Semin Liver Dis 2019; 39(03): 369-380
DOI: 10.1055/s-0039-1687853
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Magnetic Resonance Imaging in Primary Sclerosing Cholangitis—Current State and Future Directions

Roman Zenouzi
1   1st Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
,
Christopher L. Welle
2   Department of Radiology Mayo Clinic, Rochester, Minnesota
,
Sudhakar K. Venkatesh
2   Department of Radiology Mayo Clinic, Rochester, Minnesota
,
Christoph Schramm
1   1st Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
3   Martin Zeitz Center for Rare Diseases, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
,
John E. Eaton
4   Division of Gastroenterology and Hepatology Mayo Clinic, Rochester, Minnesota
› Author Affiliations
Further Information

Publication History

Publication Date:
30 April 2019 (online)

Abstract

Primary sclerosing cholangitis (PSC) is a chronic cholestatic liver disease characterized by biliary inflammation and fibrosis leading to bile duct strictures, cirrhosis, and carries an increased risk of hepatobiliary malignancies. Magnetic resonance imaging (MRI) with magnetic resonance cholangiopancreatography (MRCP) is the imaging modality of choice in PSC. As an evolving technology, MRI has other potential applications in the care and study of those patients with PSC. In this review, the authors aim to provide a technical overview on MRI/MRCP and related technologies, summarize its contemporary use in PSC, and discuss its evolving role to predict outcomes and look ahead toward emerging MRI technologies relevant to PSC.

 
  • References

  • 1 Dyson JK, Beuers U, Jones DEJ, Lohse AW, Hudson M. Primary sclerosing cholangitis. Lancet 2018; 391 (10139): 2547-2559
  • 2 Eaton JE, Talwalkar JA, Lazaridis KN, Gores GJ, Lindor KD. Pathogenesis of primary sclerosing cholangitis and advances in diagnosis and management. Gastroenterology 2013; 145 (03) 521-536
  • 3 Karlsen TH, Folseraas T, Thorburn D, Vesterhus M. Primary sclerosing cholangitis - a comprehensive review. J Hepatol 2017; 67 (06) 1298-1323
  • 4 Boonstra K, Weersma RK, van Erpecum KJ. , et al; EpiPSCPBC Study Group. Population-based epidemiology, malignancy risk, and outcome of primary sclerosing cholangitis. Hepatology 2013; 58 (06) 2045-2055
  • 5 Horsley-Silva JL, Rodriguez EA, Franco DL, Lindor KD. An update on cancer risk and surveillance in primary sclerosing cholangitis. Liver Int 2017; 37 (08) 1103-1109
  • 6 Weersma RK, Lindor KD. Shifting paradigms: what is the true prevalence and clinical course of primary sclerosing cholangitis?. Gastroenterology 2016; 151 (04) 590-593
  • 7 Chapman R, Fevery J, Kalloo A. , et al; American Association for the Study of Liver Diseases. Diagnosis and management of primary sclerosing cholangitis. Hepatology 2010; 51 (02) 660-678
  • 8 Eaton JE, Gossard AA, Talwalkar JA. Recall processes for biliary cytology in primary sclerosing cholangitis. Curr Opin Gastroenterol 2014; 30 (03) 287-294
  • 9 Ehlken H, Zenouzi R, Schramm C. Risk of cholangiocarcinoma in patients with primary sclerosing cholangitis: diagnosis and surveillance. Curr Opin Gastroenterol 2017; 33 (02) 78-84
  • 10 European Association for the Study of the Liver. EASL Clinical Practice Guidelines: management of cholestatic liver diseases. J Hepatol 2009; 51 (02) 237-267
