Skip to main content

Advertisement

SpringerLink
Log in

Influence of higher BMI for hepatitis B- and C-related hepatocellular carcinomas

  • ORIGINAL ARTICLE
  • Published:
Langenbeck's Archives of Surgery Aims and scope Submit manuscript

Abstract

Purpose

Although obesity is associated with hepatocellular carcinoma (HCC) development, its impact on the surgical outcomes of patients with hepatitis B virus (HBV)—and hepatitis C virus (HCV)—related HCC remains unclear.

Methods

We retrospectively analyzed 714 patients with HCC who underwent curative hepatectomy. Among them, the HBV-related HCC group (n = 125) and HCV-related HCC group (n = 426) were subdivided according to the presence of body mass index (BMI) ≥ 25 kg/m2. The surgical outcomes were compared.

Results

The 5-year overall survival rate after hepatectomy in the HBV-related HCC group was significantly better than that in the HCV-related HCC group. The 5-year overall survival rates of the HBV-related HCC with and without BMI ≥ 25 kg/m2 groups were 65 and 85%, respectively. The 5-year overall survival rates in the HCV-related HCC with and without BMI ≥ 25 kg/m2 groups were 75 and 65%, respectively. The HBV-related HCC with BMI ≥ 25 kg/m2 groups had a significantly worse prognosis than the HBV-related HCC without BMI ≥ 25 kg/m2 groups, while the HCV-related HCC with BMI ≥ 25 kg/m2 groups had a significantly better prognosis than the HCV-related HCC without BMI ≥ 25 kg/m2 groups. Multivariate analysis revealed that BMI ≥ 25 kg/m2 was the positive and negative prognostic factor for the surgical outcomes of patients with HBV- and HCV-related HCC, respectively.

Conclusions

BMI ≥ 25 kg/m2 negatively affected the surgical outcomes of patients with HBV-related HCC and positively affected those of patients with HCV-related HCC.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61(2):69–90. doi:10.3322/caac.20107

    Article  PubMed  Google Scholar 

  2. El-Serag HB (2012) Epidemiology of viral hepatitis and hepatocellular carcinoma. Gastroenterology 142(6):1264–1273 e1261. doi:10.1053/j.gastro.2011.12.061

    Article  PubMed  PubMed Central  Google Scholar 

  3. Freeman AJ, Dore GJ, Law MG, Thorpe M, Von Overbeck J, Lloyd AR, Marinos G, Kaldor JM (2001) Estimating progression to cirrhosis in chronic hepatitis C virus infection. Hepatology 34(4 Pt 1):809–816. doi:10.1053/jhep.2001.27831

    Article  CAS  PubMed  Google Scholar 

  4. Baffy G, Brunt EM, Caldwell SH (2012) Hepatocellular carcinoma in non-alcoholic fatty liver disease: an emerging menace. J Hepatol 56(6):1384–1391. doi:10.1016/j.jhep.2011.10.027

    Article  PubMed  Google Scholar 

  5. Bugianesi E, Leone N, Vanni E, Marchesini G, Brunello F, Carucci P, Musso A, De Paolis P, Capussotti L, Salizzoni M, Rizzetto M (2002) Expanding the natural history of nonalcoholic steatohepatitis: from cryptogenic cirrhosis to hepatocellular carcinoma. Gastroenterology 123(1):134–140

    Article  PubMed  Google Scholar 

  6. Starley BQ, Calcagno CJ, Harrison SA (2010) Nonalcoholic fatty liver disease and hepatocellular carcinoma: a weighty connection. Hepatology 51(5):1820–1832. doi:10.1002/hep.23594

    Article  PubMed  Google Scholar 

  7. White DL, Kanwal F, El-Serag HB (2012) Association between nonalcoholic fatty liver disease and risk for hepatocellular cancer, based on systematic review. Clin Gastroenterol Hepatol 10(12):1342–1359 e1342. doi:10.1016/j.cgh.2012.10.001

