Skip to main content
Top
Published in: Annals of Surgical Oncology 13/2022

17-08-2022 | Esophageal Cancer | Thoracic Oncology

Prognostic Impact of the Loss of Skeletal Muscle Mass During Neoadjuvant Chemotherapy on Older Patients with Esophageal Cancer

Authors: Tsuyoshi Harada, MSc, Tetsuya Tsuji, MD, PhD, Junya Ueno, Yu Koishihara, MSc, Nobuko Konishi, MSc, Nanako Hijikata, MD, Aiko Ishikawa, MD, PhD, Daisuke Kotani, MD, PhD, Takashi Kojima, MD, PhD, Hisashi Fujiwara, MD, PhD, Takeo Fujita, MD, PhD

Published in: Annals of Surgical Oncology | Issue 13/2022

Login to get access

Abstract

Background

In older adults, skeletal muscle mass is an important factor for health and prognosis. The loss of SMM during neoadjuvant therapy affects the prognosis of patients with locally advanced esophageal cancer. However, information is limited regarding this possibility in older patients. This study aimed to establish the prognostic impact of SMM loss during neoadjuvant chemotherapy on older patients with locally advanced esophageal cancer.

Methods

This was a single-center retrospective cohort study. Patients age 65 years or older had undergone R0 curative esophagectomy after NAC. The skeletal muscle mass index before and after NAC was calculated from computed tomography images. The percentage change in the SMI during NAC (SMI%) was calculated from the SMI before and after NAC.

Results

The study analyzed 150 patients with a mean age of 71.1 ± 3.7 years. The mean value of the SMI was 42.7 ± 7.2 cm2/m2 before NAC, and the SMI% was − 6.4% ± 5.9%. The cutoff of SMI% for overall survival was defined by the log-rank test as − 12%. The Cox proportional hazard model showed that major loss of the SMI (≥ 12%) significantly influenced OS (hazard ratio, 2.490; 95% confidence interval, 1.121–5.529; p = 0.025) independently of age, sex, pathologic T and N factors, or treatment regimen.