  • 11 European Society of Gastrointestinal Endoscopy; European Association for the Study of the Liver. Electronic address: easloffice@easloffice.eu; European Association for the Study of the Liver. Role of endoscopy in primary sclerosing cholangitis: European Society of Gastrointestinal Endoscopy (ESGE) and European Association for the Study of the Liver (EASL) Clinical Guideline. J Hepatol 2017; 66 (06) 1265-1281
  • 12 Lindor KD, Kowdley KV, Harrison ME. ; American College of Gastroenterology. ACG Clinical Guideline: primary sclerosing cholangitis. Am J Gastroenterol 2015; 110 (05) 646-659 , quiz 660
  • 13 Razumilava N, Gores GJ, Lindor KD. Cancer surveillance in patients with primary sclerosing cholangitis. Hepatology 2011; 54 (05) 1842-1852
  • 14 Rizvi S, Eaton JE, Gores GJ. Primary sclerosing cholangitis as a premalignant biliary tract disease: surveillance and management. Clin Gastroenterol Hepatol 2015; 13 (12) 2152-2165
  • 15 Schramm C, Eaton J, Ringe KI, Venkatesh S, Yamamura J. ; MRI working group of the IPSCSG. Recommendations on the use of magnetic resonance imaging in PSC-A position statement from the International PSC Study Group. Hepatology 2017; 66 (05) 1675-1688
  • 16 Isoda H, Kataoka M, Maetani Y. , et al. MRCP imaging at 3.0 T vs. 1.5 T: preliminary experience in healthy volunteers. J Magn Reson Imaging 2007; 25 (05) 1000-1006
  • 17 Kinner S, Dechêne A, Ladd SC. , et al. Comparison of different MRCP techniques for the depiction of biliary complications after liver transplantation. Eur Radiol 2010; 20 (07) 1749-1756
  • 18 Ringe KI, Hartung D, von Falck C, Wacker F, Raatschen HJ. 3D-MRCP for evaluation of intra- and extrahepatic bile ducts: comparison of different acquisition and reconstruction planes. BMC Med Imaging 2014; 14: 16
  • 19 Glockner JF, Saranathan M, Bayram E, Lee CU. Breath-held MR cholangiopancreatography (MRCP) using a 3D Dixon fat-water separated balanced steady state free precession sequence. Magn Reson Imaging 2013; 31 (08) 1263-1270
  • 20 Kim JH, Hong SS, Eun HW, Han JK, Choi BI. Clinical usefulness of free-breathing navigator-triggered 3D MRCP in non-cooperative patients: comparison with conventional breath-hold 2D MRCP. Eur J Radiol 2012; 81 (04) e513-e518
  • 21 Soto JA, Barish MA, Yucel EK. , et al. Pancreatic duct: MR cholangiopancreatography with a three-dimensional fast spin-echo technique. Radiology 1995; 196 (02) 459-464
  • 22 Mühler A, Clément O, Saeed M. , et al. Gadolinium-ethoxybenzyl-DTPA, a new liver-directed magnetic resonance contrast agent. Absence of acute hepatotoxic, cardiovascular, or immunogenic effects. Invest Radiol 1993; 28 (01) 26-32
  • 23 Vogl TJ, Pegios W, Waitzinger J, Pirovano G, Balzer J, Lissner J. NMR tomography of the liver with the new contrast agent Gd-BOPTA. The results of an in-vivo phase-I test [in German]. RoFo Fortschr Geb Rontgenstr Nuklearmed 1992; 156 (05) 465-470
  • 24 Frydrychowicz A, Jedynak AR, Kelcz F, Nagle SK, Reeder SB. Gadoxetic acid-enhanced T1-weighted MR cholangiography in primary sclerosing cholangitis. J Magn Reson Imaging 2012; 36 (03) 632-640
  • 25 Nolz R, Asenbaum U, Schoder M. , et al. Diagnostic workup of primary sclerosing cholangitis: the benefit of adding gadoxetic acid-enhanced T1-weighted magnetic resonance cholangiography to conventional T2-weighted magnetic resonance cholangiography. Clin Radiol 2014; 69 (05) 499-508
  • 26 Schulze J, Lenzen H, Hinrichs JB. , et al. An imaging biomarker for assessing hepatic function in patients with primary sclerosing cholangitis. Clin Gastroenterol Hepatol 2019; 17 (01) 192.e3-199.e3
  • 27 Muthupillai R, Lomas DJ, Rossman PJ, Greenleaf JF, Manduca A, Ehman RL. Magnetic resonance elastography by direct visualization of propagating acoustic strain waves. Science 1995; 269 (5232): 1854-1857
