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Published in: Annals of Surgical Oncology 2/2018

01-02-2018 | Thoracic Oncology

Impact of Sarcopenia on Unplanned Readmission and Survival After Esophagectomy in Patients with Esophageal Cancer

Authors: Daisuke Makiura, PhD, Rei Ono, PhD, Junichiro Inoue, PhD, Akimasa Fukuta, RPT, Miyuki Kashiwa, MSc, Yasushi Miura, PhD, Taro Oshikiri, PhD, Tetsu Nakamura, PhD, Yoshihiro Kakeji, PhD, Yoshitada Sakai, PhD

Published in: Annals of Surgical Oncology | Issue 2/2018

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Abstract

Background

Although sarcopenia increases postoperative complications following esophagectomy, its effects on prognosis remain unclear. This study was performed to identify the effect of sarcopenia on 90-day unplanned readmission and overall survival (OS) after esophagectomy.

Methods

Ninety-eight patients with esophageal cancer who underwent esophagectomy were enrolled in this study. Unplanned readmission was defined as any emergent hospitalization within 90 days after discharge. Sarcopenia, defined as low muscle mass plus low muscle strength and/or low physical performance according to the Asian consensus definition, was assessed prior to esophagectomy. Multivariate logistic regression analysis was performed to identify factors that contributed to 90-day unplanned readmission. OS was estimated using the Kaplan–Meier method, and a Cox proportional hazards model was used to assess the relationship between sarcopenia and OS.

Results

Thirty-one patients (31.6%) were diagnosed with sarcopenia. The 90-day unplanned readmission rate was significantly higher in patients with sarcopenia than those without (42.9% vs. 16.4%, respectively; p = 0.01). Multivariable logistic regression analysis showed that sarcopenia was an independent predictor of 90-day unplanned readmission [odds ratio 3.71, 95% confidence interval (CI) 1.29–11.05; p = 0.02], and the log-rank test showed that sarcopenia was associated with OS (p = 0.01). Moreover, sarcopenia was a significant predictor of OS after adjustment for age, sex, and pathological stage (hazard ratio 2.35, 95% CI 1.21–4.54; p = 0.01).

