Skip to main content

Advertisement

SpringerLink
Log in

Laparoscopic and open liver resection for hepatocellular carcinoma with type 2 diabetes mellitus: multicenter propensity score-matched study

  • Original Article
  • Published:
Hepatology International Aims and scope Submit manuscript

Abstract

Purpose

This study aimed at analyzing and comparing the perioperative results and long-term oncological outcomes of hepatocellular carcinoma (HCC) patients with type 2 diabetes mellitus (T2DM) treated with laparoscopic (LLR) versus open liver resection (OLR).

Methods

Clinicopathological data of HCC patients with T2DM who underwent LLR or OLR as initial treatment from four medical centers were retrospectively reviewed. The survival outcomes of patients who underwent laparoscopic liver resection (LLR) were compared with those of patients who underwent open liver resection (OLR). Using the Kaplan–Meier method, survival curves for the two groups of patients were generated, and the log-rank test was used to compare survival differences. Propensity score matching (PSM) analysis was used to match patients of the LLR and OLR groups in a 1:1 ratio.

Results

230 HCC patients with T2DM were enrolled, including 101 patients in the LLR group and 129 patients in the OLR group. After PSM, 90 patients were matched in each of the study group. Compared with the OLR group, the LLR group had less blood loss, a shorter hospitalization and fewer postoperative complications. The LLR group had a significantly better overall survival (OS) and recurrence-free survival (RFS) than the OLR group before and after PSM. Subgroup analysis demonstrated that HCC patients with T2DM had survival benefits from LLR regardless of the course of T2DM.

Conclusions

Laparoscopic liver resection for HCC patients with T2DM can be safely performed with favorable perioperative and long-term oncological outcomes at high-volume liver cancer centers, regardless of the course of T2DM.

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
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Parkin DM, Bray F, Ferlay J, Pisani P. Estimating the world cancer burden: Globocan 2000. Int J Cancer. 2001;94(2):153–156

    Article  CAS  PubMed  Google Scholar 

  2. El-Serag HB, Rudolph KL. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology. 2007;132(7):2557–2576

    Article  CAS  PubMed  Google Scholar 

  3. Han HS, Shehta A, Ahn S, Yoon YS, Cho JY, Choi Y. Laparoscopic versus open liver resection for hepatocellular carcinoma: case-matched study with propensity score matching. J Hepatol. 2015;63(3):643–650

    Article  PubMed  Google Scholar 

  4. Coelho FF, Kruger JA, Fonseca GM, Araújo RL, Jeismann VB, Perini MV, et al. Laparoscopic liver resection: experience based guidelines. World J Gastrointest Surg. 2016;8(1):5–26

    Article  PubMed Central  PubMed  Google Scholar 

  5. Vogel A, Cervantes A, Chau I, Daniele B, Llovet JM, Meyer T, et al. Hepatocellular carcinoma: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2019;30(5):871–873

    Article  CAS  PubMed  Google Scholar 

  6. Reich H, McGlynn F, DeCaprio J, Budin R. Laparoscopic excision of benign liver lesions. Obstet Gynecol. 1991;78(5 Pt 2):956–958

    CAS  PubMed  Google Scholar 

  7. Yoshida H, Taniai N, Yoshioka M, Hirakata A, Kawano Y, Shimizu T, et al. Current status of laparoscopic hepatectomy. J Nippon Med School = Nippon Ika Daigaku zasshi. 2019;86(4):201–206

    Article  PubMed  Google Scholar 

  8. Topal B, Fieuws S, Aerts R, Vandeweyer H, Penninckx F. Laparoscopic versus open liver resection of hepatic neoplasms: comparative analysis of short-term results. Surg Endosc. 2008;22(10):2208–2213

    Article  CAS  PubMed  Google Scholar 

  9. Belli G, Limongelli P, Fantini C, D’Agostino A, Cioffi L, Belli A, et al. Laparoscopic and open treatment of hepatocellular carcinoma in patients with cirrhosis. Br J Surg. 2009;96(9):1041–1048

    Article  CAS  PubMed  Google Scholar 

  10. Castaing D, Vibert E, Ricca L, Azoulay D, Adam R, Gayet B. Oncologic results of laparoscopic versus open hepatectomy for colorectal liver metastases in two specialized centers. Ann Surg. 2009;250(5):849–855

    Article  PubMed  Google Scholar 

  11. Nguyen KT, Gamblin TC, Geller DA. World review of laparoscopic liver resection-2804 patients. Ann Surg. 2009;250(5):831–841

    Article  PubMed  Google Scholar 

  12. Croome KP, Yamashita MH. Laparoscopic vs open hepatic resection for benign and malignant tumors: an updated meta-analysis. Arch surg. 2010;145(11):1109–1118

