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Liver Regeneration is Preserved After At Least Four Repeated Liver Resections for Hepatocellular Carcinoma

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Abstract

Introduction

Repeated resection is known to prolong survival, with an acceptable morbidity rate, in patients with hepatocellular carcinoma. However, little is known about the effect of repeated liver resection on postoperative liver regeneration and liver function. The aim of this study is to determine the impact of repeated liver resections on the postoperative liver regeneration rate and liver function.

Methods

A total of 71 patients, who had undergone more than three liver resections for hepatocellular carcinoma between May 2001 and December 2013 at a tertiary care hospital in Japan, were included in the analysis. Among them, CT-volumetric data for the first, second, third, and fourth or more resections were available for 36, 49, 53, and 24 patients. We analyzed the regeneration index (RI) defined as the postoperative TLV/preoperative TLV × 100 was calculated after each operation to measure the degree of regeneration. Liver function was evaluated using the indocyanine green retention rate at 15 min (ICG-R15).

Results

No significant differences in RI were observed among the first, second, and third or more liver resection groups. No significant difference in the ICG R15 value was seen between the first liver resection group and the second or more liver resection group (P = 0.75). However, a significant difference in the RI was observed when the 1 segmentectomy or less liver resection group (median [range] RI 98.1 [72.9–119.9]) was compared with the 2 or more segmentectomy group (median [range] RI 90.5 [62.6–113.6]) (P = 0.005).

Conclusion

The regeneration process is maintained after as many as four repeated resections. Patients with sustained liver function can safely undergo repeated liver resections for recurrences of HCC.

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References

  1. Belghiti J, Panis Y, Farges O, Benhamou JP, Fekete F (1991) Intrahepatic recurrence after resection of hepatocellular carcinoma complicating cirrhosis. Ann Surg 214:114–117

    Article  CAS  Google Scholar 

  2. Imamura H, Matsuyama Y, Miyagawa Y, Ishida K, Shimada R, Miyagawa S, Makuuchi M et al (1999) Prognostic significance of anatomical resection and des-gamma-carboxy prothrombin in patients with hepatocellular carcinoma. Br J Surg 86:1032–1038

    Article  CAS  Google Scholar 

  3. Grazi GL, Ercolani G, Pierangeli F, Del Gaudio M, Cescon M, Cavallari A, Mazziotti A (2001) Improved results of liver resection for hepatocellular carcinoma on cirrhosis give the procedure added value. Ann Surg 234:71–78

    Article  CAS  Google Scholar 

  4. Nakajima Y, Ko S, Kanamura T, Nagao M, Kanehiro H, Hisanaga M, Aomatsu Y et al (2001) Repeat liver resection for hepatocellular carcinoma. J Am Coll Surg 192:339–344

    Article  CAS  Google Scholar 

  5. Poon RT, Fan ST, Lo CM, Liu CL, Wong J (2002) Long-term survival and pattern of recurrence after resection of small hepatocellular carcinoma in patients with preserved liver function: implications for a strategy of salvage transplantation. Ann Surg 235:373–382

    Article  Google Scholar 

  6. Mise Y, Hasegawa K, Shindoh J, Ishizawa T, Aoki T, Sakamoto Y, Sugawara Y et al (2015) The feasibility of third or more repeat hepatectomy for recurrent hepatocellular carcinoma. Ann Surg 262:347–357

    Article  Google Scholar 

  7. Truant S, Bouras AF, Petrovai G, Buob D, Ernst O, Boleslawski E, Hebbar M et al (2013) Volumetric gain of the liver after major hepatectomy in obese patients: a case-matched study in 84 patients. Ann Surg 258:696–702 (discussion 702–694)

    Article  Google Scholar 

  8. Millet G, Truant S, Leteurtre E, Hebbar M, Zerbib P, Huet G, Boleslawski E et al (2012) Volumetric analysis of remnant liver regeneration after major hepatectomy in bevacizumab-treated patients: a case-matched study in 82 patients. Ann Surg 256:755–761 (discussion 761–752)

    Article  Google Scholar 

  9. Enkhbold C, Morine Y, Utsunomiya T, Imura S, Ikemoto T, Arakawa Y, Saito Y et al (2015) Dysfunction of liver regeneration in aged liver after partial hepatectomy. J Gastroenterol Hepatol 30:1217–1224

    Article  CAS  Google Scholar 

  10. Yamanaka N, Okamoto E, Kawamura E, Kato T, Oriyama T, Fujimoto J, Furukawa K et al (1993) Dynamics of normal and injured human liver regeneration after hepatectomy as assessed on the basis of computed tomography and liver function. Hepatology 18:79–85

