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Combination of Skeletal Muscle Mass and Density Predicts Postoperative Complications and Survival of Patients With Non-Small Cell Lung Cancer

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

Abstract

Background

Few studies have assessed the comprehensive skeletal muscle depletion associated with loss of muscle quantity (sarcopenia) and reduced muscle quality in cancer patients. This study aimed to clarify the impact of skeletal muscle depletion on outcomes after non-small cell lung cancer surgery.

Methods

Data for 341 patients with pathologic stages 1 to 3A non-small cell lung cancer who underwent lobectomy and mediastinal lymph node dissection from 2009 to 2013 were retrospectively reviewed. The integrative pectoralis muscle index (IPMI) was assessed by multiplying the normalized pectoralis muscle area (area/body mass index) and mean radiodensity on chest images. Postoperative outcomes were compared among sex-specific quartiles of IPMI. The trend of continuous and categorical variables was analyzed using the Jonckheere–Terpstra test and the Cochrane–Armitage test, respectively.

Results

Respiratory strength declined with decreasing quartiles of IPMI (P < 0.001). The risk of major complications escalated with the decrease of IPMI among four quartiles (7.1 %, 16.7 %, 18.4 %, and 22.4 %; P = 0.008). The hospital stay was prolonged for patients with reduced IPMI (P = 0.001). Patients in the lowest and highest quartiles had the worst and best 5-year overall survival, respectively, compared with those in the two intermediate quartiles of IPMI (67.0 %, 87.9 %, and 81.2 %, respectively; P=0.001). Multivariate analysis identified the lowest quartile of IPMI as an independent poor prognostic factor (hazard ratio, 1.88; 95 % confidence interval, 1.11–3.19; P = 0.020).

Conclusion

Comprehensive skeletal muscle profiling, including morphometric mass and componential density on chest imaging, has the potential to refine risk stratification and prognostication in non-small cell lung cancer.

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References

  1. Brown JC, Cespedes Feliciano EM, Caan BJ. The evolution of body composition in oncology-epidemiology, clinical trials, and the future of patient care: facts and numbers. J Cachexia Sarcopenia Muscle. 2018;9:1200–8.

    Article  Google Scholar 

  2. Ethun CG, Bilen MA, Jani AB, Maithel SK, Ogan K, Master VA. Frailty and cancer: implications for oncology surgery, medical oncology, and radiation oncology. CA Cancer J Clin. 2017;67:362–77.

    Article  Google Scholar 

  3. Berardi G, Antonelli G, Colasanti M, et al. Association of sarcopenia and body composition with short-term outcomes after liver resection for malignant tumors. JAMA Surg. 2020:e203336.

  4. Xiao JJ, Caan BJ, Feliciano EMC, et al. The association of medical and demographic characteristics with sarcopenia and low muscle radiodensity in patients with nonmetastatic colorectal cancer. Am J Clin Nutr. 2019;109:615–25.

    Article  Google Scholar 

  5. Daly LE, Prado CM, Ryan AM. A window beneath the skin: how computed tomography assessment of body composition can assist in the identification of hidden wasting conditions in oncology that profoundly impact outcomes. Proc Nutr Soc. 2018;77:135–51.

    Article  CAS  Google Scholar 

  6. Poltronieri TS, de Paula NS, Chaves GV. Assessing skeletal muscle radiodensity by computed tomography: an integrative review of the applied methodologies. Clin Physiol Funct Imaging. 2020;40:207–23.

    Article  Google Scholar 

  7. Ettinger DS, Wood DE, Aggarwal C, et al. Non-small cell lung cancer, version 1.2020 featured updates to the NCCN guidelines. J Natl Compr Cancer Netw. 2019;17:1464–72.

    Article  Google Scholar 

  8. Hilmi M, Jouinot A, Burns R, et al. Body composition and sarcopenia: the next generation of personalized oncology and pharmacology? Pharmacol Ther. 2019;196:135–59.

    Article  CAS  Google Scholar 

  9. Kinsey CM, Estepar RS, van der Velden J, Cole BF, Christiani DC, Washko GR. Lower pectoralis muscle area is associated with a worse overall survival in non-small cell lung cancer. Cancer Epidemiol Biomarkers Prev. 2017;26:38–43.

    Article  Google Scholar 

  10. Best TD, Mercaldo SF, Bryan DS, et al. Multilevel body composition analysis on chest computed tomography predicts hospital length of stay and complications after lobectomy for lung cancer: a multicenter study. Ann Surg. 2020. https://doi.org/10.1097/SLA.0000000000004040 (Online ahead of print).

  11. Katayama H, Kurokawa Y, Nakamura K, et al. Extended Clavien-Dindo classification of surgical complications: Japan Clinical Oncology Group postoperative complications criteria. Surg Today. 2016;46:668–85.

    Article  Google Scholar 

  12. Prado CM, Lieffers JR, McCargar LJ, et al. Prevalence and clinical implications of sarcopenic obesity in patients with solid tumours of the respiratory and gastrointestinal tracts: a population-based study. Lancet Oncol. 2008;9:629–35.

