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Published in: Journal of Gastroenterology 10/2014

01-10-2014 | Original Article—Liver, Pancreas, and Biliary Tract

Proposal of objective morphological classification system for hepatocellular carcinoma using preoperative multiphase computed tomography

Authors: Hisashi Nakayama, Tadatoshi Takayama, Takao Okubo, Tokio Higaki, Yutaka Midorikawa, Masamichi Moriguchi, Akiyoshi Itoh

Published in: Journal of Gastroenterology | Issue 10/2014

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Abstract

Background

To establish a preoperative morphological classification system for hepatocellular carcinoma using multiphase computed tomography.

Methods

All consecutive patients who were diagnosed with hepatocellular carcinoma between 2004 and 2009 were enrolled, for a total of 232 patients. The concavity and convexity of each outer contour of hepatocellular carcinoma acquired from multiphase computed tomography were analyzed, and the area and depth of each indentation were quantified. The indentation area to tumor area ratio (s:S) and the s:S ratio multiplied by the indentation depth to indentation base ratio (s:S × d:t) were used as feature values reflecting the individual shapes.

Results

Using a hierarchical cluster analysis, the shapes were classified into three groups: Type I (smooth: n = 158), Type II (jagged: n = 63), and Type III (rough: n = 11). The 5-year survival rates for Types I, II, and III were 64, 53, and 0 %, respectively (I vs. II, P = 0.038; I vs. III, P = 0.001; II vs. III, P = 0.002). The 5-year disease-free survival rates for Types I, II, and III were 27, 23, and 0 %, respectively (I vs. III, P = 0.0003 and II vs. III, P = 0.008). Microscopic portal venous invasion was significantly more likely with Type III than with Type I or II (P < 0.001 and P = 0.001, respectively).

