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Non-enhanced magnetic resonance imaging as a surveillance tool for hepatocellular carcinoma: Comparison with ultrasound

  • Author Footnotes
    † These authors contributed equally to this work as co-first authors.
    Hyo Jung Park
    Footnotes
    † These authors contributed equally to this work as co-first authors.
    Affiliations
    Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
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  • Author Footnotes
    † These authors contributed equally to this work as co-first authors.
    Hye Young Jang
    Footnotes
    † These authors contributed equally to this work as co-first authors.
    Affiliations
    Department of Radiology, National Cancer Center, Gyeonggi-do, Republic of Korea
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  • So Yeon Kim
    Correspondence
    Corresponding author. Address: Department of Radiology, Asan Medical Center, University of Ulsan College of Medicine, 88 Olympic-ro 43-gil, Songpa-gu, Seoul 05505, Republic of Korea. Tel.: 82-2-3010-5980; Fax: 82-2-476-4719.
    Affiliations
    Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
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  • So Jung Lee
    Affiliations
    Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
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  • Hyung Jin Won
    Affiliations
    Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
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  • Jae Ho Byun
    Affiliations
    Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
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  • Sang Hyun Choi
    Affiliations
    Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
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  • Seung Soo Lee
    Affiliations
    Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
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  • Jihyun An
    Affiliations
    Department of Gastroenterology and Hepatology, Hanyang University of Medicine, Guri, Republic of Korea
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  • Young-Suk Lim
    Affiliations
    Department of Gastroenterology, Liver Center, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
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  • Author Footnotes
    † These authors contributed equally to this work as co-first authors.
Published:December 10, 2019DOI:https://doi.org/10.1016/j.jhep.2019.12.001

      Highlights

      • Non-enhanced MRI consisted of diffusion-weighted and T2-weighted imaging.
      • Non-enhanced MRI showed significantly higher sensitivity and specificity than ultrasonography for HCC detection.
      • The estimated scan time of non-enhanced MRI was less than 6 min with a total of 25–35 min of room occupancy.
      • Given the good performance and lack of contrast agent-associated risks, non-enhanced MRI has potential for HCC surveillance.

      Background & Aims

      Recently revised international guidelines for hepatocellular carcinoma (HCC) suggest that patients with inadequate ultrasonography be assessed by alternative imaging modalities. Non-enhanced MRI has potential as a surveillance tool based on the short scan times required and the absence of contrast agent-associated risks. This study compared the performance of non-enhanced MRI and ultrasonography for HCC surveillance in high-risk patients.

      Methods

      We included 382 high-risk patients in a prospective cohort who underwent 1 to 3 rounds of paired gadoxetic acid-enhanced MRI and ultrasonography. Non-enhanced MRI, consisting of diffusion-weighted imaging (DWI) and T2-weighted imaging, was simulated and retrospectively analyzed, with results considered positive when lesion(s) ≥1 cm showed diffusion restriction or mild–moderate T2 hyperintensity. Ultrasonography results were retrieved from patient records. HCC was diagnosed histologically and/or radiologically. Sensitivity, positive predictive value (PPV), specificity, and negative predictive value (NPV) were evaluated using generalized estimating equations.

      Results

      Forty-eight HCCs were diagnosed in 43 patients. Per-lesion and per-exam sensitivities of non-enhanced MRI were 77.1% and 79.1%, respectively, which were higher than those achieved with ultrasonography (25.0% and 27.9%, respectively, p <0.001). Specificities of non-enhanced MRI (97.9%) and ultrasonography (94.5%) differed significantly (p <0.001). NPV was higher for non-enhanced MRI (99.1%) than ultrasonography (96.9%). Per-lesion and per-exam PPVs were higher for non-enhanced MRI (56.9% and 61.8%, respectively) than for ultrasonography (16.7% and 17.7%, respectively). The estimated scan time of non-enhanced MRI was <6 min.

      Conclusion

      Based on its good performance, short scan times, and the lack of contrast agent-associated risks, non-enhanced MRI is a promising option for HCC surveillance in high-risk patients.

      Lay summary

      Recently revised international guidelines for hepatocellular carcinoma (HCC) suggest that selected patients with inadequate surveillance on ultrasonography be assessed by alternative imaging modalities such as computed tomography or magnetic resonance imaging (MRI). Herein, we show that MRI without contrast agents performed significantly better than ultrasonography for HCC surveillance in high-risk patients. Given this good performance, as well as short scan times and the lack of contrast agent-associated risks, non-enhanced MRI is a promising option for HCC surveillance in high-risk patients.

