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Published in: Annals of Surgical Oncology 4/2012

01-04-2012 | Hepatobiliary Tumors

Relationship Between Diffusion-Weighted Magnetic Resonance Imaging and Histological Tumor Grading of Hepatocellular Carcinoma

Authors: Mitsuru Nakanishi, MD, PhD, Makoto Chuma, MD, PhD, Shuhei Hige, MD, PhD, Tokuhiko Omatsu, MD, PhD, Hideki Yokoo, MD, PhD, Kazuaki Nakanishi, MD, PhD, Toshiya Kamiyama, MD, PhD, Kanako Kubota, MD, PhD, Hironori Haga, MD, PhD, Yoshihiro Matsuno, MD, PhD, Yuya Onodera, MD, PhD, Mototsugu Kato, MD, PhD, Masahiro Asaka, MD, PhD

Published in: Annals of Surgical Oncology | Issue 4/2012

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Abstract

Background

Intrahepatic and extrahepatic recurrence remains a significant problem for hepatocellular carcinoma (HCC). The aim of this study was to determine the usefulness of diffusion-weighted magnetic resonance imaging (DWI) for histological tumor grading and preoperative prediction of early HCC recurrence within 6 months of operation.

Methods

A total of 44 patients who had undergone hepatic resection for HCC (50 nodules) were reviewed retrospectively. DWI was performed within 30 days before hepatectomy, and apparent diffusion coefficients (ADCs) were measured using 2 methods: mean ADC and minimum-spot ADC. Relationships between ADCs and histological differentiation and between ADCs and early recurrence of HCC were analyzed.

Results

Mean ADC was significantly lower in poorly differentiated HCC (n = 18, 1.07 ± 0.15 × 10−3 mm2/s) than in moderately differentiated HCC (n = 29, 1.29 ± 0.21 × 10−3 mm2/s; P < .05). Minimum-spot ADC was significantly lower in poorly differentiated HCC (n = 18, 0.69 ± 0.19 × 10−3 mm2/s) than in well-differentiated HCC (n = 3, 1.15 ± 0.10 × 10−3 mm2; P < .01) or in moderately differentiated HCC (n = 29, 0.98 ± 0.18 × 10−3 mm2/s; P < .0001). Of 34 patients who were able to be observed for >6 months after resection, 9 showed early recurrence. Minimum-spot ADC was significantly lower in patients with early recurrence (n = 9, 0.64 ± 0.24 × 10−3 mm2/s) than in patients without early recurrence (n = 25, 0.88 ± 0.19 × 10−3 mm2/s; P < .05). On multivariate analysis, minimum-spot ADC was a significant risk factor for early recurrence (P < .05).

