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Published in: Hepatology International 2/2016

01-03-2016 | Original Article

The arterial tumor enhancement pattern on contrast-enhanced computed tomography is associated with primary cancer death after radiofrequency ablation for small hepatocellular carcinoma

Authors: Ryo Shimizu, Hideyuki Tamai, Yoshiyuki Mori, Naoki Shingaki, Shuya Maeshima, Junya Nuta, Yoshimasa Maeda, Kosaku Moribata, Yosuke Muraki, Hisanobu Deguchi, Izumi Inoue, Takao Maekita, Mikitaka Iguchi, Jun Kato, Masao Ichinose

Published in: Hepatology International | Issue 2/2016

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Abstract

Background/Purpose

Critical recurrences after radiofrequency ablation for hepatocellular carcinoma (HCC), such as intrahepatic metastases or dissemination, and extrahepatic metastases or seeding, which are difficult to treat radically, almost certainly lead to primary cancer death. The present study aimed to clarify whether the arterial tumor enhancement pattern on contrast-enhanced computed tomography (CECT) is associated with critical recurrence and cancer death after RFA for small HCC.

Methods

Between April 2001 and September 2011, 226 patients with initial small hypervascular HCC (≤3 cm in diameter and ≤3 tumors) were treated by RFA. Arterial tumor enhancement patterns on CECT before RFA were categorized by whether non-enhanced areas were included inside the tumor stain.

Results

The heterogeneous enhancement group included 44 patients, and the homogeneous enhancement group included 182 patients. The cumulative 5-year critical recurrence rates of the heterogeneous and homogeneous enhancement groups were 42 and 22 % (p = 0.005), respectively. Univariate analysis for factors related to critical recurrence showed significant differences in sex, arterial enhancement pattern, and response to antiviral therapy. These factors were independent on multivariate analysis. The cumulative 5-year primary cancer death rates of the heterogeneous and homogeneous enhancement groups were 29 and 13 % (p = 0.002), respectively. Univariate analysis for factors related to primary cancer death showed significant differences in arterial enhancement pattern and response to antiviral therapy. These factors were independent on multivariate analysis.