    Article  PubMed  Google Scholar 

  13. Buell JF, Cherqui D, Geller DA, O’Rourke N, Iannitti D, Dagher I, et al. The international position on laparoscopic liver surgery: the Louisville statement, 2008. Ann Surg. 2009;250(5):825–830

    Article  PubMed  Google Scholar 

  14. Wakabayashi G, Cherqui D, Geller DA, Buell JF, Kaneko H, Han HS, et al. Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg. 2015;261(4):619–629

    PubMed  Google Scholar 

  15. Yin Z, Fan X, Ye H, Yin D, Wang J. Short- and long-term outcomes after laparoscopic and open hepatectomy for hepatocellular carcinoma: a global systematic review and meta-analysis. Ann Surg Oncol. 2013;20(4):1203–1215

    Article  PubMed  Google Scholar 

  16. Goh EL, Chidambaram S, Ma S. Laparoscopic vs open hepatectomy for hepatocellular carcinoma in patients with cirrhosis: a meta-analysis of the long-term survival outcomes. Int J Surg (London, England). 2018;50:35–42

    Article  Google Scholar 

  17. Jiang S, Wang Z, Ou M, Pang Q, Fan D, Cui P. Laparoscopic versus open hepatectomy in short- and long-term outcomes of the hepatocellular carcinoma patients with cirrhosis: a systematic review and meta-analysis. J Laparoendosc Adv Surg Tech A. 2019;29(5):643–654

    Article  PubMed  Google Scholar 

  18. Xiangfei M, Yinzhe X, Yingwei P, Shichun L, Weidong D. Open versus laparoscopic hepatic resection for hepatocellular carcinoma: a systematic review and meta-analysis. Surg Endosc. 2019;33(8):2396–2418

    Article  PubMed  Google Scholar 

  19. DeFronzo RA, Ferrannini E, Groop L, Henry RR, Herman WH, Holst JJ, et al. Type 2 diabetes mellitus. Nat Rev Dis Primers. 2015;23(1):15019

    Article  Google Scholar 

  20. Schlesinger S, Aleksandrova K, Pischon T, Jenab M, Fedirko V, Trepo E, et al. Diabetes mellitus, insulin treatment, diabetes duration, and risk of biliary tract cancer and hepatocellular carcinoma in a European cohort. Ann Oncol. 2013;24(9):2449–2455

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Yang WS, Shu XO, Gao J, Li HL, Cai H, Yang G, et al. Prospective evaluation of type 2 diabetes mellitus on the risk of primary liver cancer in Chinese men and women. Ann Oncol. 2013;24(6):1679–1685

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Kawamura Y, Ikeda K, Arase Y, Yatsuji H, Sezaki H, Hosaka T, et al. Diabetes mellitus worsens the recurrence rate after potentially curative therapy in patients with hepatocellular carcinoma associated with nonviral hepatitis. J Gastroenterol Hepatol. 2008;23(11):1739–1746

    Article  PubMed  Google Scholar 

  23. Wang WM, Xu Y, Yang XR, Wang YH, Sun HX, Fan J. Prognostic role of diabetes mellitus in hepatocellular carcinoma patients after curative treatments: a meta-analysis. Hepatobiliary Pancreat Dis Int. 2011;10(4):346–355

    Article  PubMed  Google Scholar 

  24. Martin ET, Kaye KS, Knott C, Nguyen H, Santarossa M, Evans R, et al. Diabetes and risk of surgical site infection: a systematic review and meta-analysis. Infect Control Hosp Epidemiol. 2016;37(1):88–99

    Article  PubMed  Google Scholar 

  25. Luo J, Xu L, Li L, Zhang J, Zhang M, Xu M. Diabetes mellitus and postoperative blood glucose value help predict posthepatectomy liver failure in patients with hepatocellular carcinoma. J Gastrointest Oncol. 2021;12(5):2377–2387

    Article  PubMed Central  PubMed  Google Scholar 

  26. Shen GL, Lu Y, Liang L, Lu WF, Diao YK, Xiao ZQ, et al. Impact of diabetes mellitus on the long-term prognosis of patients with hepatocellular carcinoma after hepatectomy. Expert Rev Gastroenterol Hepatol. 2022;15:1–6

    Google Scholar 

  27. Marrero JA, Kulik LM, Sirlin CB, Zhu AX, Finn RS, Abecassis MM, et al. Diagnosis, staging, and management of hepatocellular carcinoma: 2018 practice guidance by the American association for the study of liver diseases. Hepatology (Baltimore, MD). 2018;68(2):723–750

