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Ultraschall Med 2013; 34(5): 454-462
DOI: 10.1055/s-0032-1330358
Original Article
© Georg Thieme Verlag KG Stuttgart · New York

Performance of Imaging Modalities in the Diagnosis of Hepatocellular Carcinoma: a Systematic Review and Meta-Analysis

Leistungsfähigkeit der bildgebenden Verfahren bei der Diagnose des hepatozellulären Karzinoms: Systematischer Review und Metaanalyse
I. Floriani
1   Oncology department, Istituto di Ricerche Farmacologiche “Mario Negri”
,
M. D’Onofrio
2   Radiology, University of Verona
,
E. Rulli
1   Oncology department, Istituto di Ricerche Farmacologiche “Mario Negri”
,
M.-H. Chen
3   Department of Ultrasound, Peking University Cancer Hospital & Institute
,
R. Li
4   Department of Ultrasound, Southwest Hospital Affiliated to Third Military Medical University
,
L. Musicco
1   Oncology department, Istituto di Ricerche Farmacologiche “Mario Negri”
› Author Affiliations
Further Information

Publication History

08 August 2012

07 November 2012

Publication Date:
13 December 2012 (online)

Also available at
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Abstract

Purpose: The recent guidelines published in 2011 suggest the use of only one imaging method for the final imaging diagnosis of hepatocellular carcinoma. To evaluate the methods in the context of the available literature evidence, this systematic review aimed at assessing the relative performance of different imaging techniques currently used in clinical practice.

Materials and Methods: MEDLINE and EMBASE were searched from January 1996 to June 2011, with no language limitation. Eligible trials had to be conducted in patients with suspicion or diagnosis of hepatocellular carcinoma; compare at least two of the following imaging modalities: magnetic resonance imaging, computed tomography, ultrasound; have pathological findings as a reference standard. An analysis also including non-comparative studies was performed as a validation of the main comparison results.

Results: Of 5,144 screened papers, 16 studies fulfilled the eligibility criteria for the comparative analysis and 65 were eligible for the non-comparative analysis. The overall sensitivity and specificity derived by the pooled analysis were 0.78 and 0.77 for computed tomography, 0.84 and 0.84 for magnetic resonance imaging and 0.86 and 0.77 for ultrasound, respectively. In the pair-wise comparisons, ultrasound showed a statistically better specificity than magnetic resonance imaging (0.86 vs. 0.78; p = 0.014) and a statistically better sensitivity than computed tomography (0.88 vs. 0.78; p = 0.030).

Conclusion: The present systematic review did not show an obvious superiority of one imaging method. Since their accuracy is not completely overlapping, the possibility of reaching better performance by combining methods should be considered in future prospective trials.

Zusammenfassung

Ziel: Die im Jahr 2011 veröffentlichten aktuellen Leitlinien empfehlen beim hepatozellulären Karzinom, nur ein bildgebendes Verfahren zur endgültigen bildgebenden Diagnostik einzusetzen. Das Ziel dieses systematischen Reviews war es, durch die Auswertung der evidenten, verfügbaren Literatur die relative Leistung von verschiedenen, in der klinischen Praxis verwendeten bildgebenden Techniken zu bewerten.

Material und Methoden: Von Januar 1996 bis Juni 2011 wurden MEDLINE und EMBASE ohne Spracheinschränkungen durchsucht. Geeignete Studien sollten bei Patienten mit Verdachtsdiagnose bzw. diagnostisch bestätigtem hepatozellulärem Karzinom durchgeführt worden sein, wobei mindestens zwei der folgenden bildgebenden Methoden verglichen wurden: Magnetresonanztomografie, Computertomografie, Ultrasonografie. Zusätzlich sollten pathologische Befunde als Referenzstandard vorhanden sein. Es wurde eine Analyse durchgeführt, die auch nicht vergleichende Studien einschloss, um die wichtigsten Vergleichsresultate zu bewerten.

