapy using equilibrium-phase contrast computed tomography imaging in autoimmune pancreatitis. JGH Open 4:677–683

    Article  PubMed  PubMed Central  Google Scholar 

  22. Cheng SH, Cheng YJ, Jin ZY, Xue HD (2019) Unresectable pancreatic ductal adenocarcinoma: role of CT quantitative imaging biomarkers for predicting outcomes of patients treated with chemotherapy. Eur J Radiol 113:188–197

    Article  PubMed  Google Scholar 

  23. Fukukura Y, Kumagae Y, Higashi R et al (2019) Extracellular volume fraction determined by equilibrium contrast-enhanced multidetector computed tomography as a prognostic factor in unresectable pancreatic adenocarcinoma treated with chemotherapy. Eur Radiol 29:353–361

    Article  PubMed  Google Scholar 

  24. Kim SY, Kim H, Cho JY et al (2014) Quantitative assessment of pancreatic fat by using unenhanced CT: pathologic correlation and clinical implications. Radiology 271:104–112

    Article  PubMed  Google Scholar 

  25. Callery MP, Pratt WB, Kent TS, Chaikof EL, Vollmer CM Jr (2013) A prospectively validated clinical risk score accurately predicts pancreatic fistula after pancreatoduodenectomy. J Am Coll Surg 216:1–14

    Article  PubMed  Google Scholar 

  26. Yagi Y, Masuda A, Zen Y et al (2018) Pancreatic inflammation and atrophy are not associated with pancreatic cancer concomitant with intraductal papillary mucinous neoplasm. Pancreatology 18:54–60

    Article  PubMed  Google Scholar 

  27. Afdhal NH, Nunes D (2004) Evaluation of liver fibrosis: a concise review. Am J Gastroenterol 99:1160–1174

    Article  PubMed  Google Scholar 

  28. Ohta Y, Kitao S, Yunaga H et al (2018) Myocardial delayed enhancement CT for the evaluation of heart failure: comparison to MRI. Radiology 288:682–691

    Article  PubMed  Google Scholar 

  29. Fukukura Y, Kumagae Y, Higashi R et al (2020) Extracellular volume fraction determined by equilibrium contrast-enhanced dual-energy CT as a prognostic factor in patients with stage IV pancreatic ductal adenocarcinoma. Eur Radiol 30:1679–1689

    Article  PubMed  Google Scholar 

  30. Kameda F, Tanabe M, Onoda H et al (2020) Quantification of pancreas fat on dual-energy computed tomography: comparison with six-point Dixon magnetic resonance imaging. Abdom Radiol (NY) 45:2779–2785

    Article  Google Scholar 

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The authors state that this work has not received any funding.

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Authors and Affiliations

  1. Department of Radiology, Kobe University Graduate School of Medicine, 7-5-2, Kusunoki-cho, Chuo-ku, Kobe, 650-0017, Japan

    Keitaro Sofue, Eisuke Ueshima, Yoshiko Ueno, Yushi Tsujita, Takeru Yamaguchi, Shinji Yabe & Takamichi Murakami

  2. Division of Gastroenterology, Department of Internal Medicine, Kobe University Graduate School of Medicine, Kobe, Japan

    Atsuhiro Masuda, Takeshi Tanaka, Noriko Inomata & Yuzo Kodama

  3. Division of Hepato-Biliary-Pancreatic Surgery, Department of Surgery, Kobe University Graduate School of Medicine, Kobe, Japan

    Sachiyo Shirakawa, Hirochika Toyama & Takumi Fukumoto

  4. Institute of Liver Studies, King’s College Hospital & King’s College London, London, UK

    Yoh Zen

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  1. Keitaro Sofue
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Corresponding author

Correspondence to Keitaro Sofue.

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The scientific guarantor of this publication is Keitaro Sofue.

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The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

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Sofue, K., Ueshima, E., Masuda, A. et al. Estimation of pancreatic fibrosis and prediction of postoperative pancreatic fistula using extracellular volume fraction in multiphasic contrast-enhanced CT. Eur Radiol 32, 1770–1780 (2022). https://doi.org/10.1007/s00330-021-08255-4

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  • DOI: https://doi.org/10.1007/s00330-021-08255-4

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