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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

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Journal of Hepato-Biliary-Pancreatic Sciences

Abstract

Background

The value of the hepatobiliary phase of gadoxetic acid disodium (Gd-EOB-DTPA)-enhanced magnetic resonance imaging (MRI) in patients with hepatocellular carcinoma (HCC) has not been evaluated in detail.

Methods

Between 2008 and 2009, 61 patients with HCC within the Milan criteria underwent Gd-EOB-DTPA-enhanced MRI and hepatectomy. The tumor margin was determined preoperatively based on hepatobiliary phase images. Microscopic portal vein invasion (MPVI), intrahepatic metastasis (IM), and recurrence of HCC within 1 year after hepatectomy were evaluated in 24 patients with non-smooth margins at the periphery of the tumor and 37 patients with smooth margins.

Results

The number of patients with MPVI and IM of HCC was significantly higher among those with non-smooth margins (42 and 38%, respectively) than among those with smooth margins (3%; p = 0.0002 and 5%; p = 0.0042, respectively). A non-smooth margin was identified as a significant predictor of MPVI (odds ratio 18.814, p = 0.024) and IM (odds ratio 6.498, p = 0.036) of HCC on multivariate analysis. Furthermore, a non-smooth margin was identified as a significant predictor of recurrence within 1 year after hepatectomy (odds ratio 4.306, p = 0.04) on multivariate analysis.

Conclusions

A non-smooth tumor margin in the hepatobiliary phase of Gd-EOB-DTPA-enhanced MRI is useful to predict MPVI, IM, and early recurrence of HCC after hepatectomy.

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References

  1. Izumi R, Shimizu K, Ii T, Yagi M, Matsui O, Nonomura A, et al. Prognostic factors of hepatocellular carcinoma in patients undergoing hepatic resection. Gastroenterology. 1994;106:720–7.

    PubMed  CAS  Google Scholar 

  2. Tsai TJ, Chau GY, Lui WY, Tsay SH, King KL, Loong CC, et al. Clinical significance of microscopic tumor venous invasion in patients with resectable hepatocellular carcinoma. Surgery. 2000;127:603–8.

    Article  PubMed  CAS  Google Scholar 

  3. Vauthey JN, Lauwers GY, Esnaola NF, Do KA, Belghiti J, Mirza N, et al. Simplified staging for hepatocellular carcinoma. J Clin Oncol. 2002;20:1527–36.

    Article  PubMed  Google Scholar 

  4. Marsh JW, Dvorchik I, Bonham CA, Iwatsuki S. Is the pathologic TNM staging system for patients with hepatoma predictive of outcome? Cancer. 2000;88:538–43.

    Article  PubMed  CAS  Google Scholar 

  5. Hemming AW, Cattral MS, Reed AI, Van Der Werf WJ, Greig PD, Howard RJ. Liver transplantation for hepatocellular carcinoma. Ann Surg. 2001;233:652–9.

    Article  PubMed  CAS  Google Scholar 

  6. Shah SA, Tan JC, McGilvray ID, Cattral MS, Cleary SP, Levy GA, et al. Accuracy of staging as a predictor for recurrence after liver transplantation for hepatocellular carcinoma. Transplantation. 2006;81:1633–9.

    Article  PubMed  Google Scholar 

  7. Poon RT, Fan ST, Lo CM, Liu CL, Wong J. Difference in tumor invasiveness in cirrhotic patients with hepatocellular carcinoma fulfilling the Milan criteria treated by resection and transplantation. Impact on long-term survival. Ann Surg. 2007;245:51–8.

    Article  PubMed  Google Scholar 

  8. Adachi E, Maeda T, Kajiyama K, Kinukawa N, Matsumata T, Sugimachi K, et al. Factors correlated with portal venous invasion by hepatocellular carcinoma: univariate and multivariate analyses of 232 resected cases without preoperative treatments. Cancer. 1996;77:2022–31.

    Article  PubMed  CAS  Google Scholar 

  9. Esnaola NF, Lauwers GY, Mirza NQ, Nagorney DM, Doherty D, Ikai I, et al. Predictors of microvascular invasion in patients with hepatocellular carcinoma who are candidates for orthotopic liver transplantation. J Gastrointest Surg. 2002;6:224–32.