Ergebnisse: Von 5144 durchgesehenen Publikationen erfüllten 16 Studien die Eignungskriterien der vergleichenden Analyse und 65 waren für eine nicht vergleichende Analyse geeignet. Die aus der gepoolten Analyse abgeleiteten Gesamt-Sensitivitäten betragen für die Computertomografie 0,78, für die Magnetresonanztomografie 0,84 und für die Ultrasonografie 0,86, die Gesamt-Spezifitäten betragen für die Computertomografie 0,77, für die Magnetresonanztomografie 0,84 und für die Ultrasonografie 0,77. Beim paarweisen Vergleich zeigte die Ultrasonografie eine statistisch höhere Spezifität als die Magnetresonanztomografie (0,86 vs. 0,78; p = 0,014) und eine statistisch höhere Sensitivität als die Computertomografie (0,88 vs. 0,78; p = 0,030).

Schlussfolgerung: Da die diagnostische Genauigkeit nicht vollständig übereinstimmt wäre in zukünftigen prospektiven Studien zu prüfen, ob sich durch eine geschickte Methodenkombination die Ergebnisse verbessern ließen.

Key words

systematic review - hepatocellular carcinoma - diagnostic tests

Addendum

    Find Fig. 5 and Table 3 - 7
  • here
 

  • References

  • 1 Bruix J, Sherman M. Management of hepatocellular carcinoma. Hepatology 2005; 42: 1208-1236
    CrossrefPubMedSearch in Google Scholar
  • 2 Bruix J, Sherman M. Management of hepatocellular carcinoma: an update. Hepatology 53: 1020-1022
    PubMed
  • 3 Smidt E, Meissl K, Schwanninger M et al. Classification of waste materials using Fourier transform infrared spectroscopy and soft independent modeling of class analogy. Waste Manag 2008; 28: 1699-1710
    CrossrefPubMedSearch in Google Scholar
  • 4 Reitsma JB, Glas AS, Rutjes AW et al. Bivariate analysis of sensitivity and specificity produces informative summary measures in diagnostic reviews. J Clin Epidemiol 2005; 58: 982-990
    CrossrefPubMedSearch in Google Scholar
  • 5 DerSimonian R, Kacker R. Random-effects model for meta-analysis of clinical trials: an update. Contemp Clin Trials 2007; 28: 105-114
    CrossrefPubMedSearch in Google Scholar
  • 6 Sterne JA, Egger M. Funnel plots for detecting bias in meta-analysis: guidelines on choice of axis. J Clin Epidemiol 2001; 54: 1046-1055
    CrossrefPubMedSearch in Google Scholar
  • 7 Kanematsu M, Hoshi H, Yamada T et al. Small hepatic nodules in cirrhosis: ultrasonographic, CT, and MR imaging findings. Abdom Imaging 1999; 24: 47-55
    CrossrefPubMedSearch in Google Scholar
  • 8 de Ledinghen V, Laharie D, Lecesne R et al. Detection of nodules in liver cirrhosis: spiral computed tomography or magnetic resonance imaging? A prospective study of 88 nodules in 34 patients. Eur J Gastroenterol Hepatol 2002; 14: 159-165
    CrossrefPubMedSearch in Google Scholar
  • 9 Verhoef C, Valkema R, de Man RA et al. Fluorine-18 FDG imaging in hepatocellular carcinoma using positron coincidence detection and single photon emission computed tomography. Liver 2002; 22: 51-56
    Search in Google Scholar
  • 10 Kang BK, Lim JH, Kim SH et al. Preoperative depiction of hepatocellular carcinoma: ferumoxides-enhanced MR imaging versus triple-phase helical CT. Radiology 2003; 226: 79-85
    CrossrefPubMedSearch in Google Scholar
  • 11 Kim SH, Choi D, Lim JH et al. Ferucarbotran-enhanced MRI versus triple-phase MDCT for the preoperative detection of hepatocellular carcinoma. Am J Roentgenol 2005; 184: 1069-1076
    CrossrefPubMedSearch in Google Scholar
  • 12 Kim SJ, Kim SH, Lee J et al. Ferucarbotran-enhanced 3.0-T magnetic resonance imaging using parallel imaging technique compared with triple-phase multidetector row computed tomography for the preoperative detection of hepatocellular carcinoma. J Comput Assist Tomogr 2008; 32: 379-385
    CrossrefPubMedSearch in Google Scholar
