Abstract
Objective
To assess the overall diagnostic accuracy of different MR imaging sequences in the detection of the dysplastic nodule (DN).
Methods
PubMed, Cochrane Library, and Web of Science were systematically searched. Study selection and data extraction were conducted by two authors independently. Quality assessment of diagnostic accuracy studies (QUADAS) 2 in RevMan software was used to score the included studies and assess their methodological quality. A random-effects model was used for statistical pooling by Meta-Disc. Subgroup analysis and sensitivity analysis were used to explore potential sources of heterogeneity.
Results
Fourteen studies (335 DN lesions in total) were included in our meta-analysis. The area under the curve (AUC) of summary receiver operating characteristic (SROC) of T2WI was 0.87. Pooled sensitivity, specificity, positive likelihood ratio (PLR), and negative likelihood ratio (NLR) of DWI were 0.81 (95%CI, 0.73–0.87), 0.90 (95%CI, 0.86–0.93), 7.04 (95%CI, 4.49–11.04), and 0.24 (95%CI, 0.17–0.33) respectively. In the arterial phase, pooled sensitivity, specificity, PLR, and NLR were 0.89 (0.84–0.93), 0.75 (0.72–0.79), 3.72 (2.51–5.51), and 0.17 (0.12–0.25), respectively. Pooled sensitivity, specificity, PLR, and NLR of the delayed phase were 0.78 (0.72–0.83), 0.60 (0.55–0.65), 2.19 (1.55–3.10), and 0.36 (0.23–0.55) separately. Pooled sensitivity, specificity, PLR, and NLR of the hepatobiliary phase were 0.77 (0.71–0.82), 0.92 (0.89–0.94), 8.74 (5.91–12.92), and 0.24 (0.14–0.41) respectively. Pooled sensitivity, specificity, and PLR were higher on DWI and hepatobiliary phase in diagnosing LGDN than HGDN.
Conclusion
MR sequences, particularly DWI, arterial phase, and hepatobiliary phase imaging demonstrate high diagnostic accuracy for DN.
Key Points
• MRI has dramatically improved the detection and accurate diagnosis of DNs and their differentiation from hepatocellular carcinoma.
• Overall diagnostic accuracy of different MRI sequences in the detection of DN has not been studied before.
• Our meta-analysis demonstrates that MRI achieves a high diagnostic value for DN, especially when using DWI, arterial phase imaging, and hepatobiliary phase imaging.
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Change history
01 October 2021
The term "country of origin" has been revised to "country or region of origin".
Abbreviations
- CI:
-
Confidence interval
- DN:
-
Dysplastic nodule
- HCC:
-
Hepatocellular carcinoma
- HGDN:
-
High-grade dysplastic nodule
- LGDN:
-
Low-grade dysplasia nodules
- QUADAS:
-
Quality assessment of diagnostic accuracy studies
References
Sato T, Kondo F, Ebara M et al (2015) Natural history of large regenerative nodules and dysplastic nodules in liver cirrhosis: 28-year follow-up study. Hepatol Int 9:330–336. https://doi.org/10.1007/s12072-015-9620-6
Kobayashi M, Ikeda K, Hosaka T et al (2006) Dysplastic nodules frequently develop into hepatocellular carcinoma in patients with chronic viral hepatitis and cirrhosis. Cancer 106:636–647. https://doi.org/10.1002/cncr.21607
Sano K, Ichikawa T, Motosugi U et al (2011) Imaging study of early hepatocellular carcinoma: usefulness of gadoxetic acid-enhanced MR imaging. Radiology 261:834–844. https://doi.org/10.1148/radiol.11101840
Park HJ, Choi BI, Lee ES, Park SB, Lee JB (2017) How to differentiate borderline hepatic nodules in hepatocarcinogenesis: emphasis on imaging diagnosis. Liver Cancer 6:189–203. https://doi.org/10.1159/000455949