    Article  PubMed  Google Scholar 

  28. Reig M, Forner A, Rimola J, Ferrer-Fàbrega J, Burrel M, Garcia-Criado Á, et al. BCLC strategy for prognosis prediction and treatment recommendation: the 2022 update. J Hepatol. 2022;76(3):681–693

    Article  PubMed  Google Scholar 

  29. Roayaie S, Blume IN, Thung SN, Guido M, Fiel MI, Hiotis S, et al. A system of classifying microvascular invasion to predict outcome after resection in patients with hepatocellular carcinoma. Gastroenterology. 2009;137(3):850–855

    Article  PubMed  Google Scholar 

  30. Lim KC, Chow PK, Allen JC, Chia GS, Lim M, Cheow PC, et al. Microvascular invasion is a better predictor of tumor recurrence and overall survival following surgical resection for hepatocellular carcinoma compared to the Milan criteria. Ann Surg. 2011;254(1):108–113

    Article  PubMed  Google Scholar 

  31. Classification and Diagnosis of Diabetes. Standards of medical care in diabetes-2022. Diabetes Care. 2022;45(Suppl 1):S17-s38

    Google Scholar 

  32. Yoshida N, Takayama T, Midorikawa Y, Higaki T, Nakayama H, Moriguchi M, et al. Surgical outcomes in patients with hepatocellular carcinoma associated with metabolic syndrome. World J Surg. 2015;39(2):471–477

    Article  PubMed  Google Scholar 

  33. Liu YW, Yen YH, Li WF, Wang CC, Lu SN, Kee KM, et al. Minimally invasive surgery versus percutaneous radiofrequency ablation for early-stage hepatocellular carcinoma: results from a high-volume liver surgery center in East Asia. Surg Oncol. 2022;19(42): 101769

    Article  Google Scholar 

  34. Aoki T, Kubota K, Hasegawa K, Kubo S, Izumi N, Kokudo N, et al. Significance of the surgical hepatic resection margin in patients with a single hepatocellular carcinoma. Br J Surg. 2020;107(1):113–120

    Article  CAS  PubMed  Google Scholar 

  35. Nitta H, Allard MA, Sebagh M, Golse N, Ciacio O, Pittau G, et al. Ideal surgical margin to prevent early recurrence after hepatic resection for hepatocellular carcinoma. World J Surg. 2021;45(4):1159–1167

    Article  PubMed  Google Scholar 

  36. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240(2):205–213

    Article  PubMed Central  PubMed  Google Scholar 

  37. EASL Clinical Practice Guidelines. Management of hepatocellular carcinoma. J Hepatol. 2018;69(1):182–236

    Article  Google Scholar 

  38. Vogel A, Cervantes A, Chau I, Daniele B, Llovet JM, Meyer T, et al. Hepatocellular carcinoma: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2018;29(Suppl 4):iv238–iv255

    Article  CAS  PubMed  Google Scholar 

  39. Li T, Fan J, Qin LX, Zhou J, Sun HC, Qiu SJ, et al. Risk factors, prognosis, and management of early and late intrahepatic recurrence after resection of primary clear cell carcinoma of the liver. Ann Surg Oncol. 2011;18(7):1955–1963

    Article  CAS  PubMed  Google Scholar 

  40. Kabir T, Tan ZZ, Syn NL, Wu E, Lin JD, Zhao JJ, et al. Laparoscopic versus open resection of hepatocellular carcinoma in patients with cirrhosis: meta-analysis. Br J Surg. 2021;109(1):21–29

    Article  PubMed  Google Scholar 

  41. Abu Hilal M, Aldrighetti L, Dagher I, Edwin B, Troisi RI, Alikhanov R, et al. The southampton consensus guidelines for laparoscopic liver surgery: from indication to implementation. Ann Surg. 2018;268(1):11–18

    Article  PubMed  Google Scholar 

  42. Cheung TT, Han HS, She WH, Chen KH, Chow PKH, Yoong BK, et al. The Asia Pacific consensus statement on laparoscopic liver resection for hepatocellular carcinoma: a report from the 7th Asia-Pacific primary liver cancer expert meeting held in Hong Kong. Liver cancer. 2018;7(1):28–39

    Article  PubMed  Google Scholar 

  43. Coletta D, De Padua C, Parrino C, De Peppo V, Oddi A, Frigieri C, et al. Laparoscopic liver surgery: what are the advantages in patients with cirrhosis and portal hypertension? Systematic review and meta-analysis with personal experience. J Laparoendosc Adv Surg Tech A. 2020;30(10):1054–1065

    Article  PubMed  Google Scholar 

  44. Pennel L, Quesada JL, Dematteis M. Neuroticism and anxious attachment as potential vulnerability factors of repeat suicide attempts. Psychiatry Res. 2018;264:46–53