Conclusion

Quantitative measurement of ADC of HCC with magnetic resonance diffusion weighted imaging is a promising functional imaging tool in the prediction of histological grade and early recurrence before treatment.
Literature
1.
go back to reference Kiyosawa K, Uemura T, Ichijo T, Matsumoto A, Yoshizawa K, Gad A, et al. Hepatocellular carcinoma: recent trends in Japan. Gastroenterology. 2004;127:S17–S26.PubMedCrossRef Kiyosawa K, Uemura T, Ichijo T, Matsumoto A, Yoshizawa K, Gad A, et al. Hepatocellular carcinoma: recent trends in Japan. Gastroenterology. 2004;127:S17–S26.PubMedCrossRef
2.
go back to reference Park JH, Koh KC, Choi MS, Lee JH, Yoo BC, Paik SW, et al. Analysis of risk factors associated with early multinodular recurrences after hepatic resection for hepatocellular carcinoma. Am J Surg. 2006;192:29–33.PubMedCrossRef Park JH, Koh KC, Choi MS, Lee JH, Yoo BC, Paik SW, et al. Analysis of risk factors associated with early multinodular recurrences after hepatic resection for hepatocellular carcinoma. Am J Surg. 2006;192:29–33.PubMedCrossRef
3.
go back to reference Portolani N, Coniglio A, Ghidoni S, Giovanelli M, Benetti A, Tiberio GA, et al. Early and late recurrence after liver resection for hepatocellular carcinoma. Ann Surg. 2006;243:229–35.PubMedCrossRef Portolani N, Coniglio A, Ghidoni S, Giovanelli M, Benetti A, Tiberio GA, et al. Early and late recurrence after liver resection for hepatocellular carcinoma. Ann Surg. 2006;243:229–35.PubMedCrossRef
4.
go back to reference Llovet JM, Fuster J, Bruix J. Intention-to-treat analysis of surgical treatment for early hepatocellular carcinoma: resection versus transplantation. Hepatology. 1999;30:1434–40.PubMedCrossRef Llovet JM, Fuster J, Bruix J. Intention-to-treat analysis of surgical treatment for early hepatocellular carcinoma: resection versus transplantation. Hepatology. 1999;30:1434–40.PubMedCrossRef
5.
go back to reference Roayaie S, Blume IN, Thung SN, Guido M, Fiel MI, Hiotis S, et al. A system of microvascular invasion to predict outcome after resection in patients with hepatocellular carcinoma. Gastroenterology. 2009;137:786–8.CrossRef Roayaie S, Blume IN, Thung SN, Guido M, Fiel MI, Hiotis S, et al. A system of microvascular invasion to predict outcome after resection in patients with hepatocellular carcinoma. Gastroenterology. 2009;137:786–8.CrossRef
6.
go back to reference Imamura H, Matsuyama Y, Tanaka E, Ohkubo T, Hasegawa K, Miyagawa S, et al. Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol. 2003;38:200–7.PubMedCrossRef Imamura H, Matsuyama Y, Tanaka E, Ohkubo T, Hasegawa K, Miyagawa S, et al. Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol. 2003;38:200–7.PubMedCrossRef
7.
go back to reference Regimbeau JM, Abdalla EK, Vauyhey JN, Lauwers GY, Durand F, Nagorney DM, et al. Risk factors for early death due to recurrence after liver resection for hepatocellular carcinoma: result of a multicenter study. J Surg Oncol. 2004;85:36–41.PubMedCrossRef Regimbeau JM, Abdalla EK, Vauyhey JN, Lauwers GY, Durand F, Nagorney DM, et al. Risk factors for early death due to recurrence after liver resection for hepatocellular carcinoma: result of a multicenter study. J Surg Oncol. 2004;85:36–41.PubMedCrossRef
8.
go back to reference Capussotti L, Muratore A, Amisano M, Polastri R, Bouzari H, Massucco P. Liver resection for hepatocellular carcinoma on cirrhosis: analysis of mortality, mobility and survival – a European single center experience. Eur J Surg Oncol. 2005;31:986–93.PubMedCrossRef Capussotti L, Muratore A, Amisano M, Polastri R, Bouzari H, Massucco P. Liver resection for hepatocellular carcinoma on cirrhosis: analysis of mortality, mobility and survival – a European single center experience. Eur J Surg Oncol. 2005;31:986–93.PubMedCrossRef