Conclusions

Arterial heterogeneous tumor enhancement on CECT is associated with critical recurrence and cancer death after RFA for small HCC.
Literature
1.
go back to reference Arii S, Teramoto K, Kawamura T, Okamoto H, Kaido T, Mori A, Imamura M. Characteristics of recurrent hepatocellular carcinoma in Japan and our surgical experience. J Hepatobiliary Pancreat Surg. 2001;8:397–403CrossRefPubMed Arii S, Teramoto K, Kawamura T, Okamoto H, Kaido T, Mori A, Imamura M. Characteristics of recurrent hepatocellular carcinoma in Japan and our surgical experience. J Hepatobiliary Pancreat Surg. 2001;8:397–403CrossRefPubMed
2.
go back to reference Clinical Practice Guidelines for Hepatocellular Carcinoma. The Japan Society of Hepatology 2009 update. Hepatol Res. 2010;40(Suppl 1):2–144 Clinical Practice Guidelines for Hepatocellular Carcinoma. The Japan Society of Hepatology 2009 update. Hepatol Res. 2010;40(Suppl 1):2–144
3.
go back to reference EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 2012;56:908–943 EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 2012;56:908–943
4.
go back to reference Takada Y, Kurata M, Ohkohchi N. Rapid and aggressive recurrence accompanied by portal tumor thrombus after radiofrequency ablation for hepatocellular carcinoma. Int J Clin Oncol. 2003;8:332–335CrossRefPubMed Takada Y, Kurata M, Ohkohchi N. Rapid and aggressive recurrence accompanied by portal tumor thrombus after radiofrequency ablation for hepatocellular carcinoma. Int J Clin Oncol. 2003;8:332–335CrossRefPubMed
5.
go back to reference Ruzzenente A, Manzoni GD, Molfetta M, Pachera S, Genco B, Donataccio M, Guglielmi A. Rapid progression of hepatocellular carcinoma after radiofrequency ablation. World J Gastroenterol. 2004;10:1137–1140PubMedPubMedCentral Ruzzenente A, Manzoni GD, Molfetta M, Pachera S, Genco B, Donataccio M, Guglielmi A. Rapid progression of hepatocellular carcinoma after radiofrequency ablation. World J Gastroenterol. 2004;10:1137–1140PubMedPubMedCentral
6.
go back to reference Nicoli N, Casaril A, Abu Hilal M, Mangiante G, Marchiori L, Ciola M, Invernizzi L, Campagnaro T, Mansueto G. A case of rapid intrahepatic dissemination of hepatocellular carcinoma after radiofrequency thermal ablation. Am J Surg. 2004;188:165–167CrossRefPubMed Nicoli N, Casaril A, Abu Hilal M, Mangiante G, Marchiori L, Ciola M, Invernizzi L, Campagnaro T, Mansueto G. A case of rapid intrahepatic dissemination of hepatocellular carcinoma after radiofrequency thermal ablation. Am J Surg. 2004;188:165–167CrossRefPubMed
7.
go back to reference Masuda T, Beppu T, Ishiko T, Horino K, Baba Y, Mizumoto T, Hayashi H, Okabe H, Horlad H, Doi K, Okabe K, Takamori H, Hirota M, Iyama K, Baba H. Intrahepatic dissemination of hepatocellular carcinoma after local ablation therapy. J Hepatobiliary Pancreat Surg. 2008;15:589–595CrossRefPubMed Masuda T, Beppu T, Ishiko T, Horino K, Baba Y, Mizumoto T, Hayashi H, Okabe H, Horlad H, Doi K, Okabe K, Takamori H, Hirota M, Iyama K, Baba H. Intrahepatic dissemination of hepatocellular carcinoma after local ablation therapy. J Hepatobiliary Pancreat Surg. 2008;15:589–595CrossRefPubMed
8.
