Impact of malnutrition on short- and long-term outcomes following laparoscopic liver resection for hepatocellular carcinoma

Kentaro Oji , Takeshi Urade , Satoshi Omiya , Masahiro Kido , Shohei Komatsu , Kenji Fukushima , Shinichi So , Toshihiko Yoshida , Kentaro Tai , Keisuke Arai , Kosuke Iguchi , Dongha Lee , Masayuki Akita , Takuya Mizumoto , Jun Ishida , Yoshihide Nanno , Sadaki Asari , Hiroaki Yanagimoto , Takumi Fukumoto

Mini-invasive Surgery ›› 2025, Vol. 9 ›› Issue (1) : 35

PDF
Mini-invasive Surgery ›› 2025, Vol. 9 ›› Issue (1) :35 DOI: 10.20517/2574-1225.2025.91
Original Article

Impact of malnutrition on short- and long-term outcomes following laparoscopic liver resection for hepatocellular carcinoma

Author information +
History +
PDF

Abstract

Aim: Laparoscopic liver resection (LLR) is increasingly used in the management of hepatocellular carcinoma (HCC), even among patients traditionally considered high risk due to advanced age or poor nutritional status. Malnutrition, assessed by the prognostic nutritional index (PNI), is known to negatively affect surgical outcomes; however, its impact in the context of LLR remains unclear. We aimed to clarify the effect of malnutrition, defined by the PNI, on short- and long-term outcomes following laparoscopic liver resection for HCC.

Methods: We retrospectively analyzed 121 patients with HCC who underwent primary LLR between 2011 and 2019. Nutritional status was evaluated using the PNI, with a cutoff of < 40 indicating malnutrition. Short-term outcomes were assessed using the textbook outcome (TO), defined as meeting five criteria: no 30-day mortality, R0 resection, no major complications (Clavien–Dindo ≥ III), no unplanned readmission, and no prolonged hospitalization. Long-term outcomes included overall survival (OS) and recurrence-free survival (RFS).

Results: Seventeen patients (14%) were classified as malnourished. TO achievement rates were similar between the malnutrition and normal-nutrition groups (70.6% vs. 74.0%, P = 0.771). No significant differences were observed in individual TO criteria. However, OS was significantly worse in the malnutrition group (median 40 vs. 107 months, P < 0.001), while RFS showed a non-significant trend (P = 0.085). In multivariate analysis, PNI-defined malnutrition was the only independent predictor of poorer OS.

Conclusion: LLR yields acceptable short-term outcomes even in malnourished patients with HCC, as defined by the PNI. However, malnutrition remains a strong independent risk factor for decreased long-term survival. These findings underscore the importance of preoperative nutritional assessment and optimization in surgical candidates with HCC.

Keywords

Hepatocellular carcinoma / laparoscopic liver resection / malnutrition / prognostic nutritional index / textbook outcome / survival analysis

Cite this article

Download citation ▾
Kentaro Oji, Takeshi Urade, Satoshi Omiya, Masahiro Kido, Shohei Komatsu, Kenji Fukushima, Shinichi So, Toshihiko Yoshida, Kentaro Tai, Keisuke Arai, Kosuke Iguchi, Dongha Lee, Masayuki Akita, Takuya Mizumoto, Jun Ishida, Yoshihide Nanno, Sadaki Asari, Hiroaki Yanagimoto, Takumi Fukumoto. Impact of malnutrition on short- and long-term outcomes following laparoscopic liver resection for hepatocellular carcinoma. Mini-invasive Surgery, 2025, 9(1): 35 DOI:10.20517/2574-1225.2025.91

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Llovet JM,Villanueva A.Hepatocellular carcinoma.Nat Rev Dis Primers2021;7:6

[2]

Sung H,Siegel RL.Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.CA Cancer J Clin2021;71:209-49

[3]