Conclusions

The newly developed semiautomatic computed tomography-based morphological classification system appears to provide a promising additional criterion for the prognostic categorization of patients with hepatocellular carcinoma.
Literature
1.
go back to reference Edmondson HA, Steiner PE. Primary carcinoma of the liver: a study of 100 cases among 48,900 necropsies. Cancer. 1954;7:462–503.PubMedCrossRef Edmondson HA, Steiner PE. Primary carcinoma of the liver: a study of 100 cases among 48,900 necropsies. Cancer. 1954;7:462–503.PubMedCrossRef
2.
go back to reference Nakashima T, Okuda K, Kojiro M, et al. Pathology of hepatocellular carcinoma in Japan. 232 consecutive cases autopsied in ten years. Cancer. 1983;51:863–77.PubMedCrossRef Nakashima T, Okuda K, Kojiro M, et al. Pathology of hepatocellular carcinoma in Japan. 232 consecutive cases autopsied in ten years. Cancer. 1983;51:863–77.PubMedCrossRef
3.
go back to reference Okuda K, Peters RL, Simson IW. Gross anatomic features of hepatocellular carcinoma from three disparate geographic areas. Proposal of new classification. Cancer. 1984;54:2165–73.PubMedCrossRef Okuda K, Peters RL, Simson IW. Gross anatomic features of hepatocellular carcinoma from three disparate geographic areas. Proposal of new classification. Cancer. 1984;54:2165–73.PubMedCrossRef
4.
go back to reference Kanai T, Hirohashi S, Upton MP, et al. Pathology of small hepatocellular carcinoma. A proposal for a new gross classification. Cancer. 1987;60:810–9.PubMedCrossRef Kanai T, Hirohashi S, Upton MP, et al. Pathology of small hepatocellular carcinoma. A proposal for a new gross classification. Cancer. 1987;60:810–9.PubMedCrossRef
5.
go back to reference Takayama T, Makuuchi M, Hirohashi S, et al. Early hepatocellular carcinoma as an entity with a high rate of surgical cure. Hepatology. 1998;28:1241–6.PubMedCrossRef Takayama T, Makuuchi M, Hirohashi S, et al. Early hepatocellular carcinoma as an entity with a high rate of surgical cure. Hepatology. 1998;28:1241–6.PubMedCrossRef
6.
go back to reference Japan LCSGo. General rules for the clinical and pathological study of primary liver cancer. 3rd English edition. Tokyo: Kanehara; 2010. Japan LCSGo. General rules for the clinical and pathological study of primary liver cancer. 3rd English edition. Tokyo: Kanehara; 2010.
7.
go back to reference Shimada M, Rikimaru T, Hamatsu T, et al. The role of macroscopic classification in nodular-type hepatocellular carcinoma. Am J Surg. 2001;182:177–82.PubMedCrossRef Shimada M, Rikimaru T, Hamatsu T, et al. The role of macroscopic classification in nodular-type hepatocellular carcinoma. Am J Surg. 2001;182:177–82.PubMedCrossRef
8.
9.
go back to reference Takayasu K, Muramatsu Y, Mizuguchi Y, et al. CT evaluation of the progression of hypoattenuating nodular lesions in virus-related chronic liver disease. AJR Am J Roentgenol. 2006;187:454–63.PubMedCrossRef Takayasu K, Muramatsu Y, Mizuguchi Y, et al. CT evaluation of the progression of hypoattenuating nodular lesions in virus-related chronic liver disease. AJR Am J Roentgenol. 2006;187:454–63.PubMedCrossRef
10.
go back to reference Breitenstein S, DeOliveira ML, Raptis DA, et al. Novel and simple preoperative score predicting complications after liver resection in noncirrhotic patients. Ann Surg. 2010;252:726–34.PubMedCrossRef Breitenstein S, DeOliveira ML, Raptis DA, et al. Novel and simple preoperative score predicting complications after liver resection in noncirrhotic patients. Ann Surg. 2010;252:726–34.PubMedCrossRef
11.
go back to reference Torzilli G, Minagawa M, Takayama T, et al. Accurate preoperative evaluation of liver mass lesions without fine-needle biopsy. Hepatology. 1999;30:889–93.PubMedCrossRef Torzilli G, Minagawa M, Takayama T, et al. Accurate preoperative evaluation of liver mass lesions without fine-needle biopsy. Hepatology. 1999;30:889–93.PubMedCrossRef
12.
go back to reference Leoni S, Piscaglia F, Golfieri R, et al. The impact of vascular and nonvascular findings on the noninvasive diagnosis of small hepatocellular carcinoma based on the EASL and AASLD criteria. Am J Gastroenterol. 2010;105:599–609.PubMedCrossRef Leoni S, Piscaglia F, Golfieri R, et al. The impact of vascular and nonvascular findings on the noninvasive diagnosis of small hepatocellular carcinoma based on the EASL and AASLD criteria. Am J Gastroenterol. 2010;105:599–609.PubMedCrossRef