go back to reference Mori Y, Tamai H, Shingaki N, Moribata K, Shiraki T, Deguchi H, Ueda K, Enomoto S, Magari H, Inoue I, Maekita T, Iguchi M, Yanaoka K, Oka M, Ichinose M. Diffuse intrahepatic recurrence after percutaneous radiofrequency ablation for solitary and small hepatocellular carcinoma. Hepatol Int. 2009;3:509–515CrossRefPubMedPubMedCentral Mori Y, Tamai H, Shingaki N, Moribata K, Shiraki T, Deguchi H, Ueda K, Enomoto S, Magari H, Inoue I, Maekita T, Iguchi M, Yanaoka K, Oka M, Ichinose M. Diffuse intrahepatic recurrence after percutaneous radiofrequency ablation for solitary and small hepatocellular carcinoma. Hepatol Int. 2009;3:509–515CrossRefPubMedPubMedCentral
9.
go back to reference Imamura J, Tateishi R, Shiina S, Goto E, Sato T, Ohki T, Masuzaki R, Goto T, Yoshida H, Kanai F, Hamamura K, Obi S, Yoshida H, Omata M. Neoplastic seeding after radiofrequency ablation for hepatocellular carcinoma. Am J Gastroenterol. 2008;103:3057–3062CrossRefPubMed Imamura J, Tateishi R, Shiina S, Goto E, Sato T, Ohki T, Masuzaki R, Goto T, Yoshida H, Kanai F, Hamamura K, Obi S, Yoshida H, Omata M. Neoplastic seeding after radiofrequency ablation for hepatocellular carcinoma. Am J Gastroenterol. 2008;103:3057–3062CrossRefPubMed
10.
go back to reference Shirai K, Tamai H, Shingaki N, Mori Y, Moribata K, Enomoto S, Deguchi H, Ueda K, Maekita T, Inoue I, Iguchi M, Yanaoka K, Oka M, Ichinose M. Clinical features and risk factors of extrahepatic seeding after percutaneous radiofrequency ablation for hepatocellular carcinoma. Hepatol Res. 2011;41:738–745CrossRefPubMed Shirai K, Tamai H, Shingaki N, Mori Y, Moribata K, Enomoto S, Deguchi H, Ueda K, Maekita T, Inoue I, Iguchi M, Yanaoka K, Oka M, Ichinose M. Clinical features and risk factors of extrahepatic seeding after percutaneous radiofrequency ablation for hepatocellular carcinoma. Hepatol Res. 2011;41:738–745CrossRefPubMed
11.
go back to reference Yang Y, Nagano H, Ota H, Morimoto O, Nakamura M, Wada H, Noda T, Damdinsuren B, Marubashi S, Miyamoto A, Takeda Y, Dono K, Umeshita K, Nakamori S, Wakasa K, Sakon M, Monden M. Patterns and clinicopathologic features of extrahepatic recurrence of hepatocellular carcinoma after curative resection. Surgery. 2007;141:196–202CrossRefPubMed Yang Y, Nagano H, Ota H, Morimoto O, Nakamura M, Wada H, Noda T, Damdinsuren B, Marubashi S, Miyamoto A, Takeda Y, Dono K, Umeshita K, Nakamori S, Wakasa K, Sakon M, Monden M. Patterns and clinicopathologic features of extrahepatic recurrence of hepatocellular carcinoma after curative resection. Surgery. 2007;141:196–202CrossRefPubMed
12.
go back to reference Kawano Y, Sasaki A, Kai S, Endo Y, Iwaki K, Uchida H, Shibata K, Ohta M, Kitano S. Prognosis of patients with intrahepatic recurrence after hepatic resection for hepatocellular carcinoma: a retrospective study. Eur J Surg Oncol. 2009;35:174–179CrossRefPubMed Kawano Y, Sasaki A, Kai S, Endo Y, Iwaki K, Uchida H, Shibata K, Ohta M, Kitano S. Prognosis of patients with intrahepatic recurrence after hepatic resection for hepatocellular carcinoma: a retrospective study. Eur J Surg Oncol. 2009;35:174–179CrossRefPubMed
13.
go back to reference Esnaola NF, Lauwers GY, Mirza NQ, Nagorney DM, Doherty D, Ikai I, Yamaoka Y, Regimbeau JM, Belghiti J, Curley SA, Ellis LM, Vauthey JN. Predictors of microvascular invasion in patients with hepatocellular carcinoma who are candidates for orthotopic liver transplantation. J Gastrointest Surg. 2006;6:224–232 (discussion 232) CrossRef Esnaola NF, Lauwers GY, Mirza NQ, Nagorney DM, Doherty D, Ikai I, Yamaoka Y, Regimbeau JM, Belghiti J, Curley SA, Ellis LM, Vauthey JN. Predictors of microvascular invasion in patients with hepatocellular carcinoma who are candidates for orthotopic liver transplantation. J Gastrointest Surg. 2006;6:224–232 (discussion 232) CrossRef