  • 28 Srinivasa Babu A, Wells ML, Teytelboym OM. , et al. Elastography in chronic liver disease: modalities, techniques, limitations, and future directions. Radiographics 2016; 36 (07) 1987-2006
  • 29 Venkatesh SK, Yin M, Ehman RL. Magnetic resonance elastography of liver: technique, analysis, and clinical applications. J Magn Reson Imaging 2013; 37 (03) 544-555
  • 30 Kennedy P, Wagner M, Castéra L. , et al. Quantitative elastography methods in liver disease: current evidence and future directions. Radiology 2018; 286 (03) 738-763
  • 31 Dave M, Elmunzer BJ, Dwamena BA, Higgins PD. Primary sclerosing cholangitis: meta-analysis of diagnostic performance of MR cholangiopancreatography. Radiology 2010; 256 (02) 387-396
  • 32 Meagher S, Yusoff I, Kennedy W, Martel M, Adam V, Barkun A. The roles of magnetic resonance and endoscopic retrograde cholangiopancreatography (MRCP and ERCP) in the diagnosis of patients with suspected sclerosing cholangitis: a cost-effectiveness analysis. Endoscopy 2007; 39 (03) 222-228
  • 33 Talwalkar JA, Angulo P, Johnson CD, Petersen BT, Lindor KD. Cost-minimization analysis of MRC versus ERCP for the diagnosis of primary sclerosing cholangitis. Hepatology 2004; 40 (01) 39-45
  • 34 Arrivé L, Ruiz A, El Mouhadi S, Azizi L, Monnier-Cholley L, Menu Y. MRI of cholangitis: traps and tips. Diagn Interv Imaging 2013; 94 (7–8): 757-770
  • 35 Düşünceli E, Erden A, Erden I, Karayalçin S. Primary sclerosing cholangitis: MR cholangiopancreatography and T2-weighted MR imaging findings. Diagn Interv Radiol 2005; 11 (04) 213-218
  • 36 Lunder AK, Hov JR, Borthne A. , et al. Prevalence of sclerosing cholangitis detected by magnetic resonance cholangiography in patients with long-term inflammatory bowel disease. Gastroenterology 2016; 151 (04) 660.e4-669.e4
  • 37 Rossi G, Sciveres M, Maruzzelli L. , et al. Diagnosis of sclerosing cholangitis in children: blinded, comparative study of magnetic resonance versus endoscopic cholangiography. Clin Res Hepatol Gastroenterol 2013; 37 (06) 596-601
  • 38 Moff SL, Kamel IR, Eustace J. , et al. Diagnosis of primary sclerosing cholangitis: a blinded comparative study using magnetic resonance cholangiography and endoscopic retrograde cholangiography. Gastrointest Endosc 2006; 64 (02) 219-223
  • 39 Fulcher AS, Turner MA, Franklin KJ. , et al. Primary sclerosing cholangitis: evaluation with MR cholangiography-a case-control study. Radiology 2000; 215 (01) 71-80
  • 40 Stiehl A, Rudolph G, Klöters-Plachky P, Sauer P, Walker S. Development of dominant bile duct stenoses in patients with primary sclerosing cholangitis treated with ursodeoxycholic acid: outcome after endoscopic treatment. J Hepatol 2002; 36 (02) 151-156
  • 41 Zenouzi R, Liwinski T, Yamamura J. , et al; International PSC Study Group (IPSCSG). Follow-up magnetic resonance imaging/3D-magnetic resonance cholangiopancreatography in patients with primary sclerosing cholangitis: challenging for experts to interpret. Aliment Pharmacol Ther 2018; 48 (02) 169-178
  • 42 Chapman MH, Webster GJ, Bannoo S, Johnson GJ, Wittmann J, Pereira SP. Cholangiocarcinoma and dominant strictures in patients with primary sclerosing cholangitis: a 25-year single-centre experience. Eur J Gastroenterol Hepatol 2012; 24 (09) 1051-1058
  • 43 Chapman RW, Williamson KD. Are dominant strictures in primary sclerosing cholangitis a risk factor for cholangiocarcinoma?. Curr Hepatol Rep 2017; 16 (02) 124-129