9.
go back to reference Ng KK, Vauthey JN, Pawlik TM, Lauwers GY, Regimbeau JM, Belghiti J, et al. Is hepatic resection for large or multinodular hepatocellular carcinoma justified? Results from multi-institutional data base. Ann Surg Oncol. 2005:12;364–73.PubMedCrossRef Ng KK, Vauthey JN, Pawlik TM, Lauwers GY, Regimbeau JM, Belghiti J, et al. Is hepatic resection for large or multinodular hepatocellular carcinoma justified? Results from multi-institutional data base. Ann Surg Oncol. 2005:12;364–73.PubMedCrossRef
10.
go back to reference Peng SY, Chen WJ, Lai PL, Jeng YM, Sheu JC, Hsu HC. High alpha-fetoprotein level correlates with high stage, early recurrence and poor prognosis of hepatocellular carcinoma: significance of hepatitis virus infection, age, p53 and beta-catenin mutations. Int J Cancer. 2004;112:44–50.PubMedCrossRef Peng SY, Chen WJ, Lai PL, Jeng YM, Sheu JC, Hsu HC. High alpha-fetoprotein level correlates with high stage, early recurrence and poor prognosis of hepatocellular carcinoma: significance of hepatitis virus infection, age, p53 and beta-catenin mutations. Int J Cancer. 2004;112:44–50.PubMedCrossRef
11.
go back to reference Stevens WR, Johnson CD, Stephens DH, Batts KP. CT findings in hepatocellular carcinoma: correlation of tumor characteristics with causative factors, tumor size, and histologic tumor grade. Radiology. 1994;191:531–7.PubMed Stevens WR, Johnson CD, Stephens DH, Batts KP. CT findings in hepatocellular carcinoma: correlation of tumor characteristics with causative factors, tumor size, and histologic tumor grade. Radiology. 1994;191:531–7.PubMed
12.
go back to reference Hayashi M, Matsui O, Ueda K, Kawamori Y, Kadoya M, Yoshikawa J, et al. Correlation between the blood supply and grade of malignancy of hepatocellular nodules associated with liver cirrhosis: evaluation by CT during intraarterial injection of contrast medium. Am J Roentgenol. 1999;172:969–76. Hayashi M, Matsui O, Ueda K, Kawamori Y, Kadoya M, Yoshikawa J, et al. Correlation between the blood supply and grade of malignancy of hepatocellular nodules associated with liver cirrhosis: evaluation by CT during intraarterial injection of contrast medium. Am J Roentgenol. 1999;172:969–76.
13.
go back to reference Jang HG, Kim TK, Burns PN, Wilson SR. Enhancement patterns of hepatocellular carcinoma at contrast-enhanced US: comparison with histologic differentiation. Radiology. 2007;244:898–906.PubMedCrossRef Jang HG, Kim TK, Burns PN, Wilson SR. Enhancement patterns of hepatocellular carcinoma at contrast-enhanced US: comparison with histologic differentiation. Radiology. 2007;244:898–906.PubMedCrossRef
14.
go back to reference Bulakbasi IM, Kocaoglu M, Ors F, Tayfun C, Uçöz T. Combination of single-voxel proton MR spectroscopy and apparent diffusion coefficient calculation in evaluation of common brain tumors. Am J Neuroradiol. 2003;24:225–33.PubMed Bulakbasi IM, Kocaoglu M, Ors F, Tayfun C, Uçöz T. Combination of single-voxel proton MR spectroscopy and apparent diffusion coefficient calculation in evaluation of common brain tumors. Am J Neuroradiol. 2003;24:225–33.PubMed
15.
go back to reference Higano S, Yun X, Kumabe T, Watanabe M, Mugikura S, Umetsu A, et al. Malignant astrocytic tumors: clinical importance of apparent diffusion coefficient in prediction of grade and prognosis. Radiology. 2006;241:839–46.PubMedCrossRef Higano S, Yun X, Kumabe T, Watanabe M, Mugikura S, Umetsu A, et al. Malignant astrocytic tumors: clinical importance of apparent diffusion coefficient in prediction of grade and prognosis. Radiology. 2006;241:839–46.PubMedCrossRef
