Skip to main content
Top
Published in: Surgery Today 7/2021

01-07-2021 | NSCLC | Original Article

The prognostic impact of sarcopenia on elderly patients undergoing pulmonary resection for non-small cell lung cancer

Authors: Akihiro Miura, Hiromasa Yamamoto, Hiroki Sato, Yasuaki Tomioka, Toshio Shiotani, Ken Suzawa, Kentaroh Miyoshi, Shinji Otani, Mikio Okazaki, Seiichiro Sugimoto, Masaomi Yamane, Shinichi Toyooka

Published in: Surgery Today | Issue 7/2021

Login to get access

Abstract

Purpose

The number of elderly patients who undergo surgery is increasing, even though they are at a high risk due to a decreased physical strength. Furthermore, sarcopenia is generally associated with a poor prognosis in patients with non-small cell lung cancer (NSCLC).

Methods

This study included NSCLC patients  ≥ 65 years old who underwent pulmonary resection in our hospital between 2012 and 2015. Sarcopenia was assessed using the psoas muscle mass index based on computed tomography at the level of the third lumbar vertebra. We elucidated the impact of sarcopenia on short- and long-term outcomes after surgery.

Results

We enrolled 259 patients, including 179 with sarcopenia. Patients with sarcopenia before surgery tended to have postoperative complications (p = 0.0521), although they did not show a poor prognosis. In patients with sarcopenia, a multivariate analysis revealed that postoperative complications and the progression of sarcopenia 1 year after surgery were significant risk factors for a poor prognosis (p = 0.0169 and 0.00370, respectively).