  • 44 Gotthardt DN, Rudolph G, Klöters-Plachky P, Kulaksiz H, Stiehl A. Endoscopic dilation of dominant stenoses in primary sclerosing cholangitis: outcome after long-term treatment. Gastrointest Endosc 2010; 71 (03) 527-534
  • 45 Rudolph G, Gotthardt D, Klöters-Plachky P, Kulaksiz H, Rost D, Stiehl A. Influence of dominant bile duct stenoses and biliary infections on outcome in primary sclerosing cholangitis. J Hepatol 2009; 51 (01) 149-155
  • 46 Weismüller TJ, Trivedi PJ, Bergquist A. , et al; International PSC Study Group. Patient age, sex, and inflammatory bowel disease phenotype associate with course of primary sclerosing cholangitis. Gastroenterology 2017; 152 (08) 1975.e8-1984.e8
  • 47 Eaton JE, McCauley BM, Atkinson EJ. , et al. Variations in primary sclerosing cholangitis across the age spectrum. J Gastroenterol Hepatol 2017; 32 (10) 1763-1768
  • 48 Bergquist A, Ekbom A, Olsson R. , et al. Hepatic and extrahepatic malignancies in primary sclerosing cholangitis. J Hepatol 2002; 36 (03) 321-327
  • 49 Burak K, Angulo P, Pasha TM, Egan K, Petz J, Lindor KD. Incidence and risk factors for cholangiocarcinoma in primary sclerosing cholangitis. Am J Gastroenterol 2004; 99 (03) 523-526
  • 50 Fevery J, Verslype C, Lai G, Aerts R, Van Steenbergen W. Incidence, diagnosis, and therapy of cholangiocarcinoma in patients with primary sclerosing cholangitis. Dig Dis Sci 2007; 52 (11) 3123-3135
  • 51 Zenouzi R, Weismüller TJ, Jørgensen KK. , et al. No evidence that azathioprine increases risk of cholangiocarcinoma in patients with primary sclerosing cholangitis. Clin Gastroenterol Hepatol 2016; 14 (12) 1806-1812
  • 52 Charatcharoenwitthaya P, Enders FB, Halling KC, Lindor KD. Utility of serum tumor markers, imaging, and biliary cytology for detecting cholangiocarcinoma in primary sclerosing cholangitis. Hepatology 2008; 48 (04) 1106-1117
  • 53 Saluja SS, Sharma R, Pal S, Sahni P, Chattopadhyay TK. Differentiation between benign and malignant hilar obstructions using laboratory and radiological investigations: a prospective study. HPB (Oxford) 2007; 9 (05) 373-382
  • 54 Hirschfield GM, Karlsen TH, Lindor KD, Adams DH. Primary sclerosing cholangitis. Lancet 2013; 382 (9904): 1587-1599
  • 55 Wennmacker SZ, Lamberts MP, Di Martino M, Drenth JP, Gurusamy KS, van Laarhoven CJ. Transabdominal ultrasound and endoscopic ultrasound for diagnosis of gallbladder polyps. Cochrane Database Syst Rev 2018; 8: CD012233
  • 56 Tang A, Bashir MR, Corwin MT. , et al; LI-RADS Evidence Working Group. Evidence supporting LI-RADS major features for CT- and MR imaging-based diagnosis of hepatocellular carcinoma: a systematic review. Radiology 2018; 286 (01) 29-48
  • 57 Ali AH, Tabibian JH, Nasser-Ghodsi N. , et al. Surveillance for hepatobiliary cancers in patients with primary sclerosing cholangitis. Hepatology 2018; 67 (06) 2338-2351
  • 58 Rizvi S, Eaton J, Yang JD, Chandrasekhara V, Gores GJ. Emerging technologies for the diagnosis of perihilar cholangiocarcinoma. Semin Liver Dis 2018; 38 (02) 160-169
  • 59 Kanda T, Ishii K, Kawaguchi H, Kitajima K, Takenaka D. High signal intensity in the dentate nucleus and globus pallidus on unenhanced T1-weighted MR images: relationship with increasing cumulative dose of a gadolinium-based contrast material. Radiology 2014; 270 (03) 834-841
  • 60 Kanda T, Fukusato T, Matsuda M. , et al. Gadolinium-based contrast agent accumulates in the brain even in subjects without severe renal dysfunction: evaluation of autopsy brain specimens with inductively coupled plasma mass spectroscopy. Radiology 2015; 276 (01) 228-232
