Performance of imaging modalities in the diagnosis of hepatocellular carcinoma: A systematic review and meta-analysis

Ultraschall in der Medizin

Volumn 34, Issue 5, 2013, Pages 454-462

  Floriani, I ^a   D'Onofrio, M ^b   Rulli, E ^a   Chen, M H ^c   Li, R ^d   Musicco, L ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b UNIVERSITY OF VERONA   (Italy)

^c PEKING UNIVERSITY CANCER HOSPITAL AND INSTITUTE   (China)

^d THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

diagnostic tests; hepatocellular carcinoma; systematic review

Indexed keywords

COMPARATIVE STUDY; COMPUTER ASSISTED TOMOGRAPHY; ECHOGRAPHY; HUMAN; LIVER; LIVER CELL CARCINOMA; LIVER TUMOR; META ANALYSIS; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; REVIEW; SENSITIVITY AND SPECIFICITY;

CARCINOMA, HEPATOCELLULAR; HUMANS; LIVER; LIVER NEOPLASMS; MAGNETIC RESONANCE IMAGING; SENSITIVITY AND SPECIFICITY; TOMOGRAPHY, X-RAY COMPUTED; ULTRASONOGRAPHY;

EID: 84885961640     PISSN: 01724614     EISSN: 14388782     Source Type: Journal    
DOI: 10.1055/s-0032-1330358     Document Type: Review

References (88)