Conclusions

The progression of sarcopenia after surgery is associated with a poor prognosis in elderly NSCLC patients with sarcopenia. A strategy to prevent postoperative progressive sarcopenia may be necessary for improving the clinical outcome of this population.
Appendix
Available only for authorised users
Literature
1.
go back to reference Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J Clin. 2019;69:7–34.CrossRef Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J Clin. 2019;69:7–34.CrossRef
2.
go back to reference Malvezzi M, Carioli G, Bertuccio P, Boffetta P, Levi F, La Vecchia C, et al. European cancer mortality predictions for the year 2017, with focus on lung cancer. Ann Oncol. 2017;28:1117–23.CrossRef Malvezzi M, Carioli G, Bertuccio P, Boffetta P, Levi F, La Vecchia C, et al. European cancer mortality predictions for the year 2017, with focus on lung cancer. Ann Oncol. 2017;28:1117–23.CrossRef
3.
go back to reference Ginsberg RJ, Rubinstein LV. Randomized trial of lobectomy versus limited resection for T1 N0 non-small cell lung cancer. Lung Cancer Study Group. Ann Thorac Surg. 1995;60:615–23.CrossRef Ginsberg RJ, Rubinstein LV. Randomized trial of lobectomy versus limited resection for T1 N0 non-small cell lung cancer. Lung Cancer Study Group. Ann Thorac Surg. 1995;60:615–23.CrossRef
4.
go back to reference Ross PJ, Ashley S, Norton A, Priest K, Waters JS, Eisen T, et al. Do patients with weight loss have a worse outcome when undergoing chemotherapy for lung cancers? Br J Cancer. 2004;90:1905–11.CrossRef Ross PJ, Ashley S, Norton A, Priest K, Waters JS, Eisen T, et al. Do patients with weight loss have a worse outcome when undergoing chemotherapy for lung cancers? Br J Cancer. 2004;90:1905–11.CrossRef
5.
go back to reference Shimizu H, Okada M, Tangoku A, Doki Y, Committee for Scientific Affairs TJAfTS, et al. Thoracic and cardiovascular surgeries in Japan during 2017: annual report by the Japanese Association for Thoracic Surgery. Gen Thorac Cardiovasc Surg. 2020;68:414–49.CrossRef Shimizu H, Okada M, Tangoku A, Doki Y, Committee for Scientific Affairs TJAfTS, et al. Thoracic and cardiovascular surgeries in Japan during 2017: annual report by the Japanese Association for Thoracic Surgery. Gen Thorac Cardiovasc Surg. 2020;68:414–49.CrossRef
6.
go back to reference Schulte T, Schniewind B, Walter J, Dohrmann P, Kuchler T, Kurdow R. Age-related impairment of quality of life after lung resection for non-small cell lung cancer. Lung Cancer. 2010;68:115–20.CrossRef Schulte T, Schniewind B, Walter J, Dohrmann P, Kuchler T, Kurdow R. Age-related impairment of quality of life after lung resection for non-small cell lung cancer. Lung Cancer. 2010;68:115–20.CrossRef
7.
8.
go back to reference Go SI, Park MJ, Song HN, Kang MH, Park HJ, Jeon KN, et al. Sarcopenia and inflammation are independent predictors of survival in male patients newly diagnosed with small cell lung cancer. Support Care Cancer. 2016;24:2075–84.CrossRef Go SI, Park MJ, Song HN, Kang MH, Park HJ, Jeon KN, et al. Sarcopenia and inflammation are independent predictors of survival in male patients newly diagnosed with small cell lung cancer. Support Care Cancer. 2016;24:2075–84.CrossRef
9.
go back to reference Iritani S, Imai K, Takai K, Hanai T, Ideta T, Miyazaki T, et al. Skeletal muscle depletion is an independent prognostic factor for hepatocellular carcinoma. J Gastroenterol. 2015;50:323–32.CrossRef Iritani S, Imai K, Takai K, Hanai T, Ideta T, Miyazaki T, et al. Skeletal muscle depletion is an independent prognostic factor for hepatocellular carcinoma. J Gastroenterol. 2015;50:323–32.CrossRef
10.
go back to reference Kim EY, Kim YS, Park I, Ahn HK, Cho EK, Jeong YM. Prognostic significance of CT-determined sarcopenia in patients with small-cell lung cancer. J Thorac Oncol. 2015;10:1795–9.CrossRef Kim EY, Kim YS, Park I, Ahn HK, Cho EK, Jeong YM. Prognostic significance of CT-determined sarcopenia in patients with small-cell lung cancer. J Thorac Oncol. 2015;10:1795–9.CrossRef
11.