14.
go back to reference Silva MA, Hegab B, Hyde C, Guo B, Buckels JA, Mirza DF. Needle track seeding following biopsy of liver lesions in the diagnosis of hepatocellular cancer: a systematic review and meta-analysis. Gut. 2008;57:1592–1596CrossRefPubMed Silva MA, Hegab B, Hyde C, Guo B, Buckels JA, Mirza DF. Needle track seeding following biopsy of liver lesions in the diagnosis of hepatocellular cancer: a systematic review and meta-analysis. Gut. 2008;57:1592–1596CrossRefPubMed
15.
go back to reference Asayama Y, Yoshimitsu K, Nishihara Y, Irie H, Aishima S, Taketomi A, Honda H. Arterial blood supply of hepatocellular carcinoma and histologic grading: radiologic-pathologic correlation. Am J Roentgenol. 2008;190:W28–W34CrossRef Asayama Y, Yoshimitsu K, Nishihara Y, Irie H, Aishima S, Taketomi A, Honda H. Arterial blood supply of hepatocellular carcinoma and histologic grading: radiologic-pathologic correlation. Am J Roentgenol. 2008;190:W28–W34CrossRef
16.
go back to reference Nakachi K, Tamai H, Mori Y, Shingaki N, Moribata K, Deguchi H, Ueda K, Inoue I, Maekita T, Iguchi M, Kato J, Ichinose M. Prediction of poorly differentiated hepatocellular carcinoma using contrast computed tomography. Cancer Imaging. 2014;14:17PubMedPubMedCentral Nakachi K, Tamai H, Mori Y, Shingaki N, Moribata K, Deguchi H, Ueda K, Inoue I, Maekita T, Iguchi M, Kato J, Ichinose M. Prediction of poorly differentiated hepatocellular carcinoma using contrast computed tomography. Cancer Imaging. 2014;14:17PubMedPubMedCentral
17.
go back to reference Bedossa P, Poynard T. An algorithm for the grading of activity in chronic hepatitis C. The METAVIR Cooperative Study Group. Hepatology. 1996;24:289–293CrossRefPubMed Bedossa P, Poynard T. An algorithm for the grading of activity in chronic hepatitis C. The METAVIR Cooperative Study Group. Hepatology. 1996;24:289–293CrossRefPubMed
18.
go back to reference Sanada Y, Yoshida K, Itoh H. Comparison of CT enhancement patterns and histologic features in hepatocellular carcinoma up to 2 cm: assessment of malignant potential with claudin-10 immunohistochemistry. Oncol Rep. 2007;17:1177–1182PubMed Sanada Y, Yoshida K, Itoh H. Comparison of CT enhancement patterns and histologic features in hepatocellular carcinoma up to 2 cm: assessment of malignant potential with claudin-10 immunohistochemistry. Oncol Rep. 2007;17:1177–1182PubMed
19.
go back to reference Kawamura Y, Ikeda K, Hirakawa M, Yatsuji H, Sezaki H, Hosaka T, Akuta N, Kobayashi M, Saitoh S, Suzuki F, Suzuki Y, Arase Y, Kumada H. New classification of dynamic computed tomography images predictive of malignant characteristics of hepatocellular carcinoma. Hepatol Res. 2010;40:1006–1014CrossRefPubMed Kawamura Y, Ikeda K, Hirakawa M, Yatsuji H, Sezaki H, Hosaka T, Akuta N, Kobayashi M, Saitoh S, Suzuki F, Suzuki Y, Arase Y, Kumada H. New classification of dynamic computed tomography images predictive of malignant characteristics of hepatocellular carcinoma. Hepatol Res. 2010;40:1006–1014CrossRefPubMed
20.
go back to reference Kawamura Y, Ikeda K, Seko Y, Hosaka T, Kobayashi M, Saitoh S, Kumada H. Heterogeneous type 4 enhancement of hepatocellular carcinoma on dynamic CT is associated with tumor recurrence after radiofrequency ablation. Am J Roentgenol. 2011;197:W665–W673CrossRef Kawamura Y, Ikeda K, Seko Y, Hosaka T, Kobayashi M, Saitoh S, Kumada H. Heterogeneous type 4 enhancement of hepatocellular carcinoma on dynamic CT is associated with tumor recurrence after radiofrequency ablation. Am J Roentgenol. 2011;197:W665–W673CrossRef