1. Bruix J., Sherman M. Management of hepatocellular carcinoma. Hepatology: 2005; 42 1208 1236 (Pubitemid 43112690)
2. Bruix J., Sherman M. Management of hepatocellular carcinoma: an update. Hepatology 53 1020 1022
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
4. Reitsma J. B., Glas A. S., Rutjes A. W. et al. Bivariate analysis of sensitivity and specificity produces informative summary measures in diagnostic reviews. J Clin Epidemiol: 2005; 58 982 990 (Pubitemid 41316441)
5. DerSimonian R., Kacker R. Random-effects model for meta-analysis of clinical trials: an update. Contemp Clin Trials: 2007; 28 105 114 (Pubitemid 44937874)
6. Sterne J. A., Egger M. Funnel plots for detecting bias in meta-analysis: guidelines on choice of axis. J Clin Epidemiol: 2001; 54 1046 1055 (Pubitemid 32888370)
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 (Pubitemid 29036851)
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 (Pubitemid 34163995)
9. Verhoef C., Valkema R., de Man R. A. et al. Fluorine-18 FDG imaging in hepatocellular carcinoma using positron coincidence detection and single photon emission computed tomography. Liver: 2002; 22 51 56 (Pubitemid 34552525)
10. Kang B. K., Lim J. H., Kim S. H. et al. Preoperative depiction of hepatocellular carcinoma: ferumoxides-enhanced MR imaging versus triple-phase helical CT. Radiology: 2003; 226 79 85 (Pubitemid 36163911)
11. Kim S. H., Choi D., Lim J. H. et al. Ferucarbotran-enhanced MRI versus triple-phase MDCT for the preoperative detection of hepatocellular carcinoma. Am J Roentgenol: 2005; 184 1069 1076 (Pubitemid 43821878)
12. Kim S. J., Kim S. H., 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
13. Fracanzani A. L., 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 (Pubitemid 33096582)
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 (Pubitemid 46766888)
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
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
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 (Pubitemid 32440782)
18. Teefey S. A., Hildeboldt C. C., 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 (Pubitemid 36313446)
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
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 (Pubitemid 35277334)
21. Burrel M., Llovet J. M., 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 (Pubitemid 37221687)
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 (Pubitemid 38667509)
23. Krinsky G. A., Lee V. S., Theise N. D. et al. Transplantation for hepatocellular carcinoma and cirrhosis: sensitivity of magnetic resonance imaging. Liver Transpl: 2002; 8 1156 1164 (Pubitemid 35469878)
24. Bhartia B., Ward J., Guthrie J. A. 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 (Pubitemid 36237194)
25. Hecht E. M., Holland A. E., Israel G. M. 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
26. Lauenstein T. C., 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 (Pubitemid 47328550)
27. Hanna R. F., Kased N., Kwan S. W. et al. Double-contrast MRI for accurate staging of hepatocellular carcinoma in patients with cirrhosis. Am J Roentgenol: 2008; 190 47 57
28. Lee J. Y., Kim S. H., Jeon Y. H. 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
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 (Pubitemid 128516382)
30. Krinsky G. A., Lee V. S., Theise N. D. et al. Hepatocellular carcinoma and dysplastic nodules in patients with cirrhosis: prospective diagnosis with MR imaging and explantation correlation. Radiology: 2001; 219 445 454 (Pubitemid 32336360)
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 (Pubitemid 32105665)
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
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
34. Sahani D. V., Kalva S. P., Tanabe K. K. et al. Intraoperative US in patients undergoing surgery for liver neoplasms: comparison with MR imaging. Radiology: 2004; 232 810 814 (Pubitemid 39100267)
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 (Pubitemid 38680267)
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 (Pubitemid 40269956)
37. Wang C. S., Duan Q., Xue Y. J. 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
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
39. Yoo H. J., Lee J. M., Lee M. W. 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
40. Choi S. H., Lee J. M., Yu N. C. et al. Hepatocellular carcinoma in liver transplantation candidates: detection with gadobenate dimeglumine-enhanced MRI. Am J Roentgenol: 2008; 191 529 536
41. Yoo H. J., Lee J. M., Lee J. Y. 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
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
43. Lu C. H., Chen C. L., Cheng Y. F. et al. Correlation between imaging and pathologic findings in explanted livers of hepatocellular carcinoma cases. Transplant Proc 42 830 833
44. Xu P. J., Yan F. H., Wang J. H. 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
45. Chou C. T., Chen Y. L., Wu H. K. 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
46. Shapiro R. S., Katz R., Mendelson D. S. et al. Detection of hepatocellular carcinoma in cirrhotic patients: sensitivity of CT and ultrasonography. J Ultrasound Med: 1996; 15 497 502; quiz 504-504 (Pubitemid 26256405)
47. Lim J. H., Kim C. K., Lee W. J. 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
48. Peterson M. S., Baron R. L., Marsh J. W. Jr 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
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 (Pubitemid 34258352)
50. Lim J. H., Kim M. J., Chiang L. W. 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
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 (Pubitemid 47479759)
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
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 (Pubitemid 126709484)
54. Lopez Hanninen E., Vogl T. J., Bechstein W. O. et al. Biphasic spiral computed tomography for detection of hepatocellular carcinoma before resection or orthotopic liver transplantation. Invest Radiol: 1998; 33 216 221 (Pubitemid 28188883)
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
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 (Pubitemid 29281878)
57. Khan M. A., Combs C. S., Brunt E. M. et al. Positron emission tomography scanning in the evaluation of hepatocellular carcinoma. J Hepatol: 2000; 32 792 797 (Pubitemid 30262739)
58. Jang H. J., Lim J. H., Lee S. J. 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 (Pubitemid 30237830)
59. Gambarin-Gelwan M., Wolf D. C., 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 (Pubitemid 30396316)
60. Zhou K. R., Yan F. H., Tu B. W. Arterial phase of biphase enhancement spiral CT in diagnosis of small hepatocellular carcinoma. Hepatobiliary Pancreat Dis Int: 2002; 1 68 71
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 (Pubitemid 34919593)
62. Lim J. H., Choi D., Kim S. H. et al. Detection of hepatocellular carcinoma: value of adding delayed phase imaging to dual-phase helical CT. Am J Roentgenol: 2002; 179 67 73 (Pubitemid 34694813)
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 (Pubitemid 38391666)
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 (Pubitemid 44737925)
65. Doyle D. J., O'Malley M. E., Jang H. J. 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 (Pubitemid 46183345)
66. Hoque H. W., 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 (Pubitemid 351577660)
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
68. Addley H. C., Griffin N., Shaw A. S. et al. Accuracy of hepatocellular carcinoma detection on multidetector CT in a transplant liver population with explant liver correlation. Clin Radiol 66 349 356
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
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 (Pubitemid 37467586)
71. Chen M. H., 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
72. Chen M. H., Dai Y., Yan K. et al. The role of contrast-enhanced ultrasound on the diagnosis of small hepatocellular carcinoma (
73. Lanka B., Jang H. J., Kim T. K. et al. Impact of contrast-enhanced ultrasonography in a tertiary clinical practice. J Ultrasound Med: 2007; 26 1703 1714 (Pubitemid 350210078)
74. Kim Y. K., Kwak H. S., Kim C. S. 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 (Pubitemid 43134365)
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
76. Kwak H. S., Lee J. M., Kim C. S. 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
77. Jung G., Breuer J., Poll L. W. et al. Imaging characteristics of hepatocellular carcinoma using the hepatobiliary contrast agent Gd-EOB-DTPA. Acta Radiol: 2006; 47 15 23 (Pubitemid 43177525)
78. Lin M. T., Chen C. L., Wang C. C. et al. Diagnostic sensitivity of hepatocellular carcinoma imaging and its application to non-cirrhotic patients. J Gastroenterol Hepatol 26 745 750
79. Kim S. H., Lee J., Kim M. J. et al. Gadoxetic acid-enhanced MRI versus triple-phase MDCT for the preoperative detection of hepatocellular carcinoma. Am J Roentgenol: 2009; 192 1675 1681
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 (Pubitemid 46697187)
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 (Pubitemid 351171046)
82. Dai Y., Chen M. H., Fan Z. H. 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 (Pubitemid 351193957)
83. Mita K., Kim S. R., Kudo M. et al. Diagnostic sensitivity of imaging modalities for hepatocellular carcinoma smaller than 2 cm. World J Gastroenterol 16 4187 4192
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
85. Jiang X. Q., Xiao X. S., 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 (Pubitemid 351877579)
86. Park H. S., Lee J. M., Kim S. H. 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
87. Wang H., Mu X. T., Zhong X. Comparative study of dynamic MRI and MSCT in hepatocellular carcinoma with cirrhosis. Chinese Journal of Medical Imaging Technology: 2007; 23 1046 1048 (Pubitemid 47337391)
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 (Pubitemid 43340927)