    Article  PubMed  PubMed Central  Google Scholar 

  8. Nishikawa H, Osaki Y, Takeda H, Sakamoto A, Saito S, Nishijima N, Nasu A, Arimoto A, Kita R, Kimura T (2013) Effect of body mass index on survival after curative therapy for non-B non-C hepatocellular carcinoma. J Gastrointestin Liver Dis 22(2):173–181

    PubMed  Google Scholar 

  9. Yoshida N, Takayama T, Midorikawa Y, Higaki T, Nakayama H, Moriguchi M, Tsuji S (2015) Surgical outcomes in patients with hepatocellular carcinoma associated with metabolic syndrome. World J Surg 39(2):471–477. doi:10.1007/s00268-014-2828-0

    Article  PubMed  Google Scholar 

  10. Nishio T, Hatano E, Sakurai T, Taura K, Okuno M, Kasai Y, Seo S, Yasuchika K, Mori A, Kaido T, Uemoto S (2015) Impact of hepatic steatosis on disease-free survival in patients with non-B non-C hepatocellular carcinoma undergoing hepatic resection. Ann Surg Oncol 22(7):2226–2234. doi:10.1245/s10434-014-4181-9

    Article  PubMed  Google Scholar 

  11. McCurry J (2007) Japan battles with obesity. Lancet 369(9560):451–452. doi:10.1016/S0140-6736(07)60214-1

    Article  PubMed  Google Scholar 

  12. The Examination Committee of Criteria for ‘Obesity Disease’ in Japan, Japan Society for the Study of Obesity (2002) New criteria for ‘obesity disease’ in Japan. Circ J 66 (11):987–992

  13. Shiwaku K, Anuurad E, Enkhmaa B, Kitajima K, Yamane Y (2004) Appropriate BMI for Asian populations. Lancet 363(9414):1077. doi:10.1016/S0140-6736(04)15856-X

    Article  PubMed  Google Scholar 

  14. Minagawa M, Ikai I, Matsuyama Y, Yamaoka Y, Makuuchi M (2007) 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 245(6):909–922. doi:10.1097/01.sla.0000254368.65878.da

    Article  PubMed  PubMed Central  Google Scholar 

  15. Makuuchi M, Kosuge T, Takayama T, Yamazaki S, Kakazu T, Miyagawa S, Kawasaki S (1993) Surgery for small liver cancers. Semin Surg Oncol 9(4):298–304

    Article  CAS  PubMed  Google Scholar 

  16. Itamoto T, Katayama K, Nakahara H, Tashiro H, Asahara T (2003) Autologous blood storage before hepatectomy for hepatocellular carcinoma with underlying liver disease. Br J Surg 90(1):23–28. doi:10.1002/bjs.4012

    Article  CAS  PubMed  Google Scholar 

  17. Kuroda S, Tashiro H, Kobayashi T, Oshita A, Amano H, Ohdan H (2011) Selection criteria for hepatectomy in patients with hepatocellular carcinoma classified as Child-Pugh class B. World J Surg 35(4):834–841. doi:10.1007/s00268-010-0929-y

    Article  PubMed  Google Scholar 

  18. 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(2):205–213

    Article  PubMed  PubMed Central  Google Scholar 

  19. Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, de Santibanes E, Pekolj J, Slankamenac K, Bassi C, Graf R, Vonlanthen R, Padbury R, Cameron JL, Makuuchi M (2009) The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg 250(2):187–196. doi:10.1097/SLA.0b013e3181b13ca2

    Article  PubMed  Google Scholar 

  20. Takenaka K, Yamamoto K, Taketomi A, Itasaka H, Adachi E, Shirabe K, Nishizaki T, Yanaga K, Sugimachi K (1995) A comparison of the surgical results in patients with hepatitis B versus hepatitis C-related hepatocellular carcinoma. Hepatology 22(1):20–24

    CAS  PubMed  Google Scholar 

  21. Chen MF, Jeng LB, Lee WC (2002) Surgical results in patients with hepatitis virus-related hepatocellular carcinoma in Taiwan. World J Surg 26(6):742–747. doi:10.1007/s00268-002-6143-9