16.
go back to reference Dow-Mu K, David JC. Diffusion-weighted MRI in the body: Applications and challenges in oncology. Am J Roentgenol. 2007;188:1622–35.CrossRef Dow-Mu K, David JC. Diffusion-weighted MRI in the body: Applications and challenges in oncology. Am J Roentgenol. 2007;188:1622–35.CrossRef
17.
go back to reference Colagrande S, Carbone SF, Carusi LM, Cova M, Villari N. Magnetic resonance diffusion-weighted imaging: extraneurological applications. Radiol Med. 2006;111:392–419.PubMedCrossRef Colagrande S, Carbone SF, Carusi LM, Cova M, Villari N. Magnetic resonance diffusion-weighted imaging: extraneurological applications. Radiol Med. 2006;111:392–419.PubMedCrossRef
18.
go back to reference Chen YC, Li CW, Kuo YT, Jaw TS, Wu DK, Jao JC, et al. Early response of hepatocellular carcinoma to transcatheter arterial chemoembolization: choline levels and MR diffusion constants—initial experience. Radiology. 2006;239:448–456.PubMedCrossRef Chen YC, Li CW, Kuo YT, Jaw TS, Wu DK, Jao JC, et al. Early response of hepatocellular carcinoma to transcatheter arterial chemoembolization: choline levels and MR diffusion constants—initial experience. Radiology. 2006;239:448–456.PubMedCrossRef
19.
go back to reference Nishie A, Tajima T, Asayama Y, Ishigami K, Kakihara D, Nakayama T, et al. Diagnostic performance of apparent coefficient for predicting histological grade of hepatocellular carcinoma. Eur J Radiol. doi:10.1016/j.ejrad.201.06.019 [Epub ahead of print]. Nishie A, Tajima T, Asayama Y, Ishigami K, Kakihara D, Nakayama T, et al. Diagnostic performance of apparent coefficient for predicting histological grade of hepatocellular carcinoma. Eur J Radiol. doi:10.​1016/​j.​ejrad.​201.​06.​019 [Epub ahead of print].
20.
go back to reference Heo SH, Jeong YY, Shin SS, Kim JW, Lim HS, Lee JH, et al. Apparent diffusion coefficient value of diffusion-weighted imaging for hepatocellular carcinoma: correlation with histologic differentiation and the expression of vascular endothelial growth factor. Korean J Radiol. 2010;11:295–303.PubMedCrossRef Heo SH, Jeong YY, Shin SS, Kim JW, Lim HS, Lee JH, et al. Apparent diffusion coefficient value of diffusion-weighted imaging for hepatocellular carcinoma: correlation with histologic differentiation and the expression of vascular endothelial growth factor. Korean J Radiol. 2010;11:295–303.PubMedCrossRef
21.
go back to reference Nasu K, Kuroki Y, Tsukamoto T, Nakajima H, Mori K, Minami M, et al. Diffusion-weighted imaging of surgically resected hepatocellular carcinoma: imaging characteristics and relationship among signal intensity, apparent diffusion coefficient, and histopathologic grade. Am J Roentgenol. 2009;193:438–44.CrossRef Nasu K, Kuroki Y, Tsukamoto T, Nakajima H, Mori K, Minami M, et al. Diffusion-weighted imaging of surgically resected hepatocellular carcinoma: imaging characteristics and relationship among signal intensity, apparent diffusion coefficient, and histopathologic grade. Am J Roentgenol. 2009;193:438–44.CrossRef
22.
23.
go back to reference International Working Party. Terminology of nodular hepatocellular lesions. Hepatology. 1995 22:983–93. International Working Party. Terminology of nodular hepatocellular lesions. Hepatology. 1995 22:983–93.
24.