go back to reference Nakamura R, Inage Y, Tobita R, Yoneyama S, Numata T, Ota K, et al. Sarcopenia in resected NSCLC: effect on postoperative outcomes. J Thorac Oncol. 2018;13:895–903.CrossRef Nakamura R, Inage Y, Tobita R, Yoneyama S, Numata T, Ota K, et al. Sarcopenia in resected NSCLC: effect on postoperative outcomes. J Thorac Oncol. 2018;13:895–903.CrossRef
12.
go back to reference Prado CM, Baracos VE, McCargar LJ, Mourtzakis M, Mulder KE, Reiman T, et al. Body composition as an independent determinant of 5-fluorouracil-based chemotherapy toxicity. Clin Cancer Res. 2007;13:3264–8.CrossRef Prado CM, Baracos VE, McCargar LJ, Mourtzakis M, Mulder KE, Reiman T, et al. Body composition as an independent determinant of 5-fluorouracil-based chemotherapy toxicity. Clin Cancer Res. 2007;13:3264–8.CrossRef
13.
go back to reference Prado CM, Baracos VE, McCargar LJ, Reiman T, Mourtzakis M, Tonkin K, et al. Sarcopenia as a determinant of chemotherapy toxicity and time to tumor progression in metastatic breast cancer patients receiving capecitabine treatment. Clin Cancer Res. 2009;15:2920–6.CrossRef Prado CM, Baracos VE, McCargar LJ, Reiman T, Mourtzakis M, Tonkin K, et al. Sarcopenia as a determinant of chemotherapy toxicity and time to tumor progression in metastatic breast cancer patients receiving capecitabine treatment. Clin Cancer Res. 2009;15:2920–6.CrossRef
14.
go back to reference Tsukioka T, Nishiyama N, Izumi N, Mizuguchi S, Komatsu H, Okada S, et al. Sarcopenia is a novel poor prognostic factor in male patients with pathological Stage I non-small cell lung cancer. Jpn J Clin Oncol. 2017;47:363–8.CrossRef Tsukioka T, Nishiyama N, Izumi N, Mizuguchi S, Komatsu H, Okada S, et al. Sarcopenia is a novel poor prognostic factor in male patients with pathological Stage I non-small cell lung cancer. Jpn J Clin Oncol. 2017;47:363–8.CrossRef
15.
go back to reference Kiriya Y, Toshiaki N, Shibasaki I, Ogata K, Ogawa H, Takei Y, et al. Sarcopenia assessed by the quantity and quality of skeletal muscle is a prognostic factor for patients undergoing cardiac surgery. Surg Today. 2020;50:895–904.CrossRef Kiriya Y, Toshiaki N, Shibasaki I, Ogata K, Ogawa H, Takei Y, et al. Sarcopenia assessed by the quantity and quality of skeletal muscle is a prognostic factor for patients undergoing cardiac surgery. Surg Today. 2020;50:895–904.CrossRef
16.
go back to reference Morley JE. Sarcopenia: diagnosis and treatment. J Nutr Health Aging. 2008;12:452–6.CrossRef Morley JE. Sarcopenia: diagnosis and treatment. J Nutr Health Aging. 2008;12:452–6.CrossRef
17.
go back to reference Hutchins LF, Unger JM, Crowley JJ, Coltman CA Jr, Albain KS. Underrepresentation of patients 65 years of age or older in cancer-treatment trials. N Engl J Med. 1999;341:2061–7.CrossRef Hutchins LF, Unger JM, Crowley JJ, Coltman CA Jr, Albain KS. Underrepresentation of patients 65 years of age or older in cancer-treatment trials. N Engl J Med. 1999;341:2061–7.CrossRef
18.
go back to reference Canoui-Poitrine F, Lievre A, Dayde F, Lopez-Trabada-Ataz D, Baumgaertner I, Dubreuil O, et al. Inclusion of older patients with cancer in clinical trials: The SAGE prospective multicenter cohort survey. Oncologist. 2019;24:e1351–9.CrossRef Canoui-Poitrine F, Lievre A, Dayde F, Lopez-Trabada-Ataz D, Baumgaertner I, Dubreuil O, et al. Inclusion of older patients with cancer in clinical trials: The SAGE prospective multicenter cohort survey. Oncologist. 2019;24:e1351–9.CrossRef
19.
go back to reference Goldstraw P, Chansky K, Crowley J, Rami-Porta R, Asamura H, Eberhardt WE, 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.CrossRef Goldstraw P, Chansky K, Crowley J, Rami-Porta R, Asamura H, Eberhardt WE, 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.CrossRef
20.
go back to reference Travis WD, Brambilla E, Burke AP, Marx A, Nicholson AG. Introduction to The 2015 World Health Organization classification of tumors of the lung, pleura, thymus, and heart. J Thorac Oncol. 2015;10:1240–2.CrossRef Travis WD, Brambilla E, Burke AP, Marx A, Nicholson AG. Introduction to The 2015 World Health Organization classification of tumors of the lung, pleura, thymus, and heart. J Thorac Oncol. 2015;10:1240–2.CrossRef