    Article  PubMed  Google Scholar 

  22. Franssen B, Alshebeeb K, Tabrizian P, Marti J, Pierobon ES, Lubezky N, Roayaie S, Florman S, Schwartz ME (2014) Differences in surgical outcomes between hepatitis B- and hepatitis C-related hepatocellular carcinoma: a retrospective analysis of a single north American center. Ann Surg 260(4):650–656; discussion 656-658. doi:10.1097/SLA.0000000000000917

    Article  PubMed  Google Scholar 

  23. Sinn DH, Gwak GY, Cho J, Paik SW, Yoo BC (2014) Comparison of clinical manifestations and outcomes between hepatitis B virus- and hepatitis C virus-related hepatocellular carcinoma: analysis of a nationwide cohort. PLoS One 9(11):e112184. doi:10.1371/journal.pone.0112184

    Article  PubMed  PubMed Central  Google Scholar 

  24. Sasaki Y, Yamada T, Tanaka H, Ohigashi H, Eguchi H, Yano M, Ishikawa O, Imaoka S (2006) Risk of recurrence in a long-term follow-up after surgery in 417 patients with hepatitis B- or hepatitis C-related hepatocellular carcinoma. Ann Surg 244(5):771–780. doi:10.1097/01.sla.0000225126.56483.b3

    Article  PubMed  PubMed Central  Google Scholar 

  25. Naito S, Imamura H, Tukada A, Matsuyama Y, Yoshimoto J, Sugo H, Ishizaki Y, Kawasaki S (2014) Postoperative recurrence pattern and prognosis of patients with hepatocellular carcinoma, with particular reference to the hepatitis viral infection status. Liver Int 34(5):802–813. doi:10.1111/liv.12447

    Article  PubMed  Google Scholar 

  26. Chen MF, Jeng LB, Lee WC, Chen TC (1998) Surgical results in patients with dual hepatitis B- and C-related hepatocellular carcinoma compared with hepatitis B- or C-related hepatocellular carcinoma. Surgery 123(5):554–559. doi:10.1067/msy.1998.87237

    Article  CAS  PubMed  Google Scholar 

  27. Miyagawa S, Kawasaki S, Makuuchi M (1996) Comparison of the characteristics of hepatocellular carcinoma between hepatitis B and C viral infection: tumor multicentricity in cirrhotic liver with hepatitis C. Hepatology 24(2):307–310. doi:10.1053/jhep.1996.v24.pm0008690397

    Article  CAS  PubMed  Google Scholar 

  28. Shiraishi M, Hiroyasu S, Nagahama M, Tomita S, Miyahira T, Kusano T, Furukawa M, Muto Y (1999) Characteristics of hepatocellular carcinoma in patients with negative virus markers: clinicopathologic study of resected tumors. World J Surg 23(3):301–305

    Article  CAS  PubMed  Google Scholar 

  29. Yamanaka N, Tanaka T, Tanaka W, Yamanaka J, Yasui C, Kuroda N, Takada M, Okamoto E (1997) Correlation of hepatitis virus serologic status with clinicopathologic features in patients undergoing hepatectomy for hepatocellular carcinoma. Cancer 79(8):1509–1515

    Article  CAS  PubMed  Google Scholar 

  30. Utsunomiya T, Shimada M, Kudo M, Ichida T, Matsui O, Izumi N, Matsuyama Y, Sakamoto M, Nakashima O, Ku Y, Takayama T, Kokudo N (2015) A comparison of the surgical outcomes among patients with HBV-positive, HCV-positive, and non-B non-C hepatocellular carcinoma: a Nationwide study of 11,950 patients. Ann Surg 261(3):513–520. doi:10.1097/SLA.0000000000000821

    Article  PubMed  Google Scholar 

  31. Shim JH, Lee HC, Kim KM, Lim YS, Chung YH, Lee YS, Suh DJ (2010) Efficacy of entecavir in treatment-naive patients with hepatitis B virus-related decompensated cirrhosis. J Hepatol 52(2):176–182. doi:10.1016/j.jhep.2009.11.007