  • 61 McDonald RJ, McDonald JS, Kallmes DF. , et al. Intracranial gadolinium deposition after contrast-enhanced MR imaging. Radiology 2015; 275 (03) 772-782
  • 62 Kahn J, Posch H, Steffen IG. , et al. Is there long-term signal intensity increase in the central nervous system on T1-weighted images after MR imaging with the hepatospecific contrast agent gadoxetic acid? a cross-sectional study in 91 patients. Radiology 2017; 282 (03) 708-716
  • 63 Radbruch A, Weberling LD, Kieslich PJ. , et al. Gadolinium retention in the dentate nucleus and globus pallidus is dependent on the class of contrast agent. Radiology 2015; 275 (03) 783-791
  • 64 Ramalho J, Castillo M, AlObaidy M. , et al. High signal intensity in globus pallidus and dentate nucleus on unenhanced T1-weighted MR images: evaluation of two linear gadolinium-based contrast agents. Radiology 2015; 276 (03) 836-844
  • 65 ACR Manual on Contrast Media Version 10.3. 2018 . Available at: http://www.acr.org/-/media/ACR/Files/Clinical-Resources/Contrast_Media.pdf . Accessed January 17, 2019
  • 66 Lauenstein T, Ramirez-Garrido F, Kim YH. , et al. Nephrogenic systemic fibrosis risk after liver magnetic resonance imaging with gadoxetate disodium in patients with moderate to severe renal impairment: results of a prospective, open-label, multicenter study. Invest Radiol 2015; 50 (06) 416-422
  • 67 Ponsioen CY, Chapman RW, Chazouillères O. , et al. Surrogate endpoints for clinical trials in primary sclerosing cholangitis: review and results from an International PSC Study Group consensus process. Hepatology 2016; 63 (04) 1357-1367
  • 68 Al Mamari S, Djordjevic J, Halliday JS, Chapman RW. Improvement of serum alkaline phosphatase to <1.5 upper limit of normal predicts better outcome and reduced risk of cholangiocarcinoma in primary sclerosing cholangitis. J Hepatol 2013; 58 (02) 329-334
  • 69 Rupp C, Rössler A, Halibasic E. , et al. Reduction in alkaline phosphatase is associated with longer survival in primary sclerosing cholangitis, independent of dominant stenosis. Aliment Pharmacol Ther 2014; 40 (11–12): 1292-1301
  • 70 Stanich PP, Björnsson E, Gossard AA, Enders F, Jorgensen R, Lindor KD. Alkaline phosphatase normalization is associated with better prognosis in primary sclerosing cholangitis. Dig Liver Dis 2011; 43 (04) 309-313
  • 71 Stiehl A. Primary sclerosing cholangitis: the role of endoscopic therapy. Semin Liver Dis 2006; 26 (01) 62-68
  • 72 Eaton JE, Vesterhus M, McCauley BM. , et al. Primary sclerosing cholangitis risk estimate tool (PREsTo) predicts outcomes of the disease: a derivation and validation study using machine learning. Hepatology 2018 ( e-pub ahead of print). doi: 10.1002/hep.30085
  • 73 Kim WR, Therneau TM, Wiesner RH. , et al. A revised natural history model for primary sclerosing cholangitis. Mayo Clin Proc 2000; 75 (07) 688-694
  • 74 de Vries EM, de Krijger M, Färkkilä M. , et al. Validation of the prognostic value of histologic scoring systems in primary sclerosing cholangitis: an international cohort study. Hepatology 2017; 65 (03) 907-919
  • 75 Kitzing YX, Whitley SA, Upponi SS, Srivastava B, Alexander GJ, Lomas DJ. Association between progressive hepatic morphology changes on serial MR imaging and clinical outcome in primary sclerosing cholangitis. J Med Imaging Radiat Oncol 2017; 61 (05) 636-642
  • 76 Campos JT, Sirlin CB, Choi JY. Focal hepatic lesions in Gd-EOB-DTPA enhanced MRI: the atlas. Insights Imaging 2012; 3 (05) 451-474