21.
go back to reference Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, et al. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg. 2009;250:187–96.CrossRef Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, et al. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg. 2009;250:187–96.CrossRef
22.
go back to reference Shinohara S, Otsuki R, Kobayashi K, Sugaya M, Matsuo M, Nakagawa M. Impact of sarcopenia on surgical outcomes in non-small cell lung cancer. Ann Surg Oncol. 2020;27:2427–35.CrossRef Shinohara S, Otsuki R, Kobayashi K, Sugaya M, Matsuo M, Nakagawa M. Impact of sarcopenia on surgical outcomes in non-small cell lung cancer. Ann Surg Oncol. 2020;27:2427–35.CrossRef
23.
go back to reference Takamori S, Tagawa T, Toyokawa G, Shimokawa M, Kinoshita F, Kozuma Y, et al. Prognostic impact of postoperative skeletal muscle decrease in non-small cell lung cancer. Ann Thorac Surg. 2020;109:914–20.CrossRef Takamori S, Tagawa T, Toyokawa G, Shimokawa M, Kinoshita F, Kozuma Y, et al. Prognostic impact of postoperative skeletal muscle decrease in non-small cell lung cancer. Ann Thorac Surg. 2020;109:914–20.CrossRef
24.
go back to reference Chambard L, Girard N, Ollier E, Rousseau JC, Duboeuf F, Carlier MC, et al. Bone, muscle, and metabolic parameters predict survival in patients with synchronous bone metastases from lung cancers. Bone. 2018;108:202–9.CrossRef Chambard L, Girard N, Ollier E, Rousseau JC, Duboeuf F, Carlier MC, et al. Bone, muscle, and metabolic parameters predict survival in patients with synchronous bone metastases from lung cancers. Bone. 2018;108:202–9.CrossRef
25.
go back to reference Suzuki Y, Okamoto T, Fujishita T, Katsura M, Akamine T, Takamori S, et al. Clinical implications of sarcopenia in patients undergoing complete resection for early non-small cell lung cancer. Lung Cancer. 2016;101:92–7.CrossRef Suzuki Y, Okamoto T, Fujishita T, Katsura M, Akamine T, Takamori S, et al. Clinical implications of sarcopenia in patients undergoing complete resection for early non-small cell lung cancer. Lung Cancer. 2016;101:92–7.CrossRef
26.
go back to reference Matsuo Y, Mitsuyoshi T, Shintani T, Iizuka Y, Mizowaki T. Impact of low skeletal muscle mass on non-lung cancer mortality after stereotactic body radiotherapy for patients with stage I non-small cell lung cancer. J Geriatr Oncol. 2018;9:589–93.CrossRef Matsuo Y, Mitsuyoshi T, Shintani T, Iizuka Y, Mizowaki T. Impact of low skeletal muscle mass on non-lung cancer mortality after stereotactic body radiotherapy for patients with stage I non-small cell lung cancer. J Geriatr Oncol. 2018;9:589–93.CrossRef
27.
go back to reference Kim EY, Lee HY, Kim KW, Lee JI, Kim YS, Choi WJ, et al. Preoperative computed tomography-determined sarcopenia and postoperative outcome after surgery for non-small cell lung cancer. Scand J Surg. 2018;107:244–51.CrossRef Kim EY, Lee HY, Kim KW, Lee JI, Kim YS, Choi WJ, et al. Preoperative computed tomography-determined sarcopenia and postoperative outcome after surgery for non-small cell lung cancer. Scand J Surg. 2018;107:244–51.CrossRef
28.
go back to reference Stene GB, Helbostad JL, Amundsen T, Sorhaug S, Hjelde H, Kaasa S, et al. Changes in skeletal muscle mass during palliative chemotherapy in patients with advanced lung cancer. Acta Oncol. 2015;54:340–8.CrossRef Stene GB, Helbostad JL, Amundsen T, Sorhaug S, Hjelde H, Kaasa S, et al. Changes in skeletal muscle mass during palliative chemotherapy in patients with advanced lung cancer. Acta Oncol. 2015;54:340–8.CrossRef
29.
go back to reference Yancik R, Wesley MN, Ries LA, Havlik RJ, Edwards BK, Yates JW. Effect of age and comorbidity in postmenopausal breast cancer patients aged 55 years and older. JAMA. 2001;285:885–92.CrossRef Yancik R, Wesley MN, Ries LA, Havlik RJ, Edwards BK, Yates JW. Effect of age and comorbidity in postmenopausal breast cancer patients aged 55 years and older. JAMA. 2001;285:885–92.CrossRef
30.