Inchingolo R, Faletti R, Grazioli L et al (2018) MR with Gd-EOB-DTPA in assessment of liver nodules in cirrhotic patients. World J Hepatol 10:462–473. https://doi.org/10.4254/wjh.v10.i7.462
Ichikawa T, Sano K, Morisaka H (2014) Diagnosis of pathologically early HCC with EOB-MRI: experiences and current consensus. Liver Cancer 3:97–107. https://doi.org/10.1159/000343865
Chou CT, Chen YL, Wu HK, Chen RC (2011) Characterization of hyperintense nodules on precontrast T1-weighted MRI: utility of gadoxetic acid-enhanced hepatocyte-phase imaging. J Magn Reson Imaging 33:625–632. https://doi.org/10.1002/jmri.22500
Bartolozzi C, Battaglia V, Bargellini I et al (2013) Contrast-enhanced magnetic resonance imaging of 102 nodules in cirrhosis: correlation with histological findings on explanted livers. Abdom Imaging 38:290–296. https://doi.org/10.1007/s00261-012-9952-9
Shin SK, Kim YS, Choi SJ et al (2017) Characterization of small (</=3 cm) hepatic lesions with atypical enhancement feature and hypointensity in hepatobiliary phase of gadoxetic acid-enhanced MRI in cirrhosis: a STARD-compliant article. Medicine (Baltimore) 96:e7278. https://doi.org/10.1097/MD.0000000000007278
Xu PJ, Yan FH, Wang JH, Shan Y, Ji Y, Chen CZ (2010) Contribution of diffusion-weighted magnetic resonance imaging in the characterization of hepatocellular carcinomas and dysplastic nodules in cirrhotic liver. J Comput Assist Tomogr 34:506–512. https://doi.org/10.1097/RCT.0b013e3181da3671
Quaia E, De Paoli L, Pizzolato R et al (2013) Predictors of dysplastic nodule diagnosis in patients with liver cirrhosis on unenhanced and gadobenate dimeglumine-enhanced MRI with dynamic and hepatobiliary phase. AJR Am J Roentgenol 200:553–562. https://doi.org/10.2214/AJR.12.8818
Kogita S, Imai Y, Okada M et al (2010) Gd-EOB-DTPA-enhanced magnetic resonance images of hepatocellular carcinoma: correlation with histological grading and portal blood flow. Eur Radiol 20:2405–2413. https://doi.org/10.1007/s00330-010-1812-9
Gatto A, De Gaetano AM, Giuga M et al (2013) Differentiating hepatocellular carcinoma from dysplastic nodules at gadobenate dimeglumine-enhanced hepatobiliary-phase magnetic resonance imaging. Abdom Imaging 38:736–744. https://doi.org/10.1007/s00261-012-9950-y
Di Martino M, Anzidei M, Zaccagna F et al (2016) Qualitative analysis of small (</=2 cm) regenerative nodules, dysplastic nodules and well-differentiated HCCs with gadoxetic acid MRI. BMC Med Imaging 16:62. https://doi.org/10.1186/s12880-016-0165-5
Yoo HJ, Lee JM, Lee JY et al (2009) Additional value of SPIO-enhanced MR imaging for the noninvasive imaging diagnosis of hepatocellular carcinoma in cirrhotic liver. Invest Radiol 44:800–807. https://doi.org/10.1097/RLI.0b013e3181bc271d
Park MJ, Kim YK, Lee MH, Lee JH (2013) Validation of diagnostic criteria using gadoxetic acid-enhanced and diffusion-weighted MR imaging for small hepatocellular carcinoma (<= 2.0 cm) in patients with hepatitis-induced liver cirrhosis. Acta Radiol 54:127–136. https://doi.org/10.1258/ar.2012.120262
Wang YC, Chou CT, Lin CP, Chen YL, Chen YF, Chen RC (2017) The value of Gd-EOB-DTPA-enhanced MR imaging in characterizing cirrhotic nodules with atypical enhancement on Gd-DTPA-enhanced MR images. PLoS One 12:e0174594. https://doi.org/10.1371/journal.pone.0174594