Tsilimigras DI,Sahara K.Prognosis After Resection of Barcelona Clinic Liver Cancer (BCLC) Stage 0, A, and B hepatocellular carcinoma: a comprehensive assessment of the current BCLC classification.Ann Surg Oncol2019;26:3693-700

[4]

Sorin Y,Kawamura Y.Effectiveness of particle radiotherapy in various stages of hepatocellular carcinoma: a pilot study.Liver Cancer2018;7:323-34 PMCID:PMC6249594

[5]

Qin S, Chen M, Cheng AL, et al.; IMbrave050 investigators. Atezolizumab plus bevacizumab versus active surveillance in patients with resected or ablated high-risk hepatocellular carcinoma (IMbrave050): a randomised, open-label, multicentre, phase 3 trial. Lancet. 2023;402:1835-47.

[6]

Tsai KY,Wang WY.Long-term and short-term surgical outcomes of laparoscopic versus open liver resection for hepatocellular carcinoma: might laparoscopic approach be better in early HCC?.Surg Endosc2019;33:1131-9

[7]

Takahara T,Beppu T.Long-term and perioperative outcomes of laparoscopic versus open liver resection for hepatocellular carcinoma with propensity score matching: a multi-institutional Japanese study.J Hepatobiliary Pancreat Sci2015;22:721-7

[8]

Famularo S,Giani A.The impact of age and ageing on hepatocarcinoma surgery: short- and long-term outcomes in a multicentre propensity-matched cohort.Liver Int2019;39:894-904

[9]

Omiya S,Komatsu S.Impact of GLIM criteria-based malnutrition diagnosis on outcomes following liver resection for hepatocellular carcinoma.HPB2023;25:1555-65

[10]

Oji K,Omiya S.Achieving textbook outcome in liver resection for hepatocellular carcinoma: malnutrition’s pivotal role.Langenbecks Arch Surg2025;410:139 PMCID:PMC12018603

[11]

Onodera T,Kosaki G.[Prognostic nutritional index in gastrointestinal surgery of malnourished cancer patients].Nihon Geka Gakkai Zasshi1984;85:1001-5

[12]

Tanemura A,Hayasaki A.Onodera’s prognostic nutritional index is a strong prognostic indicator for patients with hepatocellular carcinoma after initial hepatectomy, especially patients with preserved liver function.BMC Surg2020;20:261 PMCID:PMC7603728

[13]

Xishan Z,Feiyan M,Shikai W.The role of prognostic nutritional index for clinical outcomes of gastric cancer after total gastrectomy.Sci Rep2020;10:17373 PMCID:PMC7562903

[14]

von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP; STROBE Initiative. Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. BMJ. 2007;335:806-8. PMCID:PMC2034723

[15]

Kudo M,Sakurai T.General Rules for the Clinical and Pathological Study of Primary Liver Cancer, Nationwide Follow-Up Survey and Clinical Practice Guidelines: the outstanding achievements of the Liver Cancer Study Group of Japan.Dig Dis2015;33:765-70

[16]

Dindo D,Clavien PA.Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey.Ann Surg2004;240:205-13 PMCID:PMC1360123

[17]

Tsilimigras DI,Moris D.Assessing textbook outcomes following liver surgery for primary liver cancer over a 12-year time period at major hepatobiliary centers.Ann Surg Oncol2020;27:3318-27

[18]

Ruzzenente A,Conci S.Factors related to textbook outcome in laparoscopic liver resections: a single western centre analysis.J Gastrointest Surg2022;26:2301-10 PMCID:PMC9643260

[19]

Kokudo N.Evidence-based clinical practice guidelines for hepatocellular carcinoma in Japan: the J-HCC guidelines.J Gastroenterol2009;44 Suppl 19:119-21

[20]

Nomi T,Kaibori M.Laparoscopic versus open liver resection for hepatocellular carcinoma in elderly patients: a multi-centre propensity score-based analysis.Surg Endosc2020;34:658-66

[21]