    Article  PubMed  Google Scholar 

  10. Pawlik TM, Delman KA, Vauthey JN, Nagorney DM, Ng IO, Ikai I, et al. Tumor size predicts vascular invasion and histologic grade: implications for selection of surgical treatment for hepatocellular carcinoma. Liver Transpl. 2005;11:1086–92.

    Article  PubMed  Google Scholar 

  11. Shirabe K, Itoh S, Yoshizumi T, Soejima Y, Taketomi A, Aishima S, et al. The predictors of microvascular invasion in candidates for liver transplantation with hepatocellular carcinoma: with special reference to the serum levels of des-gamma-carboxy prothrombin. J Surg Oncol. 2007;95:235–40.

    Article  PubMed  CAS  Google Scholar 

  12. Hasegawa K, Imamura H, Ijichi M, Matsuyama Y, Sano K, Sugawara Y, et al. Inclusion of tumor markers improves the correlation of the Milan criteria with vascular invasion and tumor cell differentiation in patients with hepatocellular carcinoma undergoing liver resection. J Gastrointest Surg. 2008;12:858–66.

    Article  PubMed  Google Scholar 

  13. Sakata J, Shirai Y, Wakai T, Kaneko K, Nagahashi M, Hatakeyama K. Preoperative predictors of vascular invasion in hepatocellular carcinoma. Eur J Surg Oncol. 2008;34:900–5.

    PubMed  CAS  Google Scholar 

  14. Miyata R, Tanimoto A, Wakabayashi G, Shimazu M, Nakatsuka S, Mukai M, et al. Accuracy of preoperative prediction of microinvasion of portal vein in hepatocellular carcinoma using superparamagnetic iron oxide-enhanced magnetic resonance imaging and computed tomography during hepatic angiography. J Gastroenterol. 2006;41:987–95.

    Article  PubMed  Google Scholar 

  15. Nishie A, Yoshimitsu K, Asayama Y, Irie H, Tajima T, Hirakawa M, et al. Radiologic detectability of minute portal venous invasion in hepatocellular carinoma. AJR Am J Roentgenol. 2008;190:81–7.

    Article  PubMed  Google Scholar 

  16. Shirabe K, Kajiyama K, Abe T, Sakamoto S, Fukuya T, Akazawa K, et al. Predictors of microscopic portal vein invasion by hepatocellular carcinoma: measurement of portal perfusion defect area ratio. J Gastroenterol Hepatol. 2009;24:1431–6.

    Article  PubMed  Google Scholar 

  17. Kim H, Park MS, Choi JY, Park YN, Kim MJ, Choi JS, et al. Can microvessel invasion of hepatocellular carcinoma be predicted by pre-operative MRI? Eur Radiol. 2009;19:1744–51.

    Article  PubMed  Google Scholar 

  18. Ichikawa T, Saito K, Yoshioka N, Tanimoto A, Gokan T, Takehara Y, et al. Detection and characterization of focal liver lesions. A Japanese phase III, multicenter comparison between Gadoxetic acid disodium-enhanced magnetic resonance imaging and contrast-enhanced computed tomography predominantly in patients with hepatocellular carcinoma and chronic liver disease. Invest Radiol. 2010;45:133–41.

    Article  PubMed  Google Scholar 

  19. Saito K, Kotake F, Ito N, Ozuki T, Mikami R, Abe K, et al. Gd-EOB-DTPA enhanced MRI for hepatocellular carcinoma: quantitative evaluation of tumor enhancement in hepatobiliary phase. Magn Reson Med Sci. 2005;4:1–9.

    Article  PubMed  Google Scholar 

  20. Kogita S, Imai Y, Okada M, Kim T, Takamura M, Fukuda K, et al. Gd-EOB-DTPA enhanced magnetic resonance images of hepatocellular carcinoma: correlation with histological grading and portal blood flow. Eur Radiol. 2010;20(10):2405–13.

    Article  PubMed  Google Scholar 

  21. Mazzaferro V, Regalia E, Doci R, Andreola S, Pulvirenti A, Bozzetti F, et al. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med. 1996;334:693–700.