  • 13 Fracanzani AL, Burdick L, Borzio M et al. Contrast-enhanced Doppler ultrasonography in the diagnosis of hepatocellular carcinoma and premalignant lesions in patients with cirrhosis. Hepatology 2001; 34: 1109-1112
    CrossrefPubMedSearch in Google Scholar
  • 14 Catala V, Nicolau C, Vilana R et al. Characterization of focal liver lesions: comparative study of contrast-enhanced ultrasound versus spiral computed tomography. Eur Radiol 2007; 17: 1066-1073
    CrossrefPubMedSearch in Google Scholar
  • 15 Quaia E, Alaimo V, Baratella E et al. The added diagnostic value of 64-row multidetector CT combined with contrast-enhanced US in the evaluation of hepatocellular nodule vascularity: implications in the diagnosis of malignancy in patients with liver cirrhosis. Eur Radiol 2009; 19: 651-663
    CrossrefPubMedSearch in Google Scholar
  • 16 Giorgio A, De Stefano G, Coppola C et al. Contrast-enhanced sonography in the characterization of small hepatocellular carcinomas in cirrhotic patients: comparison with contrast-enhanced ultrafast magnetic resonance imaging. Anticancer Res 2007; 27: 4263-4269
    PubMedSearch in Google Scholar
  • 17 Rode A, Bancel B, Douek P et al. Small nodule detection in cirrhotic livers: evaluation with US, spiral CT, and MRI and correlation with pathologic examination of explanted liver. J Comput Assist Tomogr 2001; 25: 327-336
    CrossrefPubMedSearch in Google Scholar
  • 18 Teefey SA, Hildeboldt CC, Dehdashti F et al. Detection of primary hepatic malignancy in liver transplant candidates: prospective comparison of CT, MR imaging, US, and PET. Radiology 2003; 226: 533-542
    CrossrefPubMedSearch in Google Scholar
  • 19 Blondin D, Erhardt A, Crynen K et al. [Diagnosis of focal liver lesions in cirrhotic patients: comparison of contrast-enhanced ultrasound using sulphur hexafluoride (SF6) microbubbles and MRI using Gd-EOB-DTPA]. Z Gastroenterol 49: 23-29
    Thieme ConnectPubMed
  • 20 Ishikawa M, Yogita S, Miyake H et al. Differential diagnosis of small hepatocellular carcinoma and borderline lesions and therapeutic strategy. Hepato-Gastroenterology 2002; 49: 1591-1596
    PubMedSearch in Google Scholar
  • 21 Burrel M, Llovet JM, Ayuso C et al. MRI angiography is superior to helical CT for detection of HCC prior to liver transplantation: An explant correlation. Hepatology 2003; 38: 1034-1042
    CrossrefPubMedSearch in Google Scholar
  • 22 Suzuki S, Iijima H, Moriyasu F et al. Differential diagnosis of hepatic nodules using delayed parenchymal phase imaging of levovist contrast ultrasound: Comparative study with SPIO-MRI. Hepatology Research 2004; 29: 122-126
    CrossrefPubMedSearch in Google Scholar
  • 23 Krinsky GA, Lee VS, Theise ND et al. Transplantation for hepatocellular carcinoma and cirrhosis: sensitivity of magnetic resonance imaging. Liver Transpl 2002; 8: 1156-1164
    CrossrefPubMedSearch in Google Scholar
  • 24 Bhartia B, Ward J, Guthrie JA et al. Hepatocellular carcinoma in cirrhotic livers: double-contrast thin-section MR imaging with pathologic correlation of explanted tissue. Am J Roentgenol 2003; 180: 577-584
    CrossrefPubMedSearch in Google Scholar
  • 25 Hecht EM, Holland AE, Israel GM et al. Hepatocellular carcinoma in the cirrhotic liver: gadolinium-enhanced 3D T1-weighted MR imaging as a stand-alone sequence for diagnosis. Radiology 2006; 239: 438-447
    CrossrefPubMedSearch in Google Scholar
  • 26 Lauenstein TC, Salman K, Morreira R et al. Gadolinium-enhanced MRI for tumor surveillance before liver transplantation: center-based experience. Am J Roentgenol 2007; 189: 663-670
    CrossrefPubMedSearch in Google Scholar
  • 27 Hanna RF, Kased N, Kwan SW et al. Double-contrast MRI for accurate staging of hepatocellular carcinoma in patients with cirrhosis. Am J Roentgenol 2008; 190: 47-57