Hwang J, Kim YK, Jeong WK, Choi D, Rhim H, Lee WJ (2015) Nonhypervascular hypointense nodules at gadoxetic acid-enhanced MR imaging in chronic liver disease: diffusion-weighted imaging for characterization. Radiology 276:137–146. https://doi.org/10.1148/radiol.15141350
Zhong X, Tang H, Lu B et al (2020) Differentiation of small hepatocellular carcinoma from dysplastic nodules in cirrhotic liver: texture analysis based on MRI improved performance in comparison over gadoxetic acid-enhanced MR and diffusion-weighted imaging. Front Oncol 9:1382. https://doi.org/10.3389/fonc.2019.01382
Whiting PF, Rutjes AW, Westwood ME et al (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155:529–536. https://doi.org/10.7326/0003-4819-155-8-201110180-00009
Mengoli C, Cruciani M, Barnes RA, Loeffler J, Donnelly JP (2009) Use of PCR for diagnosis of invasive aspergillosis: systematic review and meta-analysis. Lancet Infect Dis 9:89–96. https://doi.org/10.1016/S1473-3099(09)70019-2
Li C, Li X, Han H, Cui H, Wang G, Wang Z (2018) Diaphragmatic ultrasonography for predicting ventilator weaning: a meta-analysis. Medicine (Baltimore) 97:e10968. https://doi.org/10.1097/MD.0000000000010968
Lee HN, Ryu CW, Yun SJ (2018) Vessel-wall magnetic resonance imaging of intracranial atherosclerotic plaque and ischemic stroke: a systematic review and meta-analysis. Front Neurol 9:1032. https://doi.org/10.3389/fneur.2018.01032
Zamora J, Abraira V, Muriel A, Khan K, Coomarasamy A (2006) Meta-DiSc: a software for meta-analysis of test accuracy data. BMC Med Res Methodol 6:31. https://doi.org/10.1186/1471-2288-6-31
Chou CT, Chou JM, Chang TA et al (2013) Differentiation between dysplastic nodule and early-stage hepatocellular carcinoma: the utility of conventional MR imaging. World J Gastroenterol 19:7433–7439. https://doi.org/10.3748/wjg.v19.i42.7433
Pawluk RS, Tummala S, Brown JJ, Borrello JA (1999) A retrospective analysis of the accuracy of T2-weighted images and dynamic gadolinium-enhanced sequences in the detection and characterization of focal hepatic lesions. J Magn Reson Imaging 9:266–273. https://doi.org/10.1002/(sici)1522-2586(199902)9:2<266::aid-jmri17>3.0.co;2-7
Ward J, Baudouin CJ, Ridgway JP, Robinson PJ (1995) Magnetic resonance imaging in the detection of focal liver lesions: comparison of dynamic contrast-enhanced TurboFLASH and T2 weighted spin echo images. Br J Radiol 68:463–470. https://doi.org/10.1259/0007-1285-68-809-463
Shenoy-Bhangle A, Baliyan V, Kordbacheh H, Guimaraes AR, Kambadakone A (2017) Diffusion weighted magnetic resonance imaging of liver: principles, clinical applications and recent updates. World J Hepatol 9:1081–1091. https://doi.org/10.4254/wjh.v9.i26.1081
Matsui O, Kobayashi S, Sanada J et al (2011) Hepatocelluar nodules in liver cirrhosis: hemodynamic evaluation (angiography-assisted CT) with special reference to multi-step hepatocarcinogenesis. Abdom Imaging 36:264–272. https://doi.org/10.1007/s00261-011-9685-1
Golfieri R, Renzulli M, Lucidi V, Corcioni B, Trevisani F, Bolondi L (2011) Contribution of the hepatobiliary phase of Gd-EOB-DTPA-enhanced MRI to dynamic MRI in the detection of hypovascular small (</= 2 cm) HCC in cirrhosis. Eur Radiol 21:1233–1242. https://doi.org/10.1007/s00330-010-2030-1
Morana G, Grazioli L, Kirchin MA et al (2011) Solid hypervascular liver lesions: accurate identification of true benign lesions on enhanced dynamic and hepatobiliary phase magnetic resonance imaging after gadobenate dimeglumine administration. Invest Radiol 46:225–239. https://doi.org/10.1097/RLI.0b013e3181feee3a