    Article  CAS  PubMed  Google Scholar 

  32. Poon RT, Fan ST, Ng IO, Lo CM, Liu CL, Wong J (2000) Different risk factors and prognosis for early and late intrahepatic recurrence after resection of hepatocellular carcinoma. Cancer 89(3):500–507

    Article  CAS  PubMed  Google Scholar 

  33. Gassmann P, Spieker T, Haier J, Schmidt F, Mardin WA, Senninger N (2010) Prognostic impact of underlying liver fibrosis and cirrhosis after curative resection of hepatocellular carcinoma. World J Surg 34(10):2442–2451. doi:10.1007/s00268-010-0655-5

    Article  PubMed  Google Scholar 

  34. Ko S, Kanehiro H, Hisanaga M, Nagao M, Ikeda N, Nakajima Y (2002) Liver fibrosis increases the risk of intrahepatic recurrence after hepatectomy for hepatocellular carcinoma. Br J Surg 89(1):57–62. doi:10.1046/j.0007-1323.2001.01969.x

    Article  CAS  PubMed  Google Scholar 

  35. Tarao K, Ohkawa S, Shimizu A, Harada M, Nakamura Y, Ito Y, Tamai S, Hoshino H, Inoue T, Kanisawa M (1994) Significance of hepatocellular proliferation in the development of hepatocellular carcinoma from anti-hepatitis C virus-positive cirrhotic patients. Cancer 73(4):1149–1154

    Article  CAS  PubMed  Google Scholar 

  36. Rua S, Comino A, Fruttero A, Torchio P, Bouzari H, Taraglio S, Torchio B, Capussotti L (1996) Flow cytometric DNA analysis of cirrhotic liver cells in patients with hepatocellular carcinoma can provide a new prognostic factor. Cancer 78(6):1195–1202. doi:10.1002/(SICI)1097-0142(19960915)78:6<1195::AID-CNCR5>3.0.CO;2-9

    Article  CAS  PubMed  Google Scholar 

  37. Oishi K, Itamoto T, Kohashi T, Matsugu Y, Nakahara H, Kitamoto M (2014) Safety of hepatectomy for elderly patients with hepatocellular carcinoma. World J Gastroenterol 20(41):15028–15036. doi:10.3748/wjg.v20.i41.15028

    Article  PubMed  PubMed Central  Google Scholar 

  38. Harimoto N, Shirabe K, Yamashita YI, Ikegami T, Yoshizumi T, Soejima Y, Ikeda T, Maehara Y, Nishie A, Yamanaka T (2013) Sarcopenia as a predictor of prognosis in patients following hepatectomy for hepatocellular carcinoma. Br J Surg 100(11):1523–1530. doi:10.1002/bjs.9258

    Article  CAS  PubMed  Google Scholar 

  39. Voron T, Tselikas L, Pietrasz D, Pigneur F, Laurent A, Compagnon P, Salloum C, Luciani A, Azoulay D (2015) Sarcopenia impacts on short- and long-term results of hepatectomy for hepatocellular carcinoma. Ann Surg 261(6):1173–1183. doi:10.1097/SLA.0000000000000743

    Article  PubMed  Google Scholar 

  40. Newgard CB, An J, Bain JR, Muehlbauer MJ, Stevens RD, Lien LF, Haqq AM, Shah SH, Arlotto M, Slentz CA, Rochon J, Gallup D, Ilkayeva O, Wenner BR, Yancy WS Jr, Eisenson H, Musante G, Surwit RS, Millington DS, Butler MD, Svetkey LP (2009) A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab 9(4):311–326. doi:10.1016/j.cmet.2009.02.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Rauschert S, Uhl O, Koletzko B, Hellmuth C (2014) Metabolomic biomarkers for obesity in humans: a short review. Ann Nutr Metab 64(3–4):314–324. doi:10.1159/000365040

    Article  CAS  PubMed  Google Scholar 

  42. Marchesini G, Bianchi G, Merli M, Amodio P, Panella C, Loguercio C, Rossi Fanelli F, Abbiati R (2003) Nutritional supplementation with branched-chain amino acids in advanced cirrhosis: a double-blind, randomized trial. Gastroenterology 124(7):1792–1801