    CrossrefPubMedSearch in Google Scholar
  • 28 Lee JY, Kim SH, Jeon YH et al. Ferucarbotran-enhanced magnetic resonance imaging versus gadoxetic acid-enhanced magnetic resonance imaging for the preoperative detection of hepatocellular carcinoma: initial experience. J Comput Assist Tomogr 34: 127-134
    PubMed
  • 29 Kajiwara M. MR imaging of small hepatocellular carcinoma (< or = 20 mm) – correlation with vascularity and histological features. Kurume Med J 1997; 44: 327-338
    CrossrefPubMedSearch in Google Scholar
  • 30 Krinsky GA, Lee VS, Theise ND et al. Hepatocellular carcinoma and dysplastic nodules in patients with cirrhosis: prospective diagnosis with MR imaging and explantation correlation. Radiology 2001; 219: 445-454
    CrossrefPubMedSearch in Google Scholar
  • 31 Choi D, Kim S, Lim J et al. Preoperative detection of hepatocellular carcinoma: ferumoxides-enhanced mr imaging versus combined helical CT during arterial portography and CT hepatic arteriography. Am J Roentgenol 2001; 176: 475-482
    CrossrefPubMedSearch in Google Scholar
  • 32 Yan F, Zhou K, Wu D et al. Evaluation of dynamic enhanced fast multiplanar spoiling gradient recalled (FMPSPGR) in the diagnosis of small hepatocellular carcinoma. Zhonghua Gan Zang Bing Za Zhi 2001; 9: 139-141
    PubMedSearch in Google Scholar
  • 33 Mori K, Scheidler J, Helmberger T et al. Detection of malignant hepatic lesions before orthotopic liver transplantation: accuracy of ferumoxides-enhanced MR imaging. Am J Roentgenol 2002; 179: 1045-1051
    CrossrefPubMedSearch in Google Scholar
  • 34 Sahani DV, Kalva SP, Tanabe KK et al. Intraoperative US in patients undergoing surgery for liver neoplasms: comparison with MR imaging. Radiology 2004; 232: 810-814
    CrossrefPubMedSearch in Google Scholar
  • 35 Bohm B, Voth M, Geoghegan J et al. Impact of positron emission tomography on strategy in liver resection for primary and secondary liver tumors. J Cancer Res Clin Oncol 2004; 130: 266-272
    CrossrefPubMedSearch in Google Scholar
  • 36 Kondo H, Kanematsu M, Itoh K et al. Does T2-weighted MR imaging improve preoperative detection of malignant hepatic tumors? Observer performance study in 49 surgically proven cases. Magn Reson Imaging 2005; 23: 89-95
    CrossrefPubMedSearch in Google Scholar
  • 37 Wang CS, Duan Q, Xue YJ. Application of 3.0T MRI 3D-VIBE dynamic contrast-enhanced in the diagnosis of small hepatocellular carcinomas. Zhonghua Gan Zang Bing Za Zhi 2008; 16: 905-908
    PubMedSearch in Google Scholar
  • 38 Wu H, Lu Q, Luo Y et al. Application of contrast-enhanced intraoperative ultrasonography in the decision-making about hepatocellular carcinoma operation. World J Gastroenterol 16: 508-512
    PubMed
  • 39 Yoo HJ, Lee JM, Lee MW et al. Hepatocellular carcinoma in cirrhotic liver: double-contrast-enhanced, high-resolution 3.0T-MR imaging with pathologic correlation. Invest Radiol 2008; 43: 538-546
    CrossrefPubMedSearch in Google Scholar
  • 40 Choi SH, Lee JM, Yu NC et al. Hepatocellular carcinoma in liver transplantation candidates: detection with gadobenate dimeglumine-enhanced MRI. Am J Roentgenol 2008; 191: 529-536
    CrossrefPubMedSearch in Google Scholar
  • 41 Yoo HJ, Lee JM, Lee JY et al. Additional value of SPIO-enhanced MR imaging for the noninvasive imaging diagnosis of hepatocellular carcinoma in cirrhotic liver. Invest Radiol 2009; 44: 800-807
    CrossrefPubMedSearch in Google Scholar
  • 42 Macarini L, Milillo P, Cascavilla A et al. MR characterisation of dysplastic nodules and hepatocarcinoma in the cirrhotic liver with hepatospecific superparamagnetic contrast agents: pathological correlation in explanted livers. Radiol Med 2009; 114: 1267-1282