Conclusions

Major SMI loss has an impact on OS after R0 curative esophagectomy for older patients with locally advanced esophageal cancer.
Literature
1.
go back to reference Sjoquist KM, Burmeister BH, Smithers BM, et al. Survival after neoadjuvant chemotherapy or chemoradiotherapy for resectable oesophageal carcinoma: an updated meta-analysis. Lancet Oncol. 2011;12:681–92.CrossRefPubMed Sjoquist KM, Burmeister BH, Smithers BM, et al. Survival after neoadjuvant chemotherapy or chemoradiotherapy for resectable oesophageal carcinoma: an updated meta-analysis. Lancet Oncol. 2011;12:681–92.CrossRefPubMed
3.
go back to reference Kamangar F, Nasrollahzadeh D, Safiri S, et al. The global, regional, and national burden of oesophageal cancer and its attributable risk factors in 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Gastroenterol Hepatol. 2020;5:582–97.CrossRef Kamangar F, Nasrollahzadeh D, Safiri S, et al. The global, regional, and national burden of oesophageal cancer and its attributable risk factors in 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Gastroenterol Hepatol. 2020;5:582–97.CrossRef
4.
go back to reference Mohile SG, Dale W, Somerfield MR, et al. Practical assessment and management of vulnerabilities in older patients receiving chemotherapy: ASCO guideline for geriatric oncology. J Clin Oncol. 2018;36(22):2326–47.CrossRefPubMedPubMedCentral Mohile SG, Dale W, Somerfield MR, et al. Practical assessment and management of vulnerabilities in older patients receiving chemotherapy: ASCO guideline for geriatric oncology. J Clin Oncol. 2018;36(22):2326–47.CrossRefPubMedPubMedCentral
5.
go back to reference Wildiers H, Heeren P, Puts M, et al. International society of geriatric oncology consensus on geriatric assessment in older patients with cancer. J Clin Oncol. 2014;32(24):2595–603.CrossRefPubMedPubMedCentral Wildiers H, Heeren P, Puts M, et al. International society of geriatric oncology consensus on geriatric assessment in older patients with cancer. J Clin Oncol. 2014;32(24):2595–603.CrossRefPubMedPubMedCentral
7.
go back to reference Clegg A, Young J, Iliffe S, Rikkert MO, Rockwood K. Frailty in elderly people. Lancet. 2013;381(9868):752–62.CrossRefPubMed Clegg A, Young J, Iliffe S, Rikkert MO, Rockwood K. Frailty in elderly people. Lancet. 2013;381(9868):752–62.CrossRefPubMed
8.
go back to reference Fulop T, Larbi A, Witkowski JM, et al. Aging, frailty, and age-related diseases. Biogerontology. 2010;11(5):547–63.CrossRefPubMed Fulop T, Larbi A, Witkowski JM, et al. Aging, frailty, and age-related diseases. Biogerontology. 2010;11(5):547–63.CrossRefPubMed
9.
go back to reference Extermann M, Brain E, Canin B, et al. Priorities for the global advancement of care for older adults with cancer: an update of the International Society of Geriatric Oncology Priorities Initiative. Lancet Oncol. 2021;22:e29–36.CrossRefPubMed Extermann M, Brain E, Canin B, et al. Priorities for the global advancement of care for older adults with cancer: an update of the International Society of Geriatric Oncology Priorities Initiative. Lancet Oncol. 2021;22:e29–36.CrossRefPubMed
12.
go back to reference Fried LP, Tangen CM, Walston J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol Series A Biol Sci Med Sci. 2001;56:M146–57.CrossRef Fried LP, Tangen CM, Walston J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol Series A Biol Sci Med Sci. 2001;56:M146–57.CrossRef
13.
go back to reference Jang MK, Park C, Hong S, Li H, Rhee E, Doorenbos AZ. Skeletal muscle mass change during chemotherapy: a systematic review and meta-analysis. Anticancer Res. 2020;40:2409–18.CrossRefPubMed Jang MK, Park C, Hong S, Li H, Rhee E, Doorenbos AZ. Skeletal muscle mass change during chemotherapy: a systematic review and meta-analysis. Anticancer Res. 2020;40:2409–18.CrossRefPubMed
14.