    Article  PubMed  CAS  Google Scholar 

  22. Takasaki K, Kobayashi S, Tanaka S, Saito A, Yamamoto M, Hanyu F. Highly anatomically systematized hepatic resection with Glissonean sheath cord transection at the hepatic hilus. Int Surg. 1990;75:73–7.

    PubMed  CAS  Google Scholar 

  23. Takasaki K. Glissonean pedicle transection method for hepatic resection: a new concept of liver segmentation. J Hepatobiliary Pancreat Surg. 1998;5:286–91.

    Article  PubMed  CAS  Google Scholar 

  24. Liver Cancer Study Group of Japan. The general rules for the clinical and pathological study of primary liver cancer. 2nd English ed. Tokyo, Japan: Kanehara & Co., Ltd.; 2003.

  25. Terminology committee of the International Hepato-Pancreato-Biliary Association. IHPBA Brisbane 2000 Terminology of liver anatomy and resections. HPB. 2000;2:333–9.

    Google Scholar 

  26. Poon RT, Ng IO, Lau C, Zhu LX, Yu WC, Lo CM, et al. Serum vascular endothelial growth factor predicts venous invasion in hepatocellular carcinoma: a prospective study. Ann Surg. 2001;233:227–35.

    Article  PubMed  CAS  Google Scholar 

  27. Kanai T, Hirohashi S, Upton MP, Noguchi M, Kishi K, Makuuchi M, et al. Pathology of small hepatocellular carcinoma: a proposal for a new gross classification. Cancer. 1987;60:810–9.

    Article  PubMed  CAS  Google Scholar 

  28. Hui AM, Takayama T, Sano K, Kubota K, Akahane M, Ohtomo K, et al. Predictive value of gross classification of hepatocellular carcinoma on recurrence and survival after hepatectomy. J Hepatology. 2000;33:975–9.

    Article  CAS  Google Scholar 

  29. Shimada M, Rikimaru T, Hamatsu T, Yamashita Y, Terashi T, Taguchi K, et al. The role of macroscopic classification in nodular-type hepatocellular carcinoma. Am J Surg. 2001;182:177–82.

    Article  PubMed  CAS  Google Scholar 

  30. Yamamoto M, Takasaki K, Otsubo T, Katsuragawa H, Fukuda C, Katagiri S. Effectiveness of systematized hepatectomy with Glisson’s pedicle transection at hepatic hilus for small nodular hepatocellular carcinoma: retrospective analysis. Surgery. 2001;130:443–8.

    Article  PubMed  CAS  Google Scholar 

  31. Okusaka T, Okuda S, Ueno H, Ikeda M, Shimada K, Yamamoto J, et al. Satellite lesions in patients with small hepatocellular carcinoma with reference to clinicopathologic features. Cancer. 2002;95:1931–7.

    Article  PubMed  Google Scholar 

  32. Sumie S, Kuromatsu R, Okuda K, Ando E, Takata A, Fukushima N, et al. Microvascular invasion in patients with hepatocellular carcinoma and its predictable clinicopathological factors. Ann Surg Oncol. 2008;15:1375–82.

    Article  PubMed  Google Scholar 

  33. Poon RT, Fan ST, Ng IO, Lo CM, Liu CL, Wong J. Different risk factors and prognosis for early and late intrahepatic recurrence after resection of hepatocellular carcinoma. Cancer. 2000;89:500–7.

    Article  PubMed  CAS  Google Scholar 

  34. 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.

    Article  PubMed  Google Scholar 

  35. Shah SA, Greig PD, Gallinger S, Cattral MS, Dixon E, Kim RD, et al. Factors associated with early recurrence after resection for hepatocellular carcinoma and outcomes. J Am Coll Surg. 2006;202:275–83.

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors are indebted to Associate Professor Raoul Breugelmans of the Department of International Medical Communications of Tokyo Medical University for his review of this manuscript.

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Correspondence to Shun-ichi Ariizumi.

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Ariizumi, Si., 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 18, 575–585 (2011). https://doi.org/10.1007/s00534-010-0369-y

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