    CrossrefPubMedSearch in Google Scholar
  • 43 Lu CH, Chen CL, Cheng YF et al. Correlation between imaging and pathologic findings in explanted livers of hepatocellular carcinoma cases. Transplant Proc 42: 830-833
    PubMed
  • 44 Xu PJ, Yan FH, Wang JH et al. 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
    PubMed
  • 45 Chou CT, Chen YL, Wu HK et al. Characterization of hyperintense nodules on precontrast T1-weighted MRI: utility of gadoxetic acid-enhanced hepatocyte-phase imaging. J Magn Reson Imaging 33: 625-632
    PubMed
  • 46 Shapiro RS, Katz R, Mendelson DS et al. Detection of hepatocellular carcinoma in cirrhotic patients: sensitivity of CT and ultrasonography. J Ultrasound Med 1996; 15: 497-502 ; quiz 504–504
    PubMedSearch in Google Scholar
  • 47 Lim JH, Kim CK, Lee WJ et al. Detection of hepatocellular carcinomas and dysplastic nodules in cirrhotic livers: accuracy of helical CT in transplant patients. Am J Roentgenol 2000; 175: 693-698
    CrossrefPubMedSearch in Google Scholar
  • 48 Peterson MS, Baron RL, Marsh Jr JW et al. Pretransplantation surveillance for possible hepatocellular carcinoma in patients with cirrhosis: epidemiology and CT-based tumor detection rate in 430 cases with surgical pathologic correlation. Radiology 2000; 217: 743-749
    CrossrefPubMedSearch in Google Scholar
  • 49 Zacherl J, Pokieser P, Wrba F et al. Accuracy of multiphasic helical computed tomography and intraoperative sonography in patients undergoing orthotopic liver transplantation for hepatoma: what is the truth?. Ann Surg 2002; 235: 528-532
    CrossrefPubMedSearch in Google Scholar
  • 50 Lim JH, Kim MJ, Chiang LW et al. CT detection of hepatocellular carcinoma in advanced liver cirrhosis: correlation of helical CT and explanted liver. Taehan Kan Hakhoe Chi 2002; 8: 201-208
    PubMedSearch in Google Scholar
  • 51 Ronzoni A, Artioli D, Scardina R et al. Role of MDCT in the diagnosis of hepatocellular carcinoma in patients with cirrhosis undergoing orthotopic liver transplantation. Am J Roentgenol 2007; 189: 792-798
    CrossrefPubMedSearch in Google Scholar
  • 52 Denecke T, Grieser C, Froling V et al. Multislice computed tomography using a triple-phase contrast protocol for preoperative assessment of hepatic tumor load in patients with hepatocellular carcinoma before liver transplantation. Transpl Int 2009; 22: 395-402
    CrossrefPubMedSearch in Google Scholar
  • 53 Arakawa A, Nishiharu T, Matsukawa T et al. Detection of hepatocellular carcinoma by intraarterially enhanced ultrasonography with CO2 microbubbles. Comparison with DSA, dynamic CT, and Lipiodol CT. Acta Radiol 1996; 37: 250-254
    CrossrefPubMedSearch in Google Scholar
  • 54 Lopez Hanninen E, Vogl TJ, Bechstein WO et al. Biphasic spiral computed tomography for detection of hepatocellular carcinoma before resection or orthotopic liver transplantation. Invest Radiol 1998; 33: 216-221
    CrossrefPubMedSearch in Google Scholar
  • 55 Trojan J, Schroeder O, Raedle J et al. Fluorine-18 FDG positron emission tomography for imaging of hepatocellular carcinoma. Am J Gastroenterol 1999; 94: 3314-3319
    CrossrefPubMedSearch in Google Scholar
  • 56 Horigome H, Nomura T, Saso K et al. Limitations of imaging diagnosis for small hepatocellular carcinoma: comparison with histological findings. J Gastroenterol Hepatol 1999; 14: 559-565
    CrossrefPubMedSearch in Google Scholar
  • 57 Khan MA, Combs CS, Brunt EM et al. Positron emission tomography scanning in the evaluation of hepatocellular carcinoma. J Hepatol 2000; 32: 792-797
    PubMedSearch in Google Scholar