Conclusions

Sarcopenia is a risk factor for 90-day unplanned readmission and OS following esophagectomy. Assessment of sarcopenia could help to identify patients at higher risk of a poor prognosis after esophagectomy.
Literature
1.
go back to reference Wu PC, Posner MC. The role of surgery in the management of oesophageal cancer. Lancet Oncol. 2003;4(8):481–8.CrossRefPubMed Wu PC, Posner MC. The role of surgery in the management of oesophageal cancer. Lancet Oncol. 2003;4(8):481–8.CrossRefPubMed
2.
go back to reference Pultrum BB, Bosch DJ, Nijsten MWN, Rodgers MGG, Groen H, Slaets JPJ, et al. Extended esophagectomy in elderly patients with esophageal cancer: minor effect of age alone in determining the postoperative course and survival. Ann Surg Oncol. 2010;17(6):1572–80.CrossRefPubMedPubMedCentral Pultrum BB, Bosch DJ, Nijsten MWN, Rodgers MGG, Groen H, Slaets JPJ, et al. Extended esophagectomy in elderly patients with esophageal cancer: minor effect of age alone in determining the postoperative course and survival. Ann Surg Oncol. 2010;17(6):1572–80.CrossRefPubMedPubMedCentral
3.
go back to reference McLoughlin JM, Lewis JM, Meredith KL. The impact of age on morbidity and mortality following esophagectomy for esophageal cancer. Cancer Control. 2013;20(2):144–50.CrossRefPubMed McLoughlin JM, Lewis JM, Meredith KL. The impact of age on morbidity and mortality following esophagectomy for esophageal cancer. Cancer Control. 2013;20(2):144–50.CrossRefPubMed
4.
go back to reference Ida S, Watanabe M, Yoshida N, et al. Sarcopenia is a predictor of postoperative respiratory complications in patients with esophageal cancer. Ann Surg Oncol. 2015;22(13):4432–7.CrossRefPubMed Ida S, Watanabe M, Yoshida N, et al. Sarcopenia is a predictor of postoperative respiratory complications in patients with esophageal cancer. Ann Surg Oncol. 2015;22(13):4432–7.CrossRefPubMed
5.
go back to reference Nishigori T, Okabe H, Tanaka E, Tsunoda S, Hisamori S, Sakai Y. Sarcopenia as a predictor of pulmonary complications after esophagectomy for thoracic esophageal cancer. J Surg Oncol. 2016;113(6):678–84.CrossRefPubMed Nishigori T, Okabe H, Tanaka E, Tsunoda S, Hisamori S, Sakai Y. Sarcopenia as a predictor of pulmonary complications after esophagectomy for thoracic esophageal cancer. J Surg Oncol. 2016;113(6):678–84.CrossRefPubMed
6.
go back to reference Makiura D, Ono R, Inoue J, et al. Preoperative sarcopenia is a predictor of postoperative pulmonary complications in esophageal cancer following esophagectomy: a retrospective cohort study. J Geriatr Oncol. 2016;7(6):430–6.CrossRefPubMed Makiura D, Ono R, Inoue J, et al. Preoperative sarcopenia is a predictor of postoperative pulmonary complications in esophageal cancer following esophagectomy: a retrospective cohort study. J Geriatr Oncol. 2016;7(6):430–6.CrossRefPubMed
7.
go back to reference Gill TM, Allore HG, Holford TR, Guo ZC. Hospitalization, restricted activity, and the development of disability among older persons. JAMA. 2004;292(17):2115–24.CrossRefPubMed Gill TM, Allore HG, Holford TR, Guo ZC. Hospitalization, restricted activity, and the development of disability among older persons. JAMA. 2004;292(17):2115–24.CrossRefPubMed
8.
go back to reference Jencks SF, Williams MV, Coleman EA. Rehospitalizations among patients in the Medicare fee-for-service program. N Engl J Med. 2009;360(14):1418–28.CrossRefPubMed Jencks SF, Williams MV, Coleman EA. Rehospitalizations among patients in the Medicare fee-for-service program. N Engl J Med. 2009;360(14):1418–28.CrossRefPubMed
9.
go back to reference Hu Y, McMurry TL, Stukenborg GJ, Kozower BD. Readmission predicts 90-day mortality after esophagectomy: analysis of surveillance, epidemiology, and end results registry linked to medicare outcomes. J Thorac Cardiovasc Surg. 2015;150(5):1254–60.CrossRefPubMedPubMedCentral Hu Y, McMurry TL, Stukenborg GJ, Kozower BD. Readmission predicts 90-day mortality after esophagectomy: analysis of surveillance, epidemiology, and end results registry linked to medicare outcomes. J Thorac Cardiovasc Surg. 2015;150(5):1254–60.CrossRefPubMedPubMedCentral
10.
go back to reference Fernandez FG, Khullar O, Force SD, et al. Hospital readmission is associated with poor survival after esophagectomy for esophageal cancer. Ann Thorac Surg. 2015;99(1):292–7.CrossRefPubMed Fernandez FG, Khullar O, Force SD, et al. Hospital readmission is associated with poor survival after esophagectomy for esophageal cancer. Ann Thorac Surg. 2015;99(1):292–7.CrossRefPubMed
11.
go back to reference Stitzenberg KB, Chang Y, Smith AB, Nielsen ME. Exploring the burden of inpatient readmissions after major cancer surgery. J Clin Oncol. 2015;33(5):455–64.CrossRefPubMed Stitzenberg KB, Chang Y, Smith AB, Nielsen ME. Exploring the burden of inpatient readmissions after major cancer surgery. J Clin Oncol. 2015;33(5):455–64.CrossRefPubMed