    Article  CAS  PubMed  Google Scholar 

  43. Muto Y, Sato S, Watanabe A, Moriwaki H, Suzuki K, Kato A, Kato M, Nakamura T, Higuchi K, Nishiguchi S, Kumada H (2005) Effects of oral branched-chain amino acid granules on event-free survival in patients with liver cirrhosis. Clin Gastroenterol Hepatol 3(7):705–713

    Article  CAS  PubMed  Google Scholar 

  44. Plauth M, Cabre E, Riggio O, Assis-Camilo M, Pirlich M, Kondrup J, Ferenci P, Holm E, Vom Dahl S, Muller MJ, Nolte W (2006) ESPEN guidelines on enteral nutrition: liver disease. Clin Nutr 25(2):285–294. doi:10.1016/j.clnu.2006.01.018

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank Dr. M Hattori (Hiroshima University, Japan) for his assistance with the statistical analysis.

Author information

Authors and Affiliations

  1. Department of Gastroenterological and Transplant Surgery, Hiroshima University Hospital, 1-2-3 Kasumi, Minami-Ku, Hiroshima, 734-8557, Japan

    Masakazu Hashimoto, Tsuyoshi Kobayashi, Shintaro Kuroda, Michinori Hamaoka & Hideki Ohdan

  2. Department of Surgery, Kure Medical Center, National Hospital Organization, 3-1 Aoyama, Kure City, Hiroshima, 737-0023, Japan

    Hirotaka Tashiro

Authors
  1. Masakazu Hashimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hirotaka Tashiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tsuyoshi Kobayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shintaro Kuroda
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michinori Hamaoka
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hideki Ohdan
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Study conception and design: M Hashimoto, H Tashiro. Acquisition of date: M Hashimoto, M Hamaoka, H Iwako. Analysis and interpretation of date: M Hashimoto, T Kobayashi, S Kuroda. Drafting of manuscript: M Hashimoto, H Tashiro. Critical revision of manuscript: H Tashiro, H Ohdan.

Corresponding author

Correspondence to Hirotaka Tashiro.

Ethics declarations

This study was approved by the local institutional review board after informed consent was obtained from all patients.

Funding

No funding was received for research or publication.

Conflicts of interest

The authors declare that they have no conflict of interest.

Ethical approval

For this type of study, formal consent is not required.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Electronic supplementary material

Supplementary Table 1

(DOCX 25 kb)

Supplementary Figure 1

Prognosis of the patients in the hepatitis B virus–related hepatocellular cancer (HBV-HCC) and hepatitis C virus–related HCC (HCV-HCC) who underwent liver resection. Kaplan–-Meier curves of the overall survival (OS) rates after hepatectomy. OS rates of the HBV-HCC group at 3 and 5 years (87.7% and 76.4%, respectively) were significantly higher than those of the HCV-HCC group at 3 and 5 years (81.3% and 63.3%, respectively) (p = 0.003). (GIF 38 kb)

High Resolution (TIFF 1185 kb)

Supplementary Figure 2

To overcome bias due to different distributions of covariates for the HBV-HCC group and HCV-HCC group, a one-to-one match was created using propensity score analysis (age, gender, diabetes mellitus, ICG-R, AFP, DCP, background liver, type of hepatectomy, tumor size, number of tumors, vascular invasion, tumor differentiation). After matching, patient outcomes were analyzed. Kaplan-Meier curves of the overall survival (OS) rates after hepatectomy, and OS rates of the HBV-HCC group at 3 and 5 years (89.2% and 76.8%, respectively) were significantly higher than those of the HCV-HCC group at 3 and 5 years (84.0% and 70.1%, respectively) (p = 0.228). (GIF 40 kb)

High Resolution (TIFF 1796 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hashimoto, M., Tashiro, H., Kobayashi, T. et al. Influence of higher BMI for hepatitis B- and C-related hepatocellular carcinomas. Langenbecks Arch Surg 402, 745–755 (2017). https://doi.org/10.1007/s00423-017-1589-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00423-017-1589-2

Keywords

Search

Navigation