go back to reference Guo Y, Cai YQ, Cai ZL, Gao YG, An NY, Ma L, et al. Differentiation of clinically benign and malignant breast lesions using diffusion-weighted imaging. J Magn Reson Imaging. 2002;16:172–8.PubMedCrossRef Guo Y, Cai YQ, Cai ZL, Gao YG, An NY, Ma L, et al. Differentiation of clinically benign and malignant breast lesions using diffusion-weighted imaging. J Magn Reson Imaging. 2002;16:172–8.PubMedCrossRef
25.
go back to reference Guo AC, Cummings TJ, Dash RC, Provenzale JM. Lymphomas and high-grade astrocytomas: comparison of water diffusibility and histologic characteristics. Radiology. 2002;224:177–83.PubMedCrossRef Guo AC, Cummings TJ, Dash RC, Provenzale JM. Lymphomas and high-grade astrocytomas: comparison of water diffusibility and histologic characteristics. Radiology. 2002;224:177–83.PubMedCrossRef
26.
go back to reference Calvar JA, Meli FJ, Romero C, Calcagno ML, Yanez P, Martinez AR, et al. Characterization of brain tumors by MRS, DWI and Ki-67 labeling index. J Neurooncol. 2005;72:273–80.PubMedCrossRef Calvar JA, Meli FJ, Romero C, Calcagno ML, Yanez P, Martinez AR, et al. Characterization of brain tumors by MRS, DWI and Ki-67 labeling index. J Neurooncol. 2005;72:273–80.PubMedCrossRef
27.
go back to reference Taouli B, Vilgrain V, Dumont E, Daire JL, Fan B, Menu Y. Evaluation of liver diffusion isotropy and characterization of focal hepatic lesions with two single-shot echo-planar MR imaging sequences. Radiology. 2003;226:71–8.PubMedCrossRef Taouli B, Vilgrain V, Dumont E, Daire JL, Fan B, Menu Y. Evaluation of liver diffusion isotropy and characterization of focal hepatic lesions with two single-shot echo-planar MR imaging sequences. Radiology. 2003;226:71–8.PubMedCrossRef
28.
go back to reference Lewin M, Poujol-Robert A, Boelle PY, Wendum D, Lasnier E, Viallon M, et al. Diffusion-weighted magnetic resonance imaging for the assessment of fibrosis in chronic hepatitis C. Hepatology. 2007;46:658–65.PubMedCrossRef Lewin M, Poujol-Robert A, Boelle PY, Wendum D, Lasnier E, Viallon M, et al. Diffusion-weighted magnetic resonance imaging for the assessment of fibrosis in chronic hepatitis C. Hepatology. 2007;46:658–65.PubMedCrossRef
29.
go back to reference Kamel IR, Bluemke DA, Ramsey D, Abusedera M, Torbenson M, Eng J, et al. Role of diffusion-weighted imaging in estimating tumor necrosis after chemoembolization of hepatocellular carcinoma. Am J Roentgenol. 2003;181:708–10. Kamel IR, Bluemke DA, Ramsey D, Abusedera M, Torbenson M, Eng J, et al. Role of diffusion-weighted imaging in estimating tumor necrosis after chemoembolization of hepatocellular carcinoma. Am J Roentgenol. 2003;181:708–10.
30.
go back to reference Park JH, Koh KC, Choi MS, Lee JH, Yoo BC, Paik SW, et al. Analysis of risk factors associated with early multinodular recurrences after hepatic resection for hepatocellular carcinoma. Am J Surg. 2006;192:29–33.PubMedCrossRef Park JH, Koh KC, Choi MS, Lee JH, Yoo BC, Paik SW, et al. Analysis of risk factors associated with early multinodular recurrences after hepatic resection for hepatocellular carcinoma. Am J Surg. 2006;192:29–33.PubMedCrossRef
Metadata
Title
Relationship Between Diffusion-Weighted Magnetic Resonance Imaging and Histological Tumor Grading of Hepatocellular Carcinoma
Authors
Mitsuru Nakanishi, MD, PhD
Makoto Chuma, MD, PhD
Shuhei Hige, MD, PhD
Tokuhiko Omatsu, MD, PhD
Hideki Yokoo, MD, PhD
Kazuaki Nakanishi, MD, PhD
Toshiya Kamiyama, MD, PhD
Kanako Kubota, MD, PhD
Hironori Haga, MD, PhD
Yoshihiro Matsuno, MD, PhD
Yuya Onodera, MD, PhD
Mototsugu Kato, MD, PhD
Masahiro Asaka, MD, PhD
Publication date
01-04-2012
Publisher
Springer-Verlag
Published in
Annals of Surgical Oncology / Issue 4/2012
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-011-2066-8

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