Abstract
Objectives
To prospectively investigate the stiffness and fluidity of pancreatic ductal adenocarcinoma (PDAC) and autoimmune pancreatitis (AIP) with tomoelastography, and to evaluate its diagnostic performance in distinguishing the two entities.
Methods
Tomoelastography provided high-resolution maps of shear wave speed (c in m/s) and phase angle (φ in rad), allowing mechanical characterization of the stiffness and fluidity properties of the pancreas. Forty patients with untreated PDAC and 33 patients with untreated AIP who underwent diagnostic pancreatic MRI at 3-T together with multifrequency MR elastography and tomoelastography data processing were prospectively enrolled. Ten healthy volunteers served as controls. Two radiologists and a technician measured pancreatic stiffness and fluidity independently. The two radiologists also independently evaluated the patients’ conventional MR sequences using the following diagnostic score: 1, definitely PDAC; 2, probably PDAC; 3, indeterminate; 4, probably AIP; and 5, definitely AIP. Interobserver agreement was assessed. Stiffness and fluidity of PDAC, AIP, and healthy pancreas, as well as diagnostic performance of tomoelastography and conventional MRI, were compared.
Results
AIP showed significantly lower stiffness and fluidity than PDAC and significantly higher stiffness and fluidity than healthy pancreas. Pancreatic fluidity was not influenced by secondary obstructive changes. The intraclass correlation coefficient for pancreatic stiffness and fluidity by the 3 readers was near-perfect (0.951–0.979, all p < 0.001). Both stiffness and fluidity allowed distinguishing PDAC from AIP. AUCs were 0.906 for stiffness, 0.872 for fluidity, and 0.842 for conventional MRI.
Conclusions
Pancreatic stiffness and fluidity both allow differentiation of PDAC and AIP with high accuracy.
Key Points
• AIP showed significantly lower stiffness and fluidity than PDAC and significantly higher stiffness and fluidity than healthy pancreas.
• Both stiffness and fluidity allowed distinguishing PDAC from AIP.
• Pancreatic fluidity could distinguish malignancy from non-malignant secondary obstructive changes.
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Abbreviations
- AIP:
-
Autoimmune pancreatitis
- AUC:
-
Area under the curve
- CI:
-
Confidence interval
- ICC:
-
Intraclass correlation coefficient
- MRE:
-
Magnetic resonance elastography
- PDAC:
-
Pancreatic ductal adenocarcinoma
- ROC:
-
Receiver operating characteristics
References
Moffat GT, Epstein AS, O'Reilly EM (2019) Pancreatic cancer-a disease in need: optimizing and integrating supportive care. Cancer. 125(22):3927–3935
Dickerson LD, Farooq A, Bano F et al (2019) Differentiation of autoimmune pancreatitis from pancreatic Cancer remains challenging. World J Surg 43(6):1604–1611
Saavedra-Perez D, Vaquero EC, Ayuso JR et al (2014) Autoimmune pancreatitis: a surgical dilemma. Cir Esp 92(10):645–653
Khandelwal A, Inoue D, Takahashi N (2020) Autoimmune pancreatitis: an update. Abdom Radiol 45(5):1359–1370
Luo G, Liu C, Guo M et al (2017) Potential biomarkers in Lewis negative patients with pancreatic cancer. Ann Surg 265(4):800–805
Ballehaninna UK, Chamberlain RS (2012) The clinical utility of serum CA 19-9 in the diagnosis, prognosis and management of pancreatic adenocarcinoma: an evidence based appraisal. J Gastrointest Oncol 3(2):105–119
Martins C, Lago P, Sousa P et al (2017) Type 2 autoimmune pancreatitis: a challenge in the differential diagnosis of a pancreatic mass. GE Port J Gastroenterol 24(6):296–300
Ngwa T, Law R, Hart P et al (2015) Serum IgG4 elevation in pancreatic cancer: diagnostic and prognostic significance and association with autoimmune pancreatitis. Pancreas 44(4):557–560
Ghazale A, Chari ST, Smyrk TC et al (2007) Value of serum IgG4 in the diagnosis of autoimmune pancreatitis and in distinguishing it from pancreatic cancer. Am J Gastroenterol 102(8):1646–1653
Zaheer A, Singh VK, Akshintala VS et al (2014) Differentiating autoimmune pancreatitis from pancreatic adenocarcinoma using dual-phase computed tomography. J Comput Assist Tomogr 38(1):146–152
Furuhashi N, Suzuki K, Sakurai Y et al (2015) Differentiation of focal-type autoimmune pancreatitis from pancreatic carcinoma: assessment by multiphase contrast-enhanced CT. Eur Radiol 25(5):1366–1374
Muhi A, Ichikawa T, Motosugi U et al (2012) Mass-forming autoimmune pancreatitis and pancreatic carcinoma: differential diagnosis on the basis of computed tomography and magnetic resonance cholangiopancreatography, and diffusion-weighted imaging findings. J Magn Reson Imaging 35(4):827–836
Sun GF, Zuo CJ, Shao CW et al (2013) Focal autoimmune pancreatitis: radiological characteristics help to distinguish from pancreatic cancer. World J Gastroenterol 19(23):3634–3641
Kim HJ, Kim YK, Jeong WK et al (2015) Pancreatic duct “icicle sign” on MRI for distinguishing autoimmune pancreatitis from pancreatic ductal adenocarcinoma in the proximal pancreas. Eur Radiol 25(6):1551–1560
Choi SY, Kim SH, Kang TW et al (2016) Differentiating mass-forming autoimmune pancreatitis from pancreatic ductal adenocarcinoma on the basis of contrast-enhanced MRI and DWI findings. AJR Am J Roentgenol 206(2):291–300
Hur BY, Lee JM, Lee JE et al (2012) Magnetic resonance imaging findings of the mass-forming type of autoimmune pancreatitis: comparison with pancreatic adenocarcinoma. J Magn Reson Imaging 36(1):188–197