go back to reference Kamitani N, Migita K, Matsumoto S, et al. Association of skeletal muscle loss with the long-term outcomes of esophageal cancer patients treated with neoadjuvant chemotherapy. Surg Today. 2019;49:1022–8.CrossRefPubMed Kamitani N, Migita K, Matsumoto S, et al. Association of skeletal muscle loss with the long-term outcomes of esophageal cancer patients treated with neoadjuvant chemotherapy. Surg Today. 2019;49:1022–8.CrossRefPubMed
15.
go back to reference Järvinen T, Ilonen I, Kauppi J, Salo J, Räsänen J. Loss of skeletal muscle mass during neoadjuvant treatments correlates with worse prognosis in esophageal cancer: a retrospective cohort study. World J Surg Oncol. 2018;16:1–9.CrossRef Järvinen T, Ilonen I, Kauppi J, Salo J, Räsänen J. Loss of skeletal muscle mass during neoadjuvant treatments correlates with worse prognosis in esophageal cancer: a retrospective cohort study. World J Surg Oncol. 2018;16:1–9.CrossRef
16.
go back to reference Yoon HG, Oh D, Ahn YC, et al. Prognostic impact of sarcopenia and skeletal muscle loss during neoadjuvant chemoradiotherapy in esophageal cancer. Cancers. 2020;12:925.CrossRefPubMedCentral Yoon HG, Oh D, Ahn YC, et al. Prognostic impact of sarcopenia and skeletal muscle loss during neoadjuvant chemoradiotherapy in esophageal cancer. Cancers. 2020;12:925.CrossRefPubMedCentral
18.
go back to reference Nakashima Y, Saeki H, Nakanishi R, et al. Assessment of sarcopenia as a predictor of poor outcomes after esophagectomy in elderly patients with esophageal cancer. Ann Surg. 2018;267:1100–4.CrossRefPubMed Nakashima Y, Saeki H, Nakanishi R, et al. Assessment of sarcopenia as a predictor of poor outcomes after esophagectomy in elderly patients with esophageal cancer. Ann Surg. 2018;267:1100–4.CrossRefPubMed
19.
go back to reference Yamashita K, Watanabe M, Mine S, et al. The impact of the Charlson Comorbidity Index on the prognosis of esophageal cancer patients who underwent esophagectomy with curative intent. Surg Today. 2018;48:632–9.CrossRefPubMed Yamashita K, Watanabe M, Mine S, et al. The impact of the Charlson Comorbidity Index on the prognosis of esophageal cancer patients who underwent esophagectomy with curative intent. Surg Today. 2018;48:632–9.CrossRefPubMed
21.
go back to reference Huang Y, Feng JF, Liu JS, Chen QX. Prognostic role of serum C-reactive protein in esophageal cancer: a systematic review and meta-analysis. Therapeut Clin Risk Manage. 2015;11:89–94.CrossRef Huang Y, Feng JF, Liu JS, Chen QX. Prognostic role of serum C-reactive protein in esophageal cancer: a systematic review and meta-analysis. Therapeut Clin Risk Manage. 2015;11:89–94.CrossRef
22.
go back to reference Yang X, Huang Y, Feng JF, Liu JS. Prognostic significance of neutrophil-to-lymphocyte ratio in esophageal cancer: a meta-analysis. OncoTargets Ther. 2015;8:789–94.CrossRef Yang X, Huang Y, Feng JF, Liu JS. Prognostic significance of neutrophil-to-lymphocyte ratio in esophageal cancer: a meta-analysis. OncoTargets Ther. 2015;8:789–94.CrossRef
23.
go back to reference Bullock AF, Greenley SL, McKenzie GA, Paton LW, Johnson MJ. Relationship between markers of malnutrition and clinical outcomes in older adults with cancer: systematic review, narrative synthesis, and meta-analysis. Eur J Clin Nutr. 2020;74:1519–35.CrossRefPubMedPubMedCentral Bullock AF, Greenley SL, McKenzie GA, Paton LW, Johnson MJ. Relationship between markers of malnutrition and clinical outcomes in older adults with cancer: systematic review, narrative synthesis, and meta-analysis. Eur J Clin Nutr. 2020;74:1519–35.CrossRefPubMedPubMedCentral
24.
go back to reference Izaks GJ, Westendorp RG, Knook DL. The definition of anemia in older persons. JAMA. 1999;281:1714–7.CrossRefPubMed Izaks GJ, Westendorp RG, Knook DL. The definition of anemia in older persons. JAMA. 1999;281:1714–7.CrossRefPubMed
25.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
26.