21.
go back to reference Nishie A, Yoshimitsu K, Okamoto D, Tajima T, Asayama Y, Ishigami K, Kakihara D, Nakayama T, Takayama Y, Shirabe K, Fujita N, Honda H. CT prediction of histological grade of hypervascular hepatocellular carcinoma: utility of the portal phase. Jpn J Radiol. 2013;31:89–98CrossRefPubMed Nishie A, Yoshimitsu K, Okamoto D, Tajima T, Asayama Y, Ishigami K, Kakihara D, Nakayama T, Takayama Y, Shirabe K, Fujita N, Honda H. CT prediction of histological grade of hypervascular hepatocellular carcinoma: utility of the portal phase. Jpn J Radiol. 2013;31:89–98CrossRefPubMed
22.
go back to reference Shiina S, Tateishi R, Arano T, Uchino K, Enooku K, Nakagawa H, Asaoka Y, Sato T, Masuzaki R, Kondo Y, Goto T, Yoshida H, Omata M, Koike K. Radiofrequency ablation for hepatocellular carcinoma: 10-year outcome and prognostic factors. Am J Gastroenterol. 2012;107:569–577 (quiz 578) CrossRefPubMedPubMedCentral Shiina S, Tateishi R, Arano T, Uchino K, Enooku K, Nakagawa H, Asaoka Y, Sato T, Masuzaki R, Kondo Y, Goto T, Yoshida H, Omata M, Koike K. Radiofrequency ablation for hepatocellular carcinoma: 10-year outcome and prognostic factors. Am J Gastroenterol. 2012;107:569–577 (quiz 578) CrossRefPubMedPubMedCentral
23.
go back to reference Okuda H, Nakanishi T, Takatsu K, Saito A, Hayashi N, Takasaki K, Takenami K, Yamamoto M, Nakano M. Serum levels of des-gamma-carboxy prothrombin measured using the revised enzyme immunoassay kit with increased sensitivity in relation to clinicopathologic features of solitary hepatocellular carcinoma. Cancer. 2000;88:544–549CrossRefPubMed Okuda H, Nakanishi T, Takatsu K, Saito A, Hayashi N, Takasaki K, Takenami K, Yamamoto M, Nakano M. Serum levels of des-gamma-carboxy prothrombin measured using the revised enzyme immunoassay kit with increased sensitivity in relation to clinicopathologic features of solitary hepatocellular carcinoma. Cancer. 2000;88:544–549CrossRefPubMed
24.
go back to reference Sun P, Yang X, He RQ, Hu QG, Song ZF, Xiong J, Zheng QC. Antiviral therapy after curative treatment of hepatitis B/C virus-related hepatocellular carcinoma: a systematic review of randomized trials. Hepatol Res. 2014;44:259–269CrossRefPubMed Sun P, Yang X, He RQ, Hu QG, Song ZF, Xiong J, Zheng QC. Antiviral therapy after curative treatment of hepatitis B/C virus-related hepatocellular carcinoma: a systematic review of randomized trials. Hepatol Res. 2014;44:259–269CrossRefPubMed
25.
go back to reference Sun P, Dong X, Cheng X, Hu Q, Zheng Q. Nucleot(s)ide analogues for hepatitis B virus-related hepatocellular carcinoma after curative treatment: a systematic review and meta-analysis. PLoS ONE. 2014;9:e102761CrossRefPubMedPubMedCentral Sun P, Dong X, Cheng X, Hu Q, Zheng Q. Nucleot(s)ide analogues for hepatitis B virus-related hepatocellular carcinoma after curative treatment: a systematic review and meta-analysis. PLoS ONE. 2014;9:e102761CrossRefPubMedPubMedCentral
26.