Sugumar A, Levy MJ, Kamisawa T et al (2011) Endoscopic retrograde pancreatography criteria to diagnose autoimmune pancreatitis: an international multicentre study. Gut 60(5):666–670
Apte MV, Park S, Phillips PA et al (2004) Desmoplastic reaction in pancreatic cancer: role of pancreatic stellate cells. Pancreas 29(3):179–187
Zamboni G, Luttges J, Capelli P et al (2004) Histopathological features of diagnostic and clinical relevance in autoimmune pancreatitis: a study on 53 resection specimens and 9 biopsy specimens. Virchows Arch 445(6):552–563
Shi Y, Cang L, Zhang X et al (2018) The use of magnetic resonance elastography in differentiating autoimmune pancreatitis from pancreatic ductal adenocarcinoma: a preliminary study. Eur J Radiol 108:13–20
Streitberger KJ, Lilaj L, Schrank F et al (2020) How tissue fluidity influences brain tumor progression. Proc Natl Acad Sci U S A 117(1):128–134
Shahryari M, Tzschatzsch H, Guo J et al (2019) Tomoelastography distinguishes noninvasively between benign and malignant liver lesions. Cancer Res 79(22):5704–5710
Tzschatzsch H, Guo J, Dittmann F et al (2016) Tomoelastography by multifrequency wave number recovery from time-harmonic propagating shear waves. Med Image Anal 30:1–10
Streitberger KJ, Diederichs G, Guo J et al (2015) In vivo multifrequency magnetic resonance elastography of the human intervertebral disk. Magn Reson Med 74(5):1380–1387
Marticorena Garcia SR, Grossmann M, Bruns A et al (2019) Tomoelastography paired with T2* magnetic resonance imaging detects lupus nephritis with normal renal function. Invest Radiol 54(2):89–97
Bertalan G, Guo J, Tzschatzsch H et al (2019) Fast tomoelastography of the mouse brain by multifrequency single-shot MR elastography. Magn Reson Med 81(4):2676–2687
Hallgren KA (2012) Computing inter-rater reliability for observational data: an overview and tutorial. Tutor Quant Methods Psychol 8(1):23–34
Hanley JA, McNeil BJ (1982) The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143(1):29–36
Hudert CA, Tzschatzsch H, Rudolph B et al (2019) Tomoelastography for the evaluation of pediatric nonalcoholic fatty liver disease. Invest Radiol 54(4):198–203
Lang ST, Guo J, Bruns A et al (2019) Multiparametric quantitative MRI for the detection of IgA nephropathy using Tomoelastography, DWI, and BOLD imaging. Invest Radiol 54(10):669–674
Marticorena Garcia SR, Fischer T, Durr M et al (2016) Multifrequency magnetic resonance elastography for the assessment of renal allograft function. Invest Radiol 51(9):591–595
Takahashi N, Fletcher JG, Fidler JL et al (2008) Dual-phase CT of autoimmune pancreatitis: a multireader study. AJR Am J Roentgenol 190(2):280–286
Fukukura Y, Takumi K, Kamimura K et al (2012) Pancreatic adenocarcinoma: variability of diffusion-weighted MR imaging findings. Radiology 263(3):732–740
Mujica VR, Barkin JS, Go VL (2000) Acute pancreatitis secondary to pancreatic carcinoma. Study Group Participants. Pancreas 21(4):329–332
Shi Y, Liu Y, Liu YQ et al (2017) Early diagnosis and severity assessment of acute pancreatitis (AP) using MR elastography (MRE) with spin-echo echo-planar imaging. J Magn Reson Imaging 46(5):1311–1319
Liu Y, Wang M, Ji R et al (2018) Differentiation of pancreatic ductal adenocarcinoma from inflammatory mass: added value of magnetic resonance elastography. Clin Radiol 73(10):865–872
Shi Y, Gao F, Li Y et al (2018) Differentiation of benign and malignant solid pancreatic masses using magnetic resonance elastography with spin-echo echo planar imaging and three-dimensional inversion reconstruction: a prospective study. Eur Radiol 28(3):936–945
Acknowledgments
The authors sincerely acknowledge Dr.Yi Sun and Ms. Jinxia Zhu from Siemens Healthcare for the MR technical support, and Ms. Bettina Herwig from Department of Radiology, Charité-universitätsmedizin Berlin for the linguistic revision.
Funding
This study was funded by the National Natural Science Foundation of China (81901716 to L. Zhu and 81871512 to H. Xue), National Public Welfare, Basic Scientific Research Program of Chinese Academy of Medical Sciences (2019PT32008 to Z. Jin), and German Research Foundation (SFB 1340 “Matrix in Vision, GRK 2260 BIOQIC to I. Sack, J. Guo, P. Asbach, and B. Hamm).
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The scientific guarantor of this publication is Professor Ingolf Sack from the Department of Radiology, Charité-universitätsmedizin Berlin.
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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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No complex statistical methods were necessary for this paper.
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Written informed consent was obtained from all subjects (patients) in this study.
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Institutional Review Board approval was obtained.
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• Prospective
• Diagnostic study
• Performed at one institution
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Zhu, L., Guo, J., Jin, Z. et al. Distinguishing pancreatic cancer and autoimmune pancreatitis with in vivo tomoelastography. Eur Radiol 31, 3366–3374 (2021). https://doi.org/10.1007/s00330-020-07420-5
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DOI: https://doi.org/10.1007/s00330-020-07420-5