  • 58 Jang HJ, Lim JH, Lee SJ et al. Hepatocellular carcinoma: are combined CT during arterial portography and CT hepatic arteriography in addition to triple-phase helical CT all necessary for preoperative evaluation?. Radiology 2000; 215: 373-380
    CrossrefPubMedSearch in Google Scholar
  • 59 Gambarin-Gelwan M, Wolf DC, Shapiro R et al. Sensitivity of commonly available screening tests in detecting hepatocellular carcinoma in cirrhotic patients undergoing liver transplantation. Am J Gastroenterol 2000; 95: 1535-1538
    CrossrefPubMedSearch in Google Scholar
  • 60 Zhou KR, Yan FH, Tu BW. Arterial phase of biphase enhancement spiral CT in diagnosis of small hepatocellular carcinoma. Hepatobiliary Pancreat Dis Int 2002; 1: 68-71
    PubMedSearch in Google Scholar
  • 61 Ichikawa T, Kitamura T, Nakajima H et al. Hypervascular hepatocellular carcinoma: can double arterial phase imaging with multidetector CT improve tumor depiction in the cirrhotic liver?. Am J Roentgenol 2002; 179: 751-758
    CrossrefPubMedSearch in Google Scholar
  • 62 Lim JH, Choi D, Kim SH et al. Detection of hepatocellular carcinoma: value of adding delayed phase imaging to dual-phase helical CT. Am J Roentgenol 2002; 179: 67-73
    CrossrefPubMedSearch in Google Scholar
  • 63 Valls C, Cos M, Figueras J et al. Pretransplantation diagnosis and staging of hepatocellular carcinoma in patients with cirrhosis: value of dual-phase helical CT. Am J Roentgenol 2004; 182: 1011-1017
    CrossrefPubMedSearch in Google Scholar
  • 64 Rizvi S, Camci C, Yong Y et al. Is post-Lipiodol CT better than i.v. contrast CT scan for early detection of HCC? A single liver transplant center experience. Transplant Proc 2006; 38: 2993-2995
    CrossrefPubMedSearch in Google Scholar
  • 65 Doyle DJ, O’Malley ME, Jang HJ et al. Value of the unenhanced phase for detection of hepatocellular carcinomas 3 cm or less when performing multiphase computed tomography in patients with cirrhosis. J Comput Assist Tomogr 2007; 31: 86-92
    CrossrefPubMedSearch in Google Scholar
  • 66 Hoque HW, Alam S, Ahsan S et al. Ultrasonography and computer tomography evaluation of hepatocellular carcinoma with cytohistopathological correlation. Bangladesh Med Res Counc Bull 2007; 33: 73-77
    PubMedSearch in Google Scholar
  • 67 Luca A, Caruso S, Milazzo M et al. Multidetector-row computed tomography (MDCT) for the diagnosis of hepatocellular carcinoma in cirrhotic candidates for liver transplantation: prevalence of radiological vascular patterns and histological correlation with liver explants. Eur Radiol 20: 898-907
    PubMed
  • 68 Addley HC, Griffin N, Shaw AS et al. Accuracy of hepatocellular carcinoma detection on multidetector CT in a transplant liver population with explant liver correlation. Clin Radiol 66: 349-356
    PubMed
  • 69 Furlan A, Marin D, Vanzulli A et al. Hepatocellular carcinoma in cirrhotic patients at multidetector CT: hepatic venous phase versus delayed phase for the detection of tumour washout. Br J Radiol 84: 403-412
    PubMed
  • 70 Isozaki T, Numata K, Kiba T et al. Differential diagnosis of hepatic tumors by using contrast enhancement patterns at US. Radiology 2003; 229: 798-805
    CrossrefPubMedSearch in Google Scholar
  • 71 Chen MH, Dai Y, Yan K et al. Early diagnosis of small hepatocellular carcinoma by new contrast-enhanced ultrasound technique. Beijing Da Xue Xue Bao 2005; 37: 458-462
    PubMedSearch in Google Scholar
  • 72 Chen MH, Dai Y, Yan K et al. The role of contrast-enhanced ultrasound on the diagnosis of small hepatocellular carcinoma (</= 3 cm) in patients with cirrhosis. Hepatol Res 2006; 35: 281-288
    CrossrefPubMedSearch in Google Scholar
  • 73 Lanka B, Jang HJ, Kim TK et al. Impact of contrast-enhanced ultrasonography in a tertiary clinical practice. J Ultrasound Med 2007; 26: 1703-1714