      Graphical abstract

      Keywords

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      References

        • Marrero J.A.
        • Kulik L.M.
        • Sirlin C.B.
        • Zhu A.X.
        • Finn R.S.
        • Abecassis M.M.
        • et al.
        Diagnosis, staging, and management of hepatocellular carcinoma: 2018 Practice Guidance by the American Association for the Study of Liver Diseases.
        Hepatology. 2018; 68: 723-750
        • European Association for the Study of the Liver
        EASL Clinical Practice Guidelines: management of hepatocellular carcinoma.
        J Hepatol. 2018; 69: 182-236
        • Korean Liver Cancer Association
        • National Cancer Center
        2018 Korean Practice Guideline for the Management of Hepatocellular Carcinoma.
        Korean Liver Cancer Association, National Cancer Center, Seoul2018
        • Singal A.
        • Volk M.L.
        • Waljee A.
        • Salgia R.
        • Higgins P.
        • Rogers M.A.
        • et al.
        Meta-analysis: surveillance with ultrasound for early-stage hepatocellular carcinoma in patients with cirrhosis.
        Aliment Pharmacol Ther. 2009; 30: 37-47
        • Tzartzeva K.
        • Obi J.
        • Rich N.E.
        • Parikh N.D.
        • Marrero J.A.
        • Yopp A.
        • et al.
        Surveillance imaging and alpha fetoprotein for early detection of hepatocellular carcinoma in patients with cirrhosis: a meta-analysis.
        Gastroenterology. 2018; 154: 1706-1718.e1
        • Kim S.Y.
        • An J.
        • Lim Y.S.
        • Han S.
        • Lee J.Y.
        • Byun J.H.
        • et al.
        MRI with liver-specific contrast for surveillance of patients with cirrhosis at high risk of hepatocellular carcinoma.
        JAMA Oncol. 2017; 3: 456-463
        • Pocha C.
        • Dieperink E.
        • McMaken K.A.
        • Knott A.
        • Thuras P.
        • Ho S.B.
        Surveillance for hepatocellular cancer with ultrasonography vs. computed tomography – a randomised study.
        Aliment Pharmacol Ther. 2013; 38: 303-312
        • Besa C.
        • Lewis S.
        • Pandharipande P.V.
        • Chhatwal J.
        • Kamath A.
        • Cooper N.
        • et al.
        Hepatocellular carcinoma detection: diagnostic performance of a simulated abbreviated MRI protocol combining diffusion-weighted and T1-weighted imaging at the delayed phase post gadoxetic acid.
        Abdom Radiol (NY). 2017; 42: 179-190
        • Marks R.M.
        • Ryan A.
        • Heba E.R.
        • Tang A.
        • Wolfson T.J.
        • Gamst A.C.
        • et al.
        Diagnostic per-patient accuracy of an abbreviated hepatobiliary phase gadoxetic acid-enhanced MRI for hepatocellular carcinoma surveillance.
        AJR Am J Roentgenol. 2015; 204: 527-535
        • Park M.J.
        • Kim Y.K.
        • Lee M.W.
        • Lee W.J.
        • Kim Y.S.
        • Kim S.H.
        • et al.
        Small hepatocellular carcinomas: improved sensitivity by combining gadoxetic acid-enhanced and diffusion-weighted MR imaging patterns.
        Radiology. 2012; 264: 761-770
        • Piana G.
        • Trinquart L.
        • Meskine N.
        • Barrau V.
        • Beers B.V.
        • Vilgrain V.
        New MR imaging criteria with a diffusion-weighted sequence for the diagnosis of hepatocellular carcinoma in chronic liver diseases.
        J Hepatol. 2011; 55: 126-132
        • Tillman B.G.
        • Gorman J.D.
        • Hru J.M.
        • Lee M.H.
        • King M.C.
        • Sirlin C.B.
        • et al.
        Diagnostic per-lesion performance of a simulated gadoxetate disodium-enhanced abbreviated MRI protocol for hepatocellular carcinoma screening.
        Clin Radiol. 2018; 73: 485-493
        • Brenner D.J.
        • Hall E.J.
        Computed tomography--an increasing source of radiation exposure.
        N Engl J Med. 2007; 357: 2277-2284
        • Hanna R.F.
        • Miloushev V.Z.
        • Tang A.
        • Finklestone L.A.
        • Brejt S.Z.
        • Sandhu R.S.
        • et al.
        Comparative 13-year meta-analysis of the sensitivity and positive predictive value of ultrasound, CT, and MRI for detecting hepatocellular carcinoma.
        Abdom Radiol (NY). 2016; 41: 71-90
        • Lee Y.J.
        • Lee J.M.
        • Lee J.S.
        • Lee H.Y.
        • Park B.H.
        • Kim Y.H.
        • et al.
        Hepatocellular carcinoma: diagnostic performance of multidetector CT and MR imaging-a systematic review and meta-analysis.
        Radiology. 2015; 275: 97-109