    Article  Google Scholar 

  13. Sun C, Anraku M, Karasaki T, et al. Low truncal muscle area on chest computed tomography: a poor prognostic factor for the cure of early-stage non-small-cell lung cancerdagger. Eur J Cardiothorac Surg. 2019;55:414–20.

    Article  Google Scholar 

  14. Alifano M, Falcoz PE, Seegers V, et al. Preresection serum C-reactive protein measurement and survival among patients with resectable non-small cell lung cancer. J Thorac Cardiov Surg. 2011;142:1161–7.

    Article  CAS  Google Scholar 

  15. Grunnet M, Sorensen JB. Carcinoembryonic antigen (CEA) as tumor marker in lung cancer. Lung Cancer. 2012;76:138–43.

    Article  CAS  Google Scholar 

  16. Hubbard JM, Cohen HJ, Muss HB. Incorporating biomarkers into cancer and aging research. J Clin Oncol. 2014;32:2611–6.

    Article  Google Scholar 

  17. Sjoblom B, Gronberg BH, Wentzel-Larsen T, et al. Skeletal muscle radiodensity is prognostic for survival in patients with advanced non-small cell lung cancer. Clin Nutr. 2016;35:1386–93.

    Article  Google Scholar 

  18. Feliciano EMC, Kroenke CH, Meyerhardt JA, et al. Association of systemic inflammation and sarcopenia with survival in nonmetastatic colorectal cancer: results from the C SCANS study. JAMA Oncol. 2017;3:e172319.

  19. Honors MA, Kinzig KP. The role of insulin resistance in the development of muscle wasting during cancer cachexia. J Cachexia Sarcopenia Muscle. 2012;3:5–11.

    Article  Google Scholar 

  20. Marcus RL, Addison O, Kidde JP, Dibble LE, Lastayo PC. Skeletal muscle fat infiltration: impact of age, inactivity, and exercise. J Nutr Health Aging. 2010;14:362–6.

    Article  CAS  Google Scholar 

  21. Kera T, Kawai H, Hirano H, et al. Definition of respiratory sarcopenia with peak expiratory flow rate. J Am Med Dir Assoc. 2019;20:1021–5.

    Article  Google Scholar 

  22. Goldstraw P, Chansky K, Crowley J, et al. The IASLC Lung Cancer Staging Project: proposals for revision of the TNM stage groupings in the forthcoming (eighth) edition of the TNM classification for lung cancer. J Thorac Oncol. 2016;11:39–51.

    Article  Google Scholar 

  23. Martin L, Birdsell L, Macdonald N, et al. Cancer cachexia in the age of obesity: skeletal muscle depletion is a powerful prognostic factor, independent of body mass index. J Clin Oncol. 2013;31:1539–47.

    Article  Google Scholar 

  24. Baracos VE, Reiman T, Mourtzakis M, Gioulbasanis I, Antoun S. Body composition in patients with non-small cell lung cancer: a contemporary view of cancer cachexia with the use of computed tomography image analysis. Am J Clin Nutr. 2010;91:1133S-S1137.

    Article  CAS  Google Scholar 

  25. Zhang X, Liu Y, Shao H, Zheng X. Obesity paradox in lung cancer prognosis: evolving biological insights and clinical implications. J Thorac Oncol. 2017;12:1478–88.

    Article  Google Scholar 

  26. Sun C, Anraku M, Kawahara T, et al. Prognostic significance of low pectoralis muscle mass on preoperative chest computed tomography in localized non-small cell lung cancer after curative-intent surgery. Lung Cancer. 2020;147:71–6.

    Article  Google Scholar 

  27. Yang M, Shen Y, Tan L, Li W. Prognostic value of sarcopenia in lung cancer: a systematic review and meta-analysis. Chest. 2019;156:101–11.

    Article  Google Scholar 

  28. Cruz-Jentoft AJ, Bahat G, Bauer J, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48:16–31.

    Article  Google Scholar 

  29. Rondanelli M, Klersy C, Terracol G, et al. Whey protein, amino acids, and vitamin D supplementation with physical activity increases fat-free mass and strength, functionality, and quality of life and decreases inflammation in sarcopenic elderly. Am J Clin Nutr. 2016;103:830–40.

    Article  CAS  Google Scholar 

  30. Bjorkman MP, Suominen MH, Kautiainen H, et al. Effect of protein supplementation on physical performance in older people with sarcopenia: a randomized controlled trial. J Am Med Dir Assoc. 2020;21:226–32.

    Article  Google Scholar 

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Acknowledgments

Changbo Sun received a Japan-China Sasakawa Medical fellowship from the Sasakawa Memorial Health Foundation. The remaining authors have no conflicts of interest.

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Correspondence to Masaki Anraku MD, PhD.

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Sun, C., Anraku, M., Kawahara, T. et al. Combination of Skeletal Muscle Mass and Density Predicts Postoperative Complications and Survival of Patients With Non-Small Cell Lung Cancer. Ann Surg Oncol 29, 1816–1824 (2022). https://doi.org/10.1245/s10434-021-11024-8

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