Chen WZ,Zhang XZ.Comparison of laparoscopic and open radical gastrectomy for gastric cancer patients with GLIM-defined malnutrition.Eur J Surg Oncol2023;49:376-83

[22]

Wang JH,Hung CH,Lu SN.Survival comparison between surgical resection and radiofrequency ablation for patients in BCLC very early/early stage hepatocellular carcinoma.J Hepatol2012;56:412-8

[23]

Hatanaka T, Kakizaki S, Hiraoka A, et al.; Real-life Practice Experts for HCC (RELPEC) Study Group. Comparison of surgical resection and radiofrequency ablation for early-stage HCC patients with Child-Pugh Class B. J Gastroenterol Hepatol. 2025;40:2068-77.

[24]

Fu Y,Liu S.Comparison of resection, ablation, and stereotactic body radiation therapy in treating solitary hepatocellular carcinoma ≤ 5 cm: a retrospective, multicenter, cohort study.Int J Surg2025;111:1535-40 PMCID:PMC11745737

[25]

Neeman E.Surgery and stress promote cancer metastasis: new outlooks on perioperative mediating mechanisms and immune involvement.Brain Behav Immun2013;30 Suppl:S32-40 PMCID:PMC3423506

[26]

Donlon NE,Hayes C.The immune response to major gastrointestinal cancer surgery and potential implications for adjuvant immunotherapy.Crit Rev Oncol Hematol2022;175:103729

[27]

Kazi M,Sasi S.Prognostic nutritional index prior to rectal cancer resection predicts overall survival.Nutr Cancer2022;74:3228-35

[28]

Uri I,Tamás L,Dános K.Prognostic nutritional index (PNI) correlates with survival in head and neck cancer patients more precisely than other nutritional markers - real world data.Eur Arch Otorhinolaryngol2024;281:6599-611 PMCID:PMC11564356

[29]

Shoji F,Akamine T.The preoperative controlling nutritional status score predicts survival after curative surgery in patients with pathological stage I non-small cell lung cancer.Anticancer Res2017;37:741-7

[30]

Tsunematsu M,Fujiwara Y.Preoperative controlling nutritional status (CONUT) score predicts long-term outcomes in patients with non-B non-C hepatocellular carcinoma after curative hepatic resection.Langenbecks Arch Surg2021;406:99-107

[31]

Tsukagoshi M,Igarashi T.Lower geriatric nutritional risk index and prognostic nutritional index predict postoperative prognosis in patients with hepatocellular carcinoma.Nutrients2024;16:940 PMCID:PMC11013710

[32]

Zhao S,Yang Z.Comparison between Child-Pugh score and Albumin-Bilirubin grade in the prognosis of patients with HCC after liver resection using time-dependent ROC.Ann Transl Med2020;8:539 PMCID:PMC7214905

[33]

Giakoustidis A,Chatzikomnitsa P.The effects of sarcopenia on overall survival and postoperative complications of patients undergoing hepatic resection for primary or metastatic liver cancer: a systematic review and meta-analysis.J Clin Med2024;13:3869 PMCID:PMC11242440

[34]

Cederholm T, Jensen GL, Correia MITD, et al.; GLIM Core Leadership Committee, GLIM Working Group. GLIM criteria for the diagnosis of malnutrition - a consensus report from the global clinical nutrition community. Clin Nutr. 2019;38:1-9.

[35]

Ren L,Wang Z,Ahn S.Effectiveness of the CANCER-AIMS intervention on nutritional status and symptom management in patients with gastric cancer following gastrectomy: a randomized controlled trial.Int J Nurs Stud2024;159:104873

[36]

Weimann A, Braga M, Harsanyi L, et al.; DGEM (German Society for Nutritional Medicine), ESPEN (European Society for Parenteral and Enteral Nutrition). ESPEN Guidelines on Enteral Nutrition: Surgery including organ transplantation. Clin Nutr. 2006;25:224-44.

PDF

216

Accesses

0

Citation

Detail

Sections
Recommended

/