        • Rogosnitzky M.
        • Branch S.
        Gadolinium-based contrast agent toxicity: a review of known and proposed mechanisms.
        Biometals. 2016; 29: 365-376
        • Levine D.
        • McDonald R.J.
        • Kressel H.Y.
        Gadolinium retention after contrast-enhanced MRI.
        JAMA. 2018; 320: 1853-1854
        • Kim Y.K.
        • Kim Y.K.
        • Park H.J.
        • Park M.J.
        • Lee W.J.
        • Choi D.
        Noncontrast MRI with diffusion-weighted imaging as the sole imaging modality for detecting liver malignancy in patients with high risk for hepatocellular carcinoma.
        Magn Reson Imaging. 2014; 32: 610-618
        • Han S.
        • Choi J.I.
        • Park M.Y.
        • Choi M.H.
        • Rha S.E.
        • Lee Y.J.
        The diagnostic performance of liver MRI without intravenous contrast for detecting hepatocellular carcinoma: a case-controlled feasibility study.
        Korean J Radiol. 2018; 19: 568-577
        • Kim Y.K.
        • Lee W.J.
        • Park M.J.
        • Kim S.H.
        • Rhim H.
        • Choi D.
        Hypovascular hypointense nodules on hepatobiliary phase gadoxetic acid-enhanced MR images in patients with cirrhosis: potential of DW imaging in predicting progression to hypervascular HCC.
        Radiology. 2012; 265: 104-114
        • Vandecaveye V.
        • De Keyzer F.
        • Verslype C.
        • Op de Beeck K.
        • Komuta M.
        • Topal B.
        • et al.
        Diffusion-weighted MRI provides additional value to conventional dynamic contrast-enhanced MRI for detection of hepatocellular carcinoma.
        Eur Radiol. 2009; 19: 2456-2466
        • Velazquez R.F.
        • Rodriguez M.
        • Navascues C.A.
        • Linares A.
        • Perez R.
        • Sotorrios N.G.
        • et al.
        Prospective analysis of risk factors for hepatocellular carcinoma in patients with liver cirrhosis.
        Hepatology. 2003; 37: 520-527
        • American College of Radiology
        CT/MRI LI-RADS® v2018 Core.
        (Available from:)
        • Kim H.D.
        • Lim Y.S.
        • Han S.
        • An J.
        • Kim G.A.
        • Kim S.Y.
        • et al.
        Evaluation of early Stage hepatocellular carcinoma by magnetic resonance imaging with gadoxetic acid detects additional lesions and increases overall survival.
        Gastroenterology. 2015; 148: 1371-1382
        • Bruix J.
        • Sherman M.
        • American Association for the Study of Liver Disease
        Management of hepatocellular carcinoma: an update.
        Hepatology. 2011; 53: 1020-1022
        • Liu W.C.
        • Lim J.H.
        • Park C.K.
        • Kim M.J.
        • Kim S.H.
        • Lee S.J.
        • et al.
        Poor sensitivity of sonography in detection of hepatocellular carcinoma in advanced liver cirrhosis: accuracy of pretransplantation sonography in 118 patients.
        Eur Radiol. 2003; 13: 1693-1698
        • Singal A.G.
        • Nehra M.
        • Adams-Huet B.
        • Yopp A.C.
        • Tiro J.A.
        • Marrero J.A.
        • et al.
        Detection of hepatocellular carcinoma at advanced stages among patients in the HALT-C trial: where did surveillance fail?.
        Am J Gastroenterol. 2013; 108: 425-432
        • Del Poggio P.
        • Olmi S.
        • Ciccarese F.
        • Di Marco M.
        • Rapaccini G.L.
        • Benvegnu L.
        • et al.
        Factors that affect efficacy of ultrasound surveillance for early stage hepatocellular carcinoma in patients with cirrhosis.
        Clin Gastroenterol Hepatol. 2014; 12: 1927-1933.e2
        • Yu N.C.
        • Chaudhari V.
        • Raman S.S.
        • Lassman C.
        • Tong M.J.
        • Busuttil R.W.
        • et al.
        CT and MRI improve detection of hepatocellular carcinoma, compared with ultrasound alone, in patients with cirrhosis.
        Clin Gastroenterol Hepatol. 2011; 9: 161-167
        • Modica M.J.
        • Kanal K.M.
        • Gunn M.L.
        The obese emergency patient: imaging challenges and solutions.
        Radiographics. 2011; 31: 811-823
        • Kudo M.
        Management of hepatocellular carcinoma in Japan as a world-leading model.
        Liver Cancer. 2018; 7: 134-147
        • Goossens N.
        • Singal A.G.
        • King L.Y.
        • Andersson K.L.
        • Fuchs B.C.
        • Besa C.
        • et al.
        Cost-effectiveness of risk score-stratified hepatocellular carcinoma screening in patients with cirrhosis.
        Clin Transl Gastroenterol. 2017; 8: e101