12.
go back to reference Wakabayashi H, Matsushima M, Uwano R, Watanabe N, Oritsu H, Shimizu Y. Skeletal muscle mass is associated with severe dysphagia in cancer patients. J Cachexia Sarcopenia Muscle. 2015;6(4):351–7.CrossRefPubMedPubMedCentral Wakabayashi H, Matsushima M, Uwano R, Watanabe N, Oritsu H, Shimizu Y. Skeletal muscle mass is associated with severe dysphagia in cancer patients. J Cachexia Sarcopenia Muscle. 2015;6(4):351–7.CrossRefPubMedPubMedCentral
13.
go back to reference Tamandl D, Paireder M, Asari R, Baltzer PA, Schoppmann SF, Ba-Ssalamah A. Markers of sarcopenia quantified by computed tomography predict adverse long-term outcome in patients with resected oesophageal or gastro-oesophageal junction cancer. Eur Radiol. 2016;26(5):1359–67.CrossRefPubMed Tamandl D, Paireder M, Asari R, Baltzer PA, Schoppmann SF, Ba-Ssalamah A. Markers of sarcopenia quantified by computed tomography predict adverse long-term outcome in patients with resected oesophageal or gastro-oesophageal junction cancer. Eur Radiol. 2016;26(5):1359–67.CrossRefPubMed
14.
go back to reference Paireder M, Asari R, Kristo I, Rieder E, Tamandl D, Ba-Ssalamah A, et al. Impact of sarcopenia on outcome in patients with esophageal resection following neoadjuvant chemotherapy for esophageal cancer. Eur J Surg Oncol. 2017;43(2):478–84.CrossRefPubMed Paireder M, Asari R, Kristo I, Rieder E, Tamandl D, Ba-Ssalamah A, et al. Impact of sarcopenia on outcome in patients with esophageal resection following neoadjuvant chemotherapy for esophageal cancer. Eur J Surg Oncol. 2017;43(2):478–84.CrossRefPubMed
16.
go back to reference Harada K, Ida S, Baba Y, et al. Prognostic and clinical impact of sarcopenia in esophageal squamous cell carcinoma. Dis Esophagus. 2016;29(6):627–33.CrossRefPubMed Harada K, Ida S, Baba Y, et al. Prognostic and clinical impact of sarcopenia in esophageal squamous cell carcinoma. Dis Esophagus. 2016;29(6):627–33.CrossRefPubMed
17.
go back to reference Black D, Mackay C, Ramsay G, et al. Prognostic value of computed tomography: measured parameters of body composition in primary operable gastrointestinal cancers. Ann Surg Oncol. 2017;24(8):2241–51.CrossRefPubMedPubMedCentral Black D, Mackay C, Ramsay G, et al. Prognostic value of computed tomography: measured parameters of body composition in primary operable gastrointestinal cancers. Ann Surg Oncol. 2017;24(8):2241–51.CrossRefPubMedPubMedCentral
18.
go back to reference Zhan KY, Graboyes EM, Nguyen SA, Day TA. Risk factors associated with unplanned readmission in patients undergoing parotid cancer surgery a study of the national cancer database. JAMA Otolaryngol Head Neck Surg. 2016;142(6):544–50.CrossRefPubMed Zhan KY, Graboyes EM, Nguyen SA, Day TA. Risk factors associated with unplanned readmission in patients undergoing parotid cancer surgery a study of the national cancer database. JAMA Otolaryngol Head Neck Surg. 2016;142(6):544–50.CrossRefPubMed
19.
go back to reference Mathiowetz V, Kashman N, Volland G, Weber K, Dowe M, Rogers S. Grip and pinch strength: normative data for adults. Arch Phys Med Rehabil. 1985;66(2):69–74.PubMed Mathiowetz V, Kashman N, Volland G, Weber K, Dowe M, Rogers S. Grip and pinch strength: normative data for adults. Arch Phys Med Rehabil. 1985;66(2):69–74.PubMed
20.
go back to reference Charlson ME, Pompei P, Ales KL, Mackenzie CR. A new method of classifying prognostic co-morbidity in longitudial studies: development and validation. J Chronic Dis. 1987;40(5):373–83.CrossRefPubMed Charlson ME, Pompei P, Ales KL, Mackenzie CR. A new method of classifying prognostic co-morbidity in longitudial studies: development and validation. J Chronic Dis. 1987;40(5):373–83.CrossRefPubMed
21.
go back to reference Forrest LM, McMillan DC, McArdle CS, Angerson WJ, Dunlop DJ. Evaluation of cumulative prognostic scores based on the systemic inflammatory response in patients with inoperable non-small-cell lung cancer. Br J Cancer. 2003;89(6):1028–30.CrossRefPubMedPubMedCentral Forrest LM, McMillan DC, McArdle CS, Angerson WJ, Dunlop DJ. Evaluation of cumulative prognostic scores based on the systemic inflammatory response in patients with inoperable non-small-cell lung cancer. Br J Cancer. 2003;89(6):1028–30.CrossRefPubMedPubMedCentral
22.
go back to reference Sobin L, Wittekind C. TNM classification of malignant tumors, 6th edition. Hoboken, NJ: Wiley, 2002. Sobin L, Wittekind C. TNM classification of malignant tumors, 6th edition. Hoboken, NJ: Wiley, 2002.
23.
go back to reference 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(2):205–13.CrossRefPubMedPubMedCentral 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(2):205–13.CrossRefPubMedPubMedCentral