Kim BR, Lee JM, Lee DH et al (2017) Diagnostic performance of gadoxetic acid-enhanced liver MR imaging versus multidetector CT in the detection of dysplastic nodules and early hepatocellular carcinoma. Radiology 285:134–146. https://doi.org/10.1148/radiol.2017162080
Choi JY, Lee JM, Sirlin CB (2014) CT and MR imaging diagnosis and staging of hepatocellular carcinoma: part I. Development, growth, and spread: key pathologic and imaging aspects. Radiology 272:635–654. https://doi.org/10.1148/radiol.14132361
Lee DH, Lee JM, Lee JY et al (2015) Non-hypervascular hepatobiliary phase hypointense nodules on gadoxetic acid-enhanced MRI: risk of HCC recurrence after radiofrequency ablation. J Hepatol 62:1122–1130. https://doi.org/10.1016/j.jhep.2014.12.015
Toyoda H, Kumada T, Tada T et al (2013) Non-hypervascular hypointense nodules detected by Gd-EOB-DTPA-enhanced MRI are a risk factor for recurrence of HCC after hepatectomy. J Hepatol 58:1174–1180. https://doi.org/10.1016/j.jhep.2013.01.030
Wang JH, Chen TY, Ou HY et al (2016) Clinical impact of gadoxetic acid-enhanced magnetic resonance imaging on hepatoma management: a prospective study. Dig Dis Sci 61:1197–1205. https://doi.org/10.1007/s10620-015-3989-x
Di Bisceglie AM (2009) Hepatitis B and hepatocellular carcinoma. Hepatology 49:S56–S60. https://doi.org/10.1002/hep.22962
Hytiroglou P (2017) Well-differentiated hepatocellular nodule: making a diagnosis on biopsy and resection specimens of patients with advanced stage chronic liver disease. Semin Diagn Pathol 34:138–145. https://doi.org/10.1053/j.semdp.2016.12.009
International Working P (1995) Terminology of nodular hepatocellular lesions. Hepatology 22:983–993. https://doi.org/10.1016/0270-9139(95)90324-0
Park YN (2011) Update on precursor and early lesions of hepatocellular carcinomas. Arch Pathol Lab Med 135:704–715. https://doi.org/10.1043/2010-0524-RA.1
Kierans AS, Kang SK, Rosenkrantz AB (2016) The diagnostic performance of dynamic contrast-enhanced MR imaging for detection of small hepatocellular carcinoma measuring Up to 2 cm: a meta-analysis. Radiology 278:82–94. https://doi.org/10.1148/radiol.2015150177
Pawlik TM, Delman KA, Vauthey JN et al (2005) Tumor size predicts vascular invasion and histologic grade: implications for selection of surgical treatment for hepatocellular carcinoma. Liver Transpl 11:1086–1092. https://doi.org/10.1002/lt.20472
Acknowledgements
This study was funded by the General Program of National Natural Science Foundation of China, contract grant number: 30870669.
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This study has received funding from the General Program of National Natural Science Foundation of China, contract grant number: 30870669.
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The scientific guarantor of this publication is Jie Bian.
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One of the authors (Jingtong Xiong) has significant statistical expertise.
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Xiong, J., Luo, J., Bian, J. et al. Overall diagnostic accuracy of different MR imaging sequences for detection of dysplastic nodules: a systematic review and meta-analysis. Eur Radiol 32, 1285–1296 (2022). https://doi.org/10.1007/s00330-021-08022-5
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DOI: https://doi.org/10.1007/s00330-021-08022-5