go back to reference Mourtzakis M, Prado CM, Lieffers JR, Reiman T, McCargar LJ, Baracos VE. A practical and precise approach to quantification of body composition in cancer patients using computed tomography images acquired during routine care. Appl Physiol Nutr Metab. 2008;33:997–1006.CrossRefPubMed Mourtzakis M, Prado CM, Lieffers JR, Reiman T, McCargar LJ, Baracos VE. A practical and precise approach to quantification of body composition in cancer patients using computed tomography images acquired during routine care. Appl Physiol Nutr Metab. 2008;33:997–1006.CrossRefPubMed
27.
go back to reference 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(7):629–35.CrossRefPubMed 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(7):629–35.CrossRefPubMed
28.
go back to reference Stene GB, Helbostad JL, Amundsen T, et al. Changes in skeletal muscle mass during palliative chemotherapy in patients with advanced lung cancer. Acta Oncologica. 2015;54:340–8.CrossRefPubMed Stene GB, Helbostad JL, Amundsen T, et al. Changes in skeletal muscle mass during palliative chemotherapy in patients with advanced lung cancer. Acta Oncologica. 2015;54:340–8.CrossRefPubMed
29.
go back to reference Reid KF, Pasha E, Doros G, et al. Longitudinal decline of lower extremity muscle power in healthy and mobility-limited older adults: influence of muscle mass, strength, composition, neuromuscular activation, and single fiber contractile properties. Eur J Appl Physiol. 2014;114:29–39.CrossRefPubMedPubMedCentral Reid KF, Pasha E, Doros G, et al. Longitudinal decline of lower extremity muscle power in healthy and mobility-limited older adults: influence of muscle mass, strength, composition, neuromuscular activation, and single fiber contractile properties. Eur J Appl Physiol. 2014;114:29–39.CrossRefPubMedPubMedCentral
30.
go back to reference Koster A, Ding J, Stenholm S, et al. Does the amount of fat mass predict age-related loss of lean mass, muscle strength, and muscle quality in older adults. J Gerontol Series A Biomed Sci Med Sci. 2011;66:888–95.CrossRef Koster A, Ding J, Stenholm S, et al. Does the amount of fat mass predict age-related loss of lean mass, muscle strength, and muscle quality in older adults. J Gerontol Series A Biomed Sci Med Sci. 2011;66:888–95.CrossRef
31.
go back to reference Cruz-Jentoft AJ, Bahat G, Bauer J, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48:16–31.CrossRefPubMed Cruz-Jentoft AJ, Bahat G, Bauer J, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48:16–31.CrossRefPubMed
33.
go back to reference Löfgren A, Åkesson O, Johansson J, Persson J. Hospital costs and health-related quality of life from complications after esophagectomy. Eur J Surg Oncol. 2021;47:1042–7.CrossRefPubMed Löfgren A, Åkesson O, Johansson J, Persson J. Hospital costs and health-related quality of life from complications after esophagectomy. Eur J Surg Oncol. 2021;47:1042–7.CrossRefPubMed
34.
go back to reference Derogar M, Orsini N, Sadr-Azodi O, Lagergren P. Influence of major postoperative complications on health-related quality of life among long-term survivors of esophageal cancer surgery. J Clin Oncol. 2012;30:1615–9.CrossRefPubMed Derogar M, Orsini N, Sadr-Azodi O, Lagergren P. Influence of major postoperative complications on health-related quality of life among long-term survivors of esophageal cancer surgery. J Clin Oncol. 2012;30:1615–9.CrossRefPubMed
35.
go back to reference Kataoka K, Takeuchi H, Mizusawa J, et al. Prognostic impact of postoperative morbidity after esophagectomy for esophageal cancer: exploratory analysis of JCOG9907. Ann Surg. 2017;265:1152–7.CrossRefPubMed Kataoka K, Takeuchi H, Mizusawa J, et al. Prognostic impact of postoperative morbidity after esophagectomy for esophageal cancer: exploratory analysis of JCOG9907. Ann Surg. 2017;265:1152–7.CrossRefPubMed
36.
go back to reference Hironaka S, Tsubosa Y, Mizusawa J, et al. Phase I/II trial of 2-weekly docetaxel combined with cisplatin plus fluorouracil in metastatic esophageal cancer (JCOG 0807). Cancer Sci. 2014;105:1189–95.CrossRefPubMedPubMedCentral Hironaka S, Tsubosa Y, Mizusawa J, et al. Phase I/II trial of 2-weekly docetaxel combined with cisplatin plus fluorouracil in metastatic esophageal cancer (JCOG 0807). Cancer Sci. 2014;105:1189–95.CrossRefPubMedPubMedCentral