13.
go back to reference Singal AG, Nehra M, Adams-Huet B, et al. Detection of hepatocellular carcinoma at advanced stages among patients in the HALT-C trial: where did surveillance fail? Am J Gastroenterol. 2013;108:425–32.PubMedCrossRef Singal AG, Nehra M, Adams-Huet B, et al. Detection of hepatocellular carcinoma at advanced stages among patients in the HALT-C trial: where did surveillance fail? Am J Gastroenterol. 2013;108:425–32.PubMedCrossRef
14.
go back to reference Ariizumi S, Kitagawa K, Kotera Y, et al. A non-smooth tumor margin in the hepatobiliary phase of gadoxetic acid disodium (Gd-EOB-DTPA)-enhanced magnetic resonance imaging predicts microscopic portal vein invasion, intrahepatic metastasis, and early recurrence after hepatectomy in patients with hepatocellular carcinoma. J Hepatobiliary Pancreat Sci. 2011;18:575–85.PubMedCrossRef Ariizumi S, Kitagawa K, Kotera Y, et al. A non-smooth tumor margin in the hepatobiliary phase of gadoxetic acid disodium (Gd-EOB-DTPA)-enhanced magnetic resonance imaging predicts microscopic portal vein invasion, intrahepatic metastasis, and early recurrence after hepatectomy in patients with hepatocellular carcinoma. J Hepatobiliary Pancreat Sci. 2011;18:575–85.PubMedCrossRef
15.
go back to reference Wakai T, Shirai Y, Nomura T, et al. Computed tomographic features of hepatocellular carcinoma predict long-term survival after hepatic resection. Eur J Surg Oncol. 2002;28:235–42.PubMedCrossRef Wakai T, Shirai Y, Nomura T, et al. Computed tomographic features of hepatocellular carcinoma predict long-term survival after hepatic resection. Eur J Surg Oncol. 2002;28:235–42.PubMedCrossRef
16.
go back to reference Shirabe K, Aishima S, Taketomi A, et al. Prognostic importance of the gross classification of hepatocellular carcinoma in living donor-related liver transplantation. Br J Surg. 2011;98:261–7.PubMedCrossRef Shirabe K, Aishima S, Taketomi A, et al. Prognostic importance of the gross classification of hepatocellular carcinoma in living donor-related liver transplantation. Br J Surg. 2011;98:261–7.PubMedCrossRef
17.
19.
go back to reference Makuuchi M, Kosuge T, Takayama T, et al. Surgery for small liver cancers. Semin Surg Oncol. 1993;9:298–304.PubMedCrossRef Makuuchi M, Kosuge T, Takayama T, et al. Surgery for small liver cancers. Semin Surg Oncol. 1993;9:298–304.PubMedCrossRef
20.
go back to reference Ward JHJ. Hierarchical grouping to optimize an objective function. J Am Stat Assoc. 1963;58:236–44.CrossRef Ward JHJ. Hierarchical grouping to optimize an objective function. J Am Stat Assoc. 1963;58:236–44.CrossRef
21.
go back to reference Minagawa M, Ikai I, Matsuyama Y, et al. Staging of hepatocellular carcinoma: assessment of the Japanese TNM and AJCC/UICC TNM systems in a cohort of 13,772 patients in Japan. Ann Surg. 2007;245:909–22.PubMedCrossRefPubMedCentral Minagawa M, Ikai I, Matsuyama Y, et al. Staging of hepatocellular carcinoma: assessment of the Japanese TNM and AJCC/UICC TNM systems in a cohort of 13,772 patients in Japan. Ann Surg. 2007;245:909–22.PubMedCrossRefPubMedCentral
23.
go back to reference LaVange LM, Koch GG, Schwartz TA. Applying sample survey methods to clinical trials data. Stat Med. 2001;20:2609–23.PubMedCrossRef LaVange LM, Koch GG, Schwartz TA. Applying sample survey methods to clinical trials data. Stat Med. 2001;20:2609–23.PubMedCrossRef
24.
25.
go back to reference Eguchi S, Takatsuki M, Hidaka M, et al. Predictor for histological microvascular invasion of hepatocellular carcinoma: a lesson from 229 consecutive cases of curative liver resection. World J Surg. 2010;34:1034–8.PubMedCrossRef Eguchi S, Takatsuki M, Hidaka M, et al. Predictor for histological microvascular invasion of hepatocellular carcinoma: a lesson from 229 consecutive cases of curative liver resection. World J Surg. 2010;34:1034–8.PubMedCrossRef
26.
go back to reference Hui AM, Takayama T, Sano K, et al. Predictive value of gross classification of hepatocellular carcinoma on recurrence and survival after hepatectomy. J Hepatol. 2000;33:975–9.PubMedCrossRef Hui AM, Takayama T, Sano K, et al. Predictive value of gross classification of hepatocellular carcinoma on recurrence and survival after hepatectomy. J Hepatol. 2000;33:975–9.PubMedCrossRef