    Article  PubMed  Google Scholar 

  45. Yang SY, Yan ML, Duan YF, Feng JK, Ye JZ, Xiang YJ, et al. Perioperative and long-term survival outcomes of laparoscopic versus laparotomic hepatectomy for BCLC stages 0-A hepatocellular carcinoma patients associated with or without microvascular invasion: a multicenter, propensity score matching analysis. Hep Intl. 2022;16(4):892–905

    Article  Google Scholar 

Download references

Funding

Meng Chao Talent Training Program (EHBH2019YC112); the Clinical Research Plan of Shanghai Hospital Development Center (SHDC2020CR1004A); the State Key Program of National Natural Science Foundation of China (81730097); National Natural Science Foundation of China (82172846; 82072618).

Author information

Author notes

  1. Shi-Ye Yang, Jin-Kai Feng, Mao-Lin Yan and Lei Guo have contributed equally to this work.

Authors and Affiliations

  1. Department of Hepatic Surgery VI, Eastern Hepatobiliary Surgery Hospital, Second Military Medical University, 225 Changhai Road, Shanghai, 200433, China

    Shi-Ye Yang, Jin-Kai Feng, Lei Guo, Zong-Han Liu, Yan-Jun Xiang, Jie Xue, Jie Shi, Shu-Qun Cheng & Wei-Xing Guo

  2. Department of Hepatobiliary and Pancreatic Surgery, Fujian Provincial Hospital, The Shengli Clinical Medical College of Fujian Medical University, Fuzhou, China

    Mao-Lin Yan

  3. Department of Hepatobiliary and Pancreatic Surgery, The Third Affiliated Hospital of Soochow University (Changzhou People’s Hospital), Jiangsu, China

    Yun-Fei Duan

  4. Department of Hepatobiliary Pancreatic Surgery, Affiliated Tumor Hospital of Guangxi Medical University, Guangxi, China

    Jia-Zhou Ye

  5. School of Health Science and Engineering, University of Shanghai for Science and Technology, Shanghai, China

    Li Xu

  6. Faculty of Medicine, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong SAR, China

    Wan Yee Lau

Authors
  1. Shi-Ye Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jin-Kai Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mao-Lin Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lei Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yun-Fei Duan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jia-Zhou Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zong-Han Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yan-Jun Xiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Li Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jie Xue
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Jie Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Wan Yee Lau
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Shu-Qun Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Wei-Xing Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Shu-Qun Cheng or Wei-Xing Guo.

Ethics declarations

Ethics approval

The study was approved by the Clinical Research Ethics Committees of each center and was in line with the 2013 Helsinki Declaration.

Informed consent

Written informed consent was obtained from all patients prior to enrollment for this study.

Conflict of interest

Shi-Ye Yang, Jin-Kai Feng, Mao-Lin Yan, Lei Guo, Yun-Fei Duan, Jia-Zhou Ye, Zong-Han Liu, Yan-Jun Xiang, Li Xu, Jie Xue, Jie Shi, Wan Yee Lau, Shu-Qun Cheng, Wei-Xing Guo who participate in this study have no conflicts of interest to declare.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

12072_2023_10492_MOESM1_ESM.tif

Supplementary file1 Overall survival (OS) and recurrence-free survival (RFS) of non-cirrhotic HCC patients with T2DM treated with LLR or OLR before and after PSM. OS (A) and RFS (B) of non-cirrhotic HCC patients with T2DM before PSM. OS (C) and RFS (D) of non-cirrhotic HCC patients with T2DM after PSM. Abbreviations: HCC, hepatocellular carcinoma; LLR, laparoscopic liver resection; OLR, open liver resection; PSM, propensity score matching (TIF 1703 KB)

12072_2023_10492_MOESM2_ESM.tif

Supplementary file2 Overall survival (OS) and recurrence-free survival (RFS) of cirrhotic HCC patients with T2DM treated with LLR or OLR before and after PSM. OS (A) and RFS (B) of cirrhotic HCC patients with T2DM before PSM. OS (C) and RFS (D) of cirrhotic HCC patients with T2DM after PSM. Abbreviations: HCC, hepatocellular carcinoma; LLR, laparoscopic liver resection; OLR, open liver resection; PSM, propensity score matching (TIF 1682 KB)

Supplementary file3 (DOCX 15 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, SY., Feng, JK., Yan, ML. et al. Laparoscopic and open liver resection for hepatocellular carcinoma with type 2 diabetes mellitus: multicenter propensity score-matched study. Hepatol Int 17, 1251–1264 (2023). https://doi.org/10.1007/s12072-023-10492-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12072-023-10492-2

Keywords

Search

Navigation