    Article  CAS  Google Scholar 

  11. Nagasue N, Yukaya H, Ogawa Y, Kohno H, Nakamura T (1987) Human liver regeneration after major hepatic resection. A study of normal liver and livers with chronic hepatitis and cirrhosis. Ann Surg 206:30–39

    Article  CAS  Google Scholar 

  12. Makuuchi M, Kosuge T, Takayama T, Yamazaki S, Kakazu T, Miyagawa S, Kawasaki S (1993) Surgery for small liver cancers. Semin Surg Oncol 9:298–304

    Article  CAS  Google Scholar 

  13. Imamura H, Seyama Y, Kokudo N, Maema A, Sugawara Y, Sano K, Takayama T et al (2003) One thousand fifty-six hepatectomies without mortality in 8 years. Arch Surg 138:1198–1206 discussion 1206

    Article  Google Scholar 

  14. Makuuchi M, Hasegawa H, Yamazaki S (1985) Ultrasonically guided subsegmentectomy. Surg Gynecol Obstet 161:346–350

    CAS  Google Scholar 

  15. Takayama T, Makuuchi M, Watanabe K, Kosuge T, Takayasu K, Yamazaki S, Hasegawa H (1991) A new method for mapping hepatic subsegment: counterstaining identification technique. Surgery 109:226–229

    CAS  PubMed  Google Scholar 

  16. Hasegawa K, Kokudo N, Imamura H, Matsuyama Y, Aoki T, Minagawa M, Sano K et al (2005) Prognostic impact of anatomic resection for hepatocellular carcinoma. Ann Surg 242:252–259

    Article  Google Scholar 

  17. Etudes CC (1953) Anatomiques et chirurgicales. Arch Surg 66:599–616

    Article  Google Scholar 

  18. Healey JE Jr, Schroy PC (1953) Anatomy of the biliary ducts within the human liver; analysis of the prevailing pattern of branchings and the major variations of the biliary ducts. AMA Arch Surg 66:599–616

    Article  Google Scholar 

  19. Aoki T, Imamura H, Matsuyama Y, Kishi Y, Kobayashi T, Sugawara Y, Makuuchi M et al (2011) Convergence process of volumetric liver regeneration after living-donor hepatectomy. J Gastrointest Surg 15:1594–1601

    Article  Google Scholar 

  20. Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213

    Article  Google Scholar 

  21. Okamoto E, Kyo A, Yamanaka N, Tanaka N, Kuwata K (1984) Prediction of the safe limits of hepatectomy by combined volumetric and functional measurements in patients with impaired hepatic function. Surgery 95:586–592

    CAS  PubMed  Google Scholar 

  22. Zappa M, Dondero F, Sibert A, Vullierme MP, Belghiti J, Vilgrain V (2009) Liver regeneration at day 7 after right hepatectomy: global and segmental volumetric analysis by using CT. Radiology 252:426–432

    Article  Google Scholar 

  23. Dello SA, Kele PG, Porte RJ, van Dam RM, Klaase JM, Verhoef C, van Gulik T et al (2014) Influence of preoperative chemotherapy on CT volumetric liver regeneration following right hemihepatectomy. World J Surg 38:497–504. https://doi.org/10.1007/s00268-013-2278-0

    Article  PubMed  Google Scholar 

  24. Kele PG, de Boer M, van der Jagt EJ, Lisman T, Porte RJ (2012) Early hepatic regeneration index and completeness of regeneration at 6 months after partial hepatectomy. Br J Surg 99:1113–1119

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Hepato-Biliary-Pancreatic Surgery Division, Department of Surgery, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, Japan

    Takamune Yamaguchi, Takashi Kokudo, Nobuhisa Akamatsu, Junichi Kaneko, Junichi Arita, Yoshihiro Sakamoto & Kiyoshi Hasegawa

  2. National Center for Global Health and Medicine, Tokyo, Japan

    Norihiro Kokudo

Authors
  1. Takamune Yamaguchi
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  2. Takashi Kokudo
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  3. Nobuhisa Akamatsu
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  4. Junichi Kaneko
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  5. Junichi Arita
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  6. Yoshihiro Sakamoto
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  7. Norihiro Kokudo
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  8. Kiyoshi Hasegawa
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Correspondence to Norihiro Kokudo or Kiyoshi Hasegawa.

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The authors do not have any conflicts of interest to report; no financial support was received.

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Yamaguchi, T., Kokudo, T., Akamatsu, N. et al. Liver Regeneration is Preserved After At Least Four Repeated Liver Resections for Hepatocellular Carcinoma. World J Surg 42, 4070–4080 (2018). https://doi.org/10.1007/s00268-018-4714-7

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  • DOI: https://doi.org/10.1007/s00268-018-4714-7

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