37.
go back to reference Takahashi H, Arimura Y, Yamashita K, et al. Phase I/II study of docetaxel/cisplatin/fluorouracil combination chemotherapy against metastatic esophageal squamous cell carcinoma. J Thorac Oncol. 2010;5:122–8.CrossRefPubMed Takahashi H, Arimura Y, Yamashita K, et al. Phase I/II study of docetaxel/cisplatin/fluorouracil combination chemotherapy against metastatic esophageal squamous cell carcinoma. J Thorac Oncol. 2010;5:122–8.CrossRefPubMed
38.
go back to reference Tamura S, Imano M, Takiuchi H, et al. Phase II study of docetaxel, cisplatin, and 5-fluorouracil (DCF) for metastatic esophageal cancer (OGSG 0403). Anticancer Res. 2012;32:1403–8.PubMed Tamura S, Imano M, Takiuchi H, et al. Phase II study of docetaxel, cisplatin, and 5-fluorouracil (DCF) for metastatic esophageal cancer (OGSG 0403). Anticancer Res. 2012;32:1403–8.PubMed
39.
go back to reference Ando N, Iizuka T, Ide H, et al. Surgery plus chemotherapy compared with surgery alone for localized squamous cell carcinoma of the thoracic esophagus: a Japan Clinical Oncology Group Study–JCOG9204. J Clin Oncol. 2003;21(24):4592–6.CrossRefPubMed Ando N, Iizuka T, Ide H, et al. Surgery plus chemotherapy compared with surgery alone for localized squamous cell carcinoma of the thoracic esophagus: a Japan Clinical Oncology Group Study–JCOG9204. J Clin Oncol. 2003;21(24):4592–6.CrossRefPubMed
40.
go back to reference Liao CD, Chen HC, Huang SW, Liou TH. The role of muscle mass gain following protein supplementation plus exercise therapy in older adults with sarcopenia and frailty risks: a systematic review and meta-regression analysis of randomized trials. Nutrients. 2019;11:1713.CrossRefPubMedCentral Liao CD, Chen HC, Huang SW, Liou TH. The role of muscle mass gain following protein supplementation plus exercise therapy in older adults with sarcopenia and frailty risks: a systematic review and meta-regression analysis of randomized trials. Nutrients. 2019;11:1713.CrossRefPubMedCentral
41.
go back to reference Katakami N, Uchino J, Yokoyama T, et al. Anamorelin (ONO-7643) for the treatment of patients with non-small cell lung cancer and cachexia: results from a randomized, double-blind, placebo-controlled, multicenter study of Japanese patients (ONO-7643-04). Cancer. 2018;124:606–16.CrossRefPubMed Katakami N, Uchino J, Yokoyama T, et al. Anamorelin (ONO-7643) for the treatment of patients with non-small cell lung cancer and cachexia: results from a randomized, double-blind, placebo-controlled, multicenter study of Japanese patients (ONO-7643-04). Cancer. 2018;124:606–16.CrossRefPubMed
42.
go back to reference Maltoni M, Nanni O, Scarpi E, Rossi D, Serra P, Amadori D. High-dose progestins for the treatment of cancer anorexia–cachexia syndrome: a systematic review of randomized clinical trials. Ann Oncol. 2001;12:289–300.CrossRefPubMed Maltoni M, Nanni O, Scarpi E, Rossi D, Serra P, Amadori D. High-dose progestins for the treatment of cancer anorexia–cachexia syndrome: a systematic review of randomized clinical trials. Ann Oncol. 2001;12:289–300.CrossRefPubMed
Metadata
Title
Prognostic Impact of the Loss of Skeletal Muscle Mass During Neoadjuvant Chemotherapy on Older Patients with Esophageal Cancer
Authors
Tsuyoshi Harada, MSc
Tetsuya Tsuji, MD, PhD
Junya Ueno
Yu Koishihara, MSc
Nobuko Konishi, MSc
Nanako Hijikata, MD
Aiko Ishikawa, MD, PhD
Daisuke Kotani, MD, PhD
Takashi Kojima, MD, PhD
Hisashi Fujiwara, MD, PhD
Takeo Fujita, MD, PhD
Publication date
17-08-2022
Publisher
Springer International Publishing
Published in
Annals of Surgical Oncology / Issue 13/2022
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-022-12379-2

Other articles of this Issue 13/2022

Annals of Surgical Oncology 13/2022 Go to the issue