    PubMedSearch in Google Scholar
  • 74 Kim YK, Kwak HS, Kim CS et al. Hepatocellular carcinoma in patients with chronic liver disease: comparison of SPIO-enhanced MR imaging and 16-detector row CT. Radiology 2006; 238: 531-541
    CrossrefPubMedSearch in Google Scholar
  • 75 Wagnetz U, Atri M, Massey C et al. Intraoperative ultrasound of the liver in primary and secondary hepatic malignancies: comparison with preoperative 1.5-T MRI and 64-MDCT. Am J Roentgenol 196: 562-568
    PubMed
  • 76 Kwak HS, Lee JM, Kim CS. Preoperative detection of hepatocellular carcinoma: comparison of combined contrast-enhanced MR imaging and combined CT during arterial portography and CT hepatic arteriography. Eur Radiol 2004; 14: 447-457
    CrossrefPubMedSearch in Google Scholar
  • 77 Jung G, Breuer J, Poll LW et al. Imaging characteristics of hepatocellular carcinoma using the hepatobiliary contrast agent Gd-EOB-DTPA. Acta Radiol 2006; 47: 15-23
    CrossrefPubMedSearch in Google Scholar
  • 78 Lin MT, Chen CL, Wang CC et al. Diagnostic sensitivity of hepatocellular carcinoma imaging and its application to non-cirrhotic patients. J Gastroenterol Hepatol 26: 745-750
    PubMed
  • 79 Kim SH, Lee J, Kim MJ et al. Gadoxetic acid-enhanced MRI versus triple-phase MDCT for the preoperative detection of hepatocellular carcinoma. Am J Roentgenol 2009; 192: 1675-1681
    CrossrefPubMedSearch in Google Scholar
  • 80 Li R, Guo Y, Hua X et al. Characterization of focal liver lesions: comparison of pulse-inversion harmonic contrast-enhanced sonography with contrast-enhanced CT. J Clin Ultrasound 2007; 35: 109-117
    CrossrefPubMedSearch in Google Scholar
  • 81 Forner A, Vilana R, Ayuso C et al. Diagnosis of hepatic nodules 20 mm or smaller in cirrhosis: Prospective validation of the noninvasive diagnostic criteria for hepatocellular carcinoma. Hepatology 2008; 47: 97-104
    CrossrefPubMedSearch in Google Scholar
  • 82 Dai Y, Chen MH, Fan ZH et al. Diagnosis of small hepatic nodules detected by surveillance ultrasound in patients with cirrhosis: Comparison between contrast-enhanced ultrasound and contrast-enhanced helical computed tomography. Hepatol Res 2008; 38: 281-290
    CrossrefPubMedSearch in Google Scholar
  • 83 Mita K, Kim SR, Kudo M et al. Diagnostic sensitivity of imaging modalities for hepatocellular carcinoma smaller than 2 cm. World J Gastroenterol 16: 4187-4192
    PubMed
  • 84 Kawada N, Ohkawa K, Tanaka S et al. Improved diagnosis of well-differentiated hepatocellular carcinoma with gadolinium ethoxybenzyl diethylene triamine pentaacetic acid-enhanced magnetic resonance imaging and Sonazoid contrast-enhanced ultrasonography. Hepatol Res 40: 930-936
    PubMed
  • 85 Jiang XQ, Xiao XS, Xie Q et al. Detection of hepatocellular carcinoma with multi-slices sprial CT by using double-arterial phase and portal venous phase enhanced scanning. Chinese Journal of Radiology 2008; 42: 628-631
    PubMedSearch in Google Scholar
  • 86 Park HS, Lee JM, Kim SH et al. Differentiation of well-differentiated hepatocellular carcinomas from other hepatocellular nodules in cirrhotic liver: Value of SPIO-enhanced MR imaging at 3.0 tesla. Journal of Magnetic Resonance Imaging 2009; 29: 328-335
    CrossrefPubMedSearch in Google Scholar
  • 87 Wang H, Mu XT, Zhong X. Comparative study of dynamic MRI and MSCT in hepatocellular carcinoma with cirrhosis. Chinese Journal of Medical Imaging Technology 2007; 23: 1046-1048
    PubMedSearch in Google Scholar
  • 88 Colli A, Fraquelli M, Casazza G et al. Accuracy of ultrasonography, spiral CT, magnetic resonance, and alpha-fetoprotein in diagnosing hepatocellular carcinoma: a systematic review. Am J Gastroenterol 2006; 101: 513-523
    CrossrefPubMedSearch in Google Scholar