27.
go back to reference Kawamura Y, Ikeda K, Hirakawa M, et al. New classification of dynamic computed tomography images predictive of malignant characteristics of hepatocellular carcinoma. Hepatol Res. 2010;40:1006–14.PubMedCrossRef Kawamura Y, Ikeda K, Hirakawa M, et al. New classification of dynamic computed tomography images predictive of malignant characteristics of hepatocellular carcinoma. Hepatol Res. 2010;40:1006–14.PubMedCrossRef
28.
go back to reference Tanaka H, Iijima H, Higashiura A, et al. New malignant grading system for hepatocellular carcinoma using the Sonazoid contrast agent for ultrasonography. J Gastroenterol (Epub ahead of print). Tanaka H, Iijima H, Higashiura A, et al. New malignant grading system for hepatocellular carcinoma using the Sonazoid contrast agent for ultrasonography. J Gastroenterol (Epub ahead of print).
29.
go back to reference Yang LY, Fang F, Ou DP, et al. Solitary large hepatocellular carcinoma: a specific subtype of hepatocellular carcinoma with good outcome after hepatic resection. Ann Surg. 2009;249:118–23.PubMedCrossRef Yang LY, Fang F, Ou DP, et al. Solitary large hepatocellular carcinoma: a specific subtype of hepatocellular carcinoma with good outcome after hepatic resection. Ann Surg. 2009;249:118–23.PubMedCrossRef
30.
go back to reference Choi GH, Han DH, Kim DH, et al. Outcome after curative resection for a huge (> or = 10 cm) hepatocellular carcinoma and prognostic significance of gross tumor classification. Am J Surg. 2009;198:693–701.PubMedCrossRef Choi GH, Han DH, Kim DH, et al. Outcome after curative resection for a huge (> or = 10 cm) hepatocellular carcinoma and prognostic significance of gross tumor classification. Am J Surg. 2009;198:693–701.PubMedCrossRef
31.
go back to reference Shiina S, Tateishi R, Arano T, et al. Radiofrequency ablation for hepatocellular carcinoma: 10-year outcome and prognostic factors. Am J Gastroenterol. 2012;107:569–77.PubMedCrossRefPubMedCentral Shiina S, Tateishi R, Arano T, et al. Radiofrequency ablation for hepatocellular carcinoma: 10-year outcome and prognostic factors. Am J Gastroenterol. 2012;107:569–77.PubMedCrossRefPubMedCentral
32.
go back to reference Torzilli G, Belghiti J, Kokudo N, et al. A snapshot of the effective indications and results of surgery for hepatocellular carcinoma in tertiary referral centers: is it adherent to the EASL/AASLD recommendations? An observational study of the HCC East-West Study Group. Ann Surg. 2013;257:929–37.PubMedCrossRef Torzilli G, Belghiti J, Kokudo N, et al. A snapshot of the effective indications and results of surgery for hepatocellular carcinoma in tertiary referral centers: is it adherent to the EASL/AASLD recommendations? An observational study of the HCC East-West Study Group. Ann Surg. 2013;257:929–37.PubMedCrossRef
34.
go back to reference Takayama T, Sekine T, Makuuchi M, et al. Adoptive immunotherapy to lower postsurgical recurrence rates of hepatocellular carcinoma: a randomised trial. Lancet. 2000;356:802–7.PubMedCrossRef Takayama T, Sekine T, Makuuchi M, et al. Adoptive immunotherapy to lower postsurgical recurrence rates of hepatocellular carcinoma: a randomised trial. Lancet. 2000;356:802–7.PubMedCrossRef
35.
go back to reference Saito S, Yamanaka J, Miura K, et al. A novel 3D hepatectomy simulation based on liver circulation: application to liver resection and transplantation. Hepatology. 2005;41:1297–304.PubMedCrossRef Saito S, Yamanaka J, Miura K, et al. A novel 3D hepatectomy simulation based on liver circulation: application to liver resection and transplantation. Hepatology. 2005;41:1297–304.PubMedCrossRef
Metadata
Title
Proposal of objective morphological classification system for hepatocellular carcinoma using preoperative multiphase computed tomography
Authors
Hisashi Nakayama
Tadatoshi Takayama
Takao Okubo
Tokio Higaki
Yutaka Midorikawa
Masamichi Moriguchi
Akiyoshi Itoh
Publication date
01-10-2014
Publisher
Springer Japan
Published in
Journal of Gastroenterology / Issue 10/2014
Print ISSN: 0944-1174
Electronic ISSN: 1435-5922
DOI
https://doi.org/10.1007/s00535-013-0908-9

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