go back to reference Yancik R, Wesley MN, Ries LA, Havlik RJ, Long S, Edwards BK, et al. Comorbidity and age as predictors of risk for early mortality of male and female colon carcinoma patients: a population-based study. Cancer. 1998;82:2123–34.CrossRef Yancik R, Wesley MN, Ries LA, Havlik RJ, Long S, Edwards BK, et al. Comorbidity and age as predictors of risk for early mortality of male and female colon carcinoma patients: a population-based study. Cancer. 1998;82:2123–34.CrossRef
31.
go back to reference Mayo NE, Feldman L, Scott S, Zavorsky G, Kim DJ, Charlebois P, et al. Impact of preoperative change in physical function on postoperative recovery: argument supporting prehabilitation for colorectal surgery. Surgery. 2011;150:505–14.CrossRef Mayo NE, Feldman L, Scott S, Zavorsky G, Kim DJ, Charlebois P, et al. Impact of preoperative change in physical function on postoperative recovery: argument supporting prehabilitation for colorectal surgery. Surgery. 2011;150:505–14.CrossRef
32.
go back to reference Benzo R, Wigle D, Novotny P, Wetzstein M, Nichols F, Shen RK, et al. Preoperative pulmonary rehabilitation before lung cancer resection: results from two randomized studies. Lung Cancer. 2011;74:441–5.CrossRef Benzo R, Wigle D, Novotny P, Wetzstein M, Nichols F, Shen RK, et al. Preoperative pulmonary rehabilitation before lung cancer resection: results from two randomized studies. Lung Cancer. 2011;74:441–5.CrossRef
33.
go back to reference Lin HS, Watts JN, Peel NM, Hubbard RE. Frailty and post-operative outcomes in older surgical patients: a systematic review. BMC Geriatr. 2016;16:157.CrossRef Lin HS, Watts JN, Peel NM, Hubbard RE. Frailty and post-operative outcomes in older surgical patients: a systematic review. BMC Geriatr. 2016;16:157.CrossRef
34.
go back to reference Jones SE, Maddocks M, Kon SS, Canavan JL, Nolan CM, Clark AL, et al. Sarcopenia in COPD: prevalence, clinical correlates and response to pulmonary rehabilitation. Thorax. 2015;70:213–8.CrossRef Jones SE, Maddocks M, Kon SS, Canavan JL, Nolan CM, Clark AL, et al. Sarcopenia in COPD: prevalence, clinical correlates and response to pulmonary rehabilitation. Thorax. 2015;70:213–8.CrossRef
35.
go back to reference Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, et al. Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on sarcopenia in older people. Age Ageing. 2010;39:412–23.CrossRef Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, et al. Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on sarcopenia in older people. Age Ageing. 2010;39:412–23.CrossRef
36.
go back to reference Studenski SA, Peters KW, Alley DE, Cawthon PM, McLean RR, Harris TB, et al. The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. J Gerontol A Biol Sci Med Sci. 2014;69:547–58.CrossRef Studenski SA, Peters KW, Alley DE, Cawthon PM, McLean RR, Harris TB, et al. The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. J Gerontol A Biol Sci Med Sci. 2014;69:547–58.CrossRef
37.
go back to reference Chen LK, Liu LK, Woo J, Assantachai P, Auyeung TW, Bahyah KS, et al. Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia. J Am Med Dir Assoc. 2014;15:95–101.CrossRef Chen LK, Liu LK, Woo J, Assantachai P, Auyeung TW, Bahyah KS, et al. Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia. J Am Med Dir Assoc. 2014;15:95–101.CrossRef
38.
go back to reference Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE, Newman AB, et al. Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc. 2011;12:249–56.CrossRef Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE, Newman AB, et al. Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc. 2011;12:249–56.CrossRef
Metadata
Title
The prognostic impact of sarcopenia on elderly patients undergoing pulmonary resection for non-small cell lung cancer
Authors
Akihiro Miura
Hiromasa Yamamoto
Hiroki Sato
Yasuaki Tomioka
Toshio Shiotani
Ken Suzawa
Kentaroh Miyoshi
Shinji Otani
Mikio Okazaki
Seiichiro Sugimoto
Masaomi Yamane
Shinichi Toyooka
Publication date
01-07-2021
Publisher
Springer Singapore
Published in
Surgery Today / Issue 7/2021
Print ISSN: 0941-1291
Electronic ISSN: 1436-2813
DOI
https://doi.org/10.1007/s00595-020-02221-1

Other articles of this Issue 7/2021

Surgery Today 7/2021 Go to the issue