24.
go back to reference Kunieda K, Ohno T, Fujishima I, Hojo K, Morita T. Reliability and validity of a tool to measure the severity of dysphagia: the food intake level scale. J Pain Symptom Manage. 2013;46(2):201–6.CrossRefPubMed Kunieda K, Ohno T, Fujishima I, Hojo K, Morita T. Reliability and validity of a tool to measure the severity of dysphagia: the food intake level scale. J Pain Symptom Manage. 2013;46(2):201–6.CrossRefPubMed
25.
go back to reference Chen L-K, Liu L-K, Woo J, et al. Sarcopenia in Asia: consensus report of the asian working group for sarcopenia. J Am Med Dir Assoc. 2014;15(2):95–101.CrossRefPubMed Chen L-K, Liu L-K, Woo J, et al. Sarcopenia in Asia: consensus report of the asian working group for sarcopenia. J Am Med Dir Assoc. 2014;15(2):95–101.CrossRefPubMed
26.
go back to reference Sheetz KH, Zhao L, Holcombe SA, et al. Decreased core muscle size is associated with worse patient survival following esophagectomy for cancer. Dis Esophagus. 2013;26(7):716–22.PubMedPubMedCentral Sheetz KH, Zhao L, Holcombe SA, et al. Decreased core muscle size is associated with worse patient survival following esophagectomy for cancer. Dis Esophagus. 2013;26(7):716–22.PubMedPubMedCentral
27.
go back to reference Kanda Y. Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant. 2013;48(3):452–8.CrossRefPubMed Kanda Y. Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant. 2013;48(3):452–8.CrossRefPubMed
28.
go back to reference Shah SP, Xu T, Hooker CM, et al. Why are patients being readmitted after surgery for esophageal cancer? J Thorac Cardiovasc Surg. 2015;149(5):1384–9.CrossRefPubMed Shah SP, Xu T, Hooker CM, et al. Why are patients being readmitted after surgery for esophageal cancer? J Thorac Cardiovasc Surg. 2015;149(5):1384–9.CrossRefPubMed
29.
go back to reference Honkoop P, Siersema PD, Tilanus HW, Stassen LP, Hop WC, van Blankenstein M. Benign anastomotic strictures after transhiatal esophagectomy and cervical esophagogastrostomy: risk factors and management. J Thorac Cardiovasc Surg. 1996;111(6):1141–7.CrossRefPubMed Honkoop P, Siersema PD, Tilanus HW, Stassen LP, Hop WC, van Blankenstein M. Benign anastomotic strictures after transhiatal esophagectomy and cervical esophagogastrostomy: risk factors and management. J Thorac Cardiovasc Surg. 1996;111(6):1141–7.CrossRefPubMed
30.
go back to reference van Heijl M, Gooszen JA, Fockens P, Busch OR, van Lanschot JJ, van Berge Henegouwen MI. Risk factors for development of benign cervical strictures after esophagectomy. Ann Surg. 2010;251(6):1064–9.CrossRefPubMed van Heijl M, Gooszen JA, Fockens P, Busch OR, van Lanschot JJ, van Berge Henegouwen MI. Risk factors for development of benign cervical strictures after esophagectomy. Ann Surg. 2010;251(6):1064–9.CrossRefPubMed
31.
go back to reference Huang Q, Zhong J, Yang T, et al. Impacts of anastomotic complications on the health-related quality of life after esophagectomy. J Surg Oncol. 2015;111(4):365–70.CrossRefPubMed Huang Q, Zhong J, Yang T, et al. Impacts of anastomotic complications on the health-related quality of life after esophagectomy. J Surg Oncol. 2015;111(4):365–70.CrossRefPubMed
32.
go back to reference Berry MF, Atkins BZ, Tong BC, Harpole DH, D’Amico TA, Onaitis MW. A comprehensive evaluation for aspiration after esophagectomy reduces the incidence of postoperative pneumonia. J Thorac Cardiovasc Surg. 2010;140(6):1266–71.CrossRefPubMedPubMedCentral Berry MF, Atkins BZ, Tong BC, Harpole DH, D’Amico TA, Onaitis MW. A comprehensive evaluation for aspiration after esophagectomy reduces the incidence of postoperative pneumonia. J Thorac Cardiovasc Surg. 2010;140(6):1266–71.CrossRefPubMedPubMedCentral
33.
go back to reference Cawthon PM, Fox KM, Gandra SR, et al. Do muscle mass, muscle density, strength, and physical function similarly influence risk of hospitalization in older adults? J Am Geriatr Soc. 2009;57(8):1411–9.CrossRefPubMedPubMedCentral Cawthon PM, Fox KM, Gandra SR, et al. Do muscle mass, muscle density, strength, and physical function similarly influence risk of hospitalization in older adults? J Am Geriatr Soc. 2009;57(8):1411–9.CrossRefPubMedPubMedCentral
34.
go back to reference Penninx B, Ferrucci L, Leveille SG, Rantanen T, Pahor M, Guralnik JM. Lower extremity performance in nondisabled older persons as a predictor of subsequent hospitalization. J Gerontol A Biol Sci Med Sci. 2000;55(11):M691–7.CrossRefPubMed Penninx B, Ferrucci L, Leveille SG, Rantanen T, Pahor M, Guralnik JM. Lower extremity performance in nondisabled older persons as a predictor of subsequent hospitalization. J Gerontol A Biol Sci Med Sci. 2000;55(11):M691–7.CrossRefPubMed
36.
go back to reference Levolger S, van Vugt JLA, de Bruin RWF, