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Significance of Frailty in Prognosis After Hepatectomy for Elderly Patients with Hepatocellular Carcinoma

  • Hepatobiliary Tumors
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Background

The concept of frailty becomes important for patients who undergo surgery in this recent aging society. The aim of this study is to investigate the frailty as a prognostic factor in elderly patients with hepatocellular carcinoma (HCC) who underwent hepatectomy.

Patients and Methods

A total of 92 patients over 75 years old who underwent hepatectomy were enrolled in this study. Frailty was defined as clinical frailty scale (CFS) ≥ 4. Patients were divided into two groups, i.e., frailty group (n = 21) and no-frailty group (n = 71), and clinicopathological features were compared between them.

Results

The frailty group showed significant higher PIVKA-II level and larger tumor diameter (p < 0.05). CRP level and modified Glasgow prognostic score were significantly higher in the frailty group (p < 0.05). The frailty group showed higher rate of postoperative complications of Clavien–Dindo III (p = 0.06) and longer postoperative stay (p = 0.08). Cancer-specific, overall, and disease-free survival rates were significantly worse in the frailty group (p < 0.05). Frailty was detected as an independent prognostic factor on multivariate analysis of cancer-specific survival.

Conclusion

Frailty can estimate the prognosis of HCC patients who underwent hepatectomy.

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References

  1. Kaibori M, Matsui K, Ishizaki M, et al. Hepatic resection in the elderly. J Surg Oncol. 2009;99:154–160.

    Article  Google Scholar 

  2. Yamada S, Shimada M, Miyake H, Utsunomiya T, Morine Y, Imura S, Ikemoto T, Mori H, Hanaoka J, Iwahashi S, Saito Y. Outcome of hepatectomy in super-elderly patients with hepatocellular carcinoma. Hepatol Res. 2012;42:454–8.

    Article  CAS  Google Scholar 

  3. Hogan DB, MacKnight C, Bergman H, et al. Models, definitions, and criteria of frailty. Aging Clin Exp Res. 2003;15(3 Suppl):1–29.

    PubMed  Google Scholar 

  4. Rockwood K, Song X, MacKnight C, et al. A global clinical measure of fitness and frailty in elderly people. CMAJ (Can Med Assoc J). 2005;173:489–95.

    Article  Google Scholar 

  5. Rolfson DB, Majumdar SR, Tsuyuki RT, et al. Validity and reliability of the edmonton frail scale. Age Ageing. 2006;35:526–9.

    Article  Google Scholar 

  6. Makary MA, Segev DL, Pronovost PJ, et al. Frailty as a predictor of surgical outcomes in older patients. J Am Coll Surg. 2010;210:901–8.

    Article  Google Scholar 

  7. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56:146–56.

    Article  Google Scholar 

  8. Ensrud KE, Ewing SK, Taylor BC, Fink HA, Cawthon PM, Stone KL, et al. Comparison of 2 frailty indexes for prediction of falls, disability, fractures, and death in older women. Arch Intern Med. 2008;168:382–9.

    Article  Google Scholar 

  9. Morley JE, Malmstrom TK, Miller DK. A simple frailty questionnaire (FRAIL) predicts outcomes in middle aged African Americans. J Nutr Health Aging. 2012;16:601–8.

    Article  CAS  Google Scholar 

  10. Chow WB, Rosenthal R, Merkow RP, et al. Optimal preoperative assessment of the geriatric surgical patient: a best practices guideline from the American College of Surgeons National Surgical Quality Improvement Program and the American Geriatrics Society. J Am Coll Surg. 2012;215:453–66.

    Article  Google Scholar 

  11. McIsaac DI, Taljaard M, Bryson GL, et al. Frailty as a predictor of death or new disability after surgery: a prospective cohort study. Ann Surg. 2018; https://doi.org/10.1097/sla.0000000000002967.

    Article  PubMed  Google Scholar 

  12. Rockwood K, Song X, MacKnight C, et al. A global clinical measure of fitness and frailty in elderly people. CMAJ. 2005;173:489–95.

    Article  Google Scholar 

  13. Minagawa M, Ikai I, Matsuyama Y, Yamaoka Y, Makuuchi M. 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. 2007;245:909–922.

    Article  Google Scholar 

  14. Kayadibi H, Sertoglu E, Uyanik M, Tapan S. Neutrophil-lymphocyte ratio is useful for the prognosis of patients with hepatocellular carcinoma. World J Gastroenterol. 2014;20:9631–2.

    Article  Google Scholar 

  15. Pinato DJ, North BV, Sharma R. A novel, externally validated inflammation-based prognostic algorithm in hepatocellular carcinoma: the prognostic nutritional index (PNI). Br J Cancer. 2012;106:1439–45.

    Article  CAS  Google Scholar 

  16. Onodera T, Goseki N, Kosaki G. Prognostic nutritional index in gastrointestinal surgery of malnourished cancer patients. Nihon Geka Gakkai Zasshi. 1984;85:1001–5.

    CAS  PubMed  Google Scholar 

  17. 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;240:205–13.

    Article  Google Scholar 

  18. Rockwood K, Mitnitski A, Song X, Steen B, Skoog I. Long-term risks of death and institutionalization of elderly people in relation to deficit accumulation at age 70. J Am Geriatr Soc. 2006;54:975–79.

    Article  Google Scholar 

  19. Clough-Gorr KM, Thwin SS, Stuck AE, Silliman RA. Examining five- and ten-year survival in older women with breast cancer using cancer-specific geriatric assessment. Eur J Cancer. 2012;48:805–12.

    Article  Google Scholar 

  20. Lu J, Cao LL, Zheng CH, et al. The preoperative frailty versus inflammation-based prognostic score: which is better as an objective predictor for gastric cancer patients 80 years and older? Ann Surg Oncol. 2017;24:754–62.

    Article  Google Scholar 

  21. Ngo-Huang A, Holmes HM, des Bordes JKA, Parker NH, Fogelman D, Petzel MQB, Song J, Bruera E, Katz MHG. Association between frailty syndrome and survival in patients with pancreatic adenocarcinoma. Cancer Med. 2019;8:2867–76.

    Article  Google Scholar 

  22. Harneshaug M, Kirkhus L, Benth JŠ, Grønberg BH, Bergh S, Whist JE, Rostoft S, Jordhøy MS. Screening for frailty among older patients with cancer using blood biomarkers of inflammation. J Geriatr Oncol. 2019;10:272–78.

    Article  Google Scholar 

  23. Lealdini V, Trufelli DC, da Silva FB, Normando SR, Camargo EW, Matos LL, Fonseca FL, Santi PX, Del Giglio A. Applicability of modified Glasgow Prognostic Score in the assessment of elderly patients with cancer: a pilot study. J Geriatr Oncol. 2015;6:479–83.

    Article  Google Scholar 

  24. Nozoe T, Matsumata T, Sugimachi K. Preoperative elevation of serum C-reactive protein is related to impaired immunity in patients with colorectal cancer. Am J Clin Oncol. 2000;23:263–6.

    Article  CAS  Google Scholar 

  25. Leitch EF, Chakrabarti M, Crozier JE, McKee RF, Anderson JH, Horgan PG, et al. Comparison of the prognostic value of selected markers of the systemic inflammatory response in patients with colorectal cancer. Br J Cancer. 2007;97:1266–70.

    Article  CAS  Google Scholar 

  26. Canna K, McArdle PA, McMillan DC, McNicol AM, Smith GW, McKee RF, et al. The relationship between tumour T-lymphocyte infiltration, the systemic inflammatory response and survival in patients undergoing curative resection for colorectal cancer. Br J Cancer. 2005;92:651–4.

    Article  CAS  Google Scholar 

  27. Du Clos TW, Mold C. C-reactive protein: an activator of innate immunity and a modulator of adaptive immunity. Immunol Res. 2004;30:261–77.

    Article  Google Scholar 

  28. Ytting H, Christensen IJ, Basse L, Lykke J, Thiel S, Jensenius JC, et al. Influence of major surgery on the mannan-binding lectin pathway of innate immunity. Clin Exp Immunol. 2006;144:239–46.