  • 77 Ni Mhuircheartaigh JM, Lee KS, Curry MP, Pedrosa I, Mortele KJ. Early peribiliary hyperenhancement on MRI in patients with primary sclerosing cholangitis: significance and association with the mayo risk score. Abdom Radiol (NY) 2017; 42 (01) 152-158
  • 78 Petrovic BD, Nikolaidis P, Hammond NA. , et al. Correlation between findings on MRCP and gadolinium-enhanced MR of the liver and a survival model for primary sclerosing cholangitis. Dig Dis Sci 2007; 52 (12) 3499-3506
  • 79 Ruiz A, Lemoinne S, Carrat F, Corpechot C, Chazouillères O, Arrivé L. Radiologic course of primary sclerosing cholangitis: assessment by three-dimensional magnetic resonance cholangiography and predictive features of progression. Hepatology 2014; 59 (01) 242-250
  • 80 Corpechot C, Gaouar F, El Naggar A. , et al. Baseline values and changes in liver stiffness measured by transient elastography are associated with severity of fibrosis and outcomes of patients with primary sclerosing cholangitis. Gastroenterology 2014; 146 (04) 970-979 , quiz e15–e16
  • 81 Ehlken H, Wroblewski R, Corpechot C. , et al. Validation of transient elastography and comparison with spleen length measurement for staging of fibrosis and clinical prognosis in primary sclerosing cholangitis. PLoS One 2016; 11 (10) e0164224
  • 82 Eaton JE, Dzyubak B, Venkatesh SK. , et al. Performance of magnetic resonance elastography in primary sclerosing cholangitis. J Gastroenterol Hepatol 2016; 31 (06) 1184-1190
  • 83 Jhaveri KS, Hosseini-Nik H, Sadoughi N. , et al. The development and validation of magnetic resonance elastography for fibrosis staging in primary sclerosing cholangitis. Eur Radiol 2019; 29 (02) 1039-1047
  • 84 Bookwalter CA, Venkatesh SK, Eaton JE, Smyrk TD, Ehman RL. MR elastography in primary sclerosing cholangitis: correlating liver stiffness with bile duct strictures and parenchymal changes. Abdom Radiol (NY) 2018; 43 (12) 3260-3270
  • 85 Ehlken H, Wroblewski R, Corpechot C. , et al. Spleen size for the prediction of clinical outcome in patients with primary sclerosing cholangitis. Gut 2016; 65 (07) 1230-1232
  • 86 Singh S, Venkatesh SK, Wang Z. , et al. Diagnostic performance of magnetic resonance elastography in staging liver fibrosis: a systematic review and meta-analysis of individual participant data. Clin Gastroenterol Hepatol 2015; 13 (03) 440.e6-451.e6
  • 87 Venkatesh SK, Wells ML, Miller FH. , et al. Magnetic resonance elastography: beyond liver fibrosis-a case-based pictorial review. Abdom Radiol (NY) 2018; 43 (07) 1590-1611
  • 88 Kovač JD, Daković M, Stanisavljević D. , et al. Diffusion-weighted MRI versus transient elastography in quantification of liver fibrosis in patients with chronic cholestatic liver diseases. Eur J Radiol 2012; 81 (10) 2500-2506
  • 89 Kovač JD, Ješić R, Stanisavljević D, Kovač B, Maksimovic R. MR imaging of primary sclerosing cholangitis: additional value of diffusion-weighted imaging and ADC measurement. Acta Radiol 2013; 54 (03) 242-248
  • 90 Keller S, Aigner A, Zenouzi R. , et al. Association of gadolinium-enhanced magnetic resonance imaging with hepatic fibrosis and inflammation in primary sclerosing cholangitis. PLoS One 2018; 13 (03) e0193929
  • 91 Keller S, Sedlacik J, Schuler T. , et al. Prospective comparison of diffusion-weighted MRI and dynamic Gd-EOB-DTPA-enhanced MRI for detection and staging of hepatic fibrosis in primary sclerosing cholangitis. Eur Radiol 2019; 29 (02) 818-828.