go back to reference Mazzaferro V, Romito R, Schiavo M, Mariani L, Camerini T, Bhoori S, Capussotti L, Calise F, Pellicci R, Belli G, Tagger A, Colombo M, Bonino F, Majno P, Llovet JM. Force HCCIT. Prevention of hepatocellular carcinoma recurrence with alpha-interferon after liver resection in HCV cirrhosis. Hepatology. 2006;44:1543–1554CrossRefPubMed Mazzaferro V, Romito R, Schiavo M, Mariani L, Camerini T, Bhoori S, Capussotti L, Calise F, Pellicci R, Belli G, Tagger A, Colombo M, Bonino F, Majno P, Llovet JM. Force HCCIT. Prevention of hepatocellular carcinoma recurrence with alpha-interferon after liver resection in HCV cirrhosis. Hepatology. 2006;44:1543–1554CrossRefPubMed
27.
go back to reference Farinati F, Sergio A, Giacomin A, Di Nolfo MA, Del Poggio P, Benvegnu L, Rapaccini G, Zoli M, Borzio F, Giannini EG, Caturelli E, Trevisani F. Italian Liver Cancer g. Is female sex a significant favorable prognostic factor in hepatocellular carcinoma? Eur J Gastroenterol Hepatol. 2009;21:1212–1218CrossRefPubMed Farinati F, Sergio A, Giacomin A, Di Nolfo MA, Del Poggio P, Benvegnu L, Rapaccini G, Zoli M, Borzio F, Giannini EG, Caturelli E, Trevisani F. Italian Liver Cancer g. Is female sex a significant favorable prognostic factor in hepatocellular carcinoma? Eur J Gastroenterol Hepatol. 2009;21:1212–1218CrossRefPubMed
28.
go back to reference Ahmed M, Solbiati L, Brace CL, Breen DJ, Callstrom MR, Charboneau JW, Chen MH, Choi BI, de Baere T, Dodd GD 3rd, Dupuy DE, Gervais DA, Gianfelice D, Gillams AR, Lee FT Jr, Leen E, Lencioni R, Littrup PJ, Livraghi T, Lu DS, McGahan JP, Meloni MF, Nikolic B, Pereira PL, Liang P, Rhim H, Rose SC, Salem R, Sofocleous CT, Solomon SB, Soulen MC, Tanaka M, Vogl TJ, Wood BJ, Goldberg SN. International Working Group on image-guided tumor ablation, Interventional Oncology Sans Frontieres Expert Panel, Technology Assessment Committee of the Society of Interventional Radiology, Standard of Practice Committee of the Cardiovascular and Interventional Radiological Society of Europe. Image-guided tumor ablation: standardization of terminology and reporting criteria—a 10-year update. Radiology. 2014;273:241–260CrossRefPubMedPubMedCentral Ahmed M, Solbiati L, Brace CL, Breen DJ, Callstrom MR, Charboneau JW, Chen MH, Choi BI, de Baere T, Dodd GD 3rd, Dupuy DE, Gervais DA, Gianfelice D, Gillams AR, Lee FT Jr, Leen E, Lencioni R, Littrup PJ, Livraghi T, Lu DS, McGahan JP, Meloni MF, Nikolic B, Pereira PL, Liang P, Rhim H, Rose SC, Salem R, Sofocleous CT, Solomon SB, Soulen MC, Tanaka M, Vogl TJ, Wood BJ, Goldberg SN. International Working Group on image-guided tumor ablation, Interventional Oncology Sans Frontieres Expert Panel, Technology Assessment Committee of the Society of Interventional Radiology, Standard of Practice Committee of the Cardiovascular and Interventional Radiological Society of Europe. Image-guided tumor ablation: standardization of terminology and reporting criteria—a 10-year update. Radiology. 2014;273:241–260CrossRefPubMedPubMedCentral
Metadata
Title
The arterial tumor enhancement pattern on contrast-enhanced computed tomography is associated with primary cancer death after radiofrequency ablation for small hepatocellular carcinoma
Authors
Ryo Shimizu
Hideyuki Tamai
Yoshiyuki Mori
Naoki Shingaki
Shuya Maeshima
Junya Nuta
Yoshimasa Maeda
Kosaku Moribata
Yosuke Muraki
Hisanobu Deguchi
Izumi Inoue
Takao Maekita
Mikitaka Iguchi
Jun Kato
Masao Ichinose
Publication date
01-03-2016
Publisher
Springer India
Published in
Hepatology International / Issue 2/2016
Print ISSN: 1936-0533
Electronic ISSN: 1936-0541
DOI
https://doi.org/10.1007/s12072-015-9678-1

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