    Article  CAS  Google Scholar 

  29. McMillan DC, Scott HR, Watson WS, Preston T, Milroy R, McArdle CS. Longitudinal study of body cell mass depletion and the inflammatory response in cancer patients. Nutr Cancer. 1998;31:101–5.

    Article  CAS  Google Scholar 

  30. McMillan DC, Watson WS, O’Gorman P, Preston T, Scott HR, McArdle CS. Albumin concentrations are primarily determined by the body cell mass and the systemic inflammatory response in cancer patients with weight loss. Nutr Cancer. 2001;39: 210–3.

    Article  CAS  Google Scholar 

  31. Lu Y, Tan CT, Nyunt MS, Mok EW, Camous X, Kared H, Fulop T, Feng L, Ng TP, Larbi A. Inflammatory and immune markers associated with physical frailty syndrome: findings from Singapore longitudinal aging studies. Oncotarget. 2016 17;7:28783–95.

    Article  Google Scholar 

  32. Sabel MS, Lee J, Cai M, Englesbe MJ, Holcombe S, Wang S. Sarcopenia as a prognostic factor among patients with stage III melanoma. Ann Surg Oncol. 2011;18:3579–85.

    Article  Google Scholar 

  33. Sparchez Z, Mocan T, Radu P, Mocan LP, Sparchez M, Leucuta DC, et al. Prognostic factors after percutaneous radiofrequency ablation in the treatment of hepatocellular carcinoma: impact of incomplete ablation on recurrence and overall survival rates. J Gastrointestin Liver Dis. 2018;27:399–407.

    Article  Google Scholar 

  34. Huisingh-Scheetz M, Walston J. How should older adults with cancer be evaluated for frailty? J Geriatr Oncol. 2017;8:8–15.

    Article  Google Scholar 

  35. Beggs T, Sepehri A, Szwajcer A, Tangri N, Arora RC. Frailty and perioperative outcomes: a narrative review. Can J Anaesth. 2015;62:143-57.

    Article  Google Scholar 

  36. Tanaka S, Ueno M, Iida H, Kaibori M, Nomi T, Hirokawa F, Ikoma H, Nakai T, Eguchi H, Kubo S. Preoperative assessment of frailty predicts age-related events after hepatic resection: a prospective multicenter study. J Hepatobiliary Pancreat Sci. 2018;25:377–387.

    Article  Google Scholar 

  37. Gani F, Cerullo M, Amini N, Buettner S, Margonis GA, Sasaki K, Kim Y, Pawlik TM. Frailty as a risk predictor of morbidity and mortality following liver surgery. J Gastrointest Surg. 2017;21:822–830.

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Surgery, Tokushima University, Tokushima City, Tokushima, Japan

    Shinichiro Yamada MD, PhD, FACS, Mitsuo Shimada MD, PhD, FACS, Yuji Morine MD, PhD, FACS, Satoru Imura MD, PhD, FACS, Tetsuya Ikemoto MD, PhD, FACS, Yusuke Arakawa MD, PhD, FACS, Yu Saito MD, PhD, FACS, Masato Yoshikawa MD, PhD & Katsuki Miyazaki MD

Authors
  1. Shinichiro Yamada MD, PhD, FACS
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  2. Mitsuo Shimada MD, PhD, FACS
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  3. Yuji Morine MD, PhD, FACS
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  4. Satoru Imura MD, PhD, FACS
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  5. Tetsuya Ikemoto MD, PhD, FACS
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  6. Yusuke Arakawa MD, PhD, FACS
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  7. Yu Saito MD, PhD, FACS
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  8. Masato Yoshikawa MD, PhD
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  9. Katsuki Miyazaki MD
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Correspondence to Shinichiro Yamada MD, PhD, FACS.

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Yamada, S., Shimada, M., Morine, Y. et al. Significance of Frailty in Prognosis After Hepatectomy for Elderly Patients with Hepatocellular Carcinoma. Ann Surg Oncol 28, 439–446 (2021). https://doi.org/10.1245/s10434-020-08742-w

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  • DOI: https://doi.org/10.1245/s10434-020-08742-w

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