  • 92 House MJ, Bangma SJ, Thomas M. , et al. Texture-based classification of liver fibrosis using MRI. J Magn Reson Imaging 2015; 41 (02) 322-328
  • 93 Kato H, Kanematsu M, Zhang X. , et al. Computer-aided diagnosis of hepatic fibrosis: preliminary evaluation of MRI texture analysis using the finite difference method and an artificial neural network. AJR Am J Roentgenol 2007; 189 (01) 117-122
  • 94 Lubner MG, Malecki K, Kloke J, Ganeshan B, Pickhardt PJ. Texture analysis of the liver at MDCT for assessing hepatic fibrosis. Abdom Radiol (NY) 2017; 42 (08) 2069-2078
  • 95 Zhang X, Gao X, Liu BJ. , et al. Effective staging of fibrosis by the selected texture features of liver: which one is better, CT or MR imaging?. Comput Med Imaging Graph 2015; 46 (Pt 2): 227-236
  • 96 Wu Z, Matsui O, Kitao A. , et al. Hepatitis C related chronic liver cirrhosis: feasibility of texture analysis of MR images for classification of fibrosis stage and necroinflammatory activity grade. PLoS One 2015; 10 (03) e0118297
  • 97 Pickhardt PJ, Malecki K, Kloke J, Lubner MG. Accuracy of liver surface nodularity quantification on MDCT as a noninvasive biomarker for staging hepatic fibrosis. AJR Am J Roentgenol 2016; 207 (06) 1194-1199
  • 98 Smith AD, Branch CR, Zand K. , et al. Liver surface nodularity quantification from routine CT images as a biomarker for detection and evaluation of cirrhosis. Radiology 2016; 280 (03) 771-781
  • 99 Yin M, Glaser KJ, Manduca A. , et al. Distinguishing between hepatic inflammation and fibrosis with MR elastography. Radiology 2017; 284 (03) 694-705
  • 100 Guo J, Hirsch S, Streitberger KJ. , et al. Patient-activated three-dimensional multifrequency magnetic resonance elastography for high-resolution mechanical imaging of the liver and spleen. RoFo Fortschr Geb Rontgenstr Nuklearmed 2014; 186 (03) 260-266
  • 101 Loomba R, Cui J, Wolfson T. , et al. Novel 3D magnetic resonance elastography for the noninvasive diagnosis of advanced fibrosis in NAFLD: a prospective study. Am J Gastroenterol 2016; 111 (07) 986-994
  • 102 Narang S, Lehrer M, Yang D. , et al. Radiomics in glioblastoma: current status, challenges and potential opportunities. Transl Cancer Res 2016; 5: 383-397
  • 103 Atkinson EJ, Therneau TM, Melton III LJ. , et al. Assessing fracture risk using gradient boosting machine (GBM) models. J Bone Miner Res 2012; 27 (06) 1397-1404
  • 104 Ayaru L, Ypsilantis PP, Nanapragasam A. , et al. Prediction of outcome in acute lower gastrointestinal bleeding using gradient boosting. PLoS One 2015; 10 (07) e0132485
  • 105 Casanova R, Saldana S, Chew EY, Danis RP, Greven CM, Ambrosius WT. Application of random forests methods to diabetic retinopathy classification analyses. PLoS One 2014; 9 (06) e98587
  • 106 Kourou K, Exarchos TP, Exarchos KP, Karamouzis MV, Fotiadis DI. Machine learning applications in cancer prognosis and prediction. Comput Struct Biotechnol J 2014; 13: 8-17
  • 107 Maroco J, Silva D, Rodrigues A, Guerreiro M, Santana I, de Mendonça A. Data mining methods in the prediction of dementia: a real-data comparison of the accuracy, sensitivity and specificity of linear discriminant analysis, logistic regression, neural networks, support vector machines, classification trees and random forests. BMC Res Notes 2011; 4: 299
  • 108 Natekin A, Knoll A. Gradient boosting machines, a tutorial. Front Neurorobot 2013; 7: 21
  • 109 Weng SF, Reps J, Kai J, Garibaldi JM, Qureshi N. Can machine-learning improve cardiovascular risk prediction using routine clinical data?. PLoS One 2017; 12 (04) e0174944
  • 110 Chartrand G, Cresson T, Chav R, Gotra A, Tang A, De Guise JA. Liver segmentation on CT and MR using laplacian mesh optimization. IEEE Trans Biomed Eng 2017; 64 (09) 2110-2121
  • 111 Wang K, Lu X, Zhou H. , et al. Deep learning radiomics of shear wave elastography significantly improved diagnostic performance for assessing liver fibrosis in chronic hepatitis B: a prospective multicentre study. Gut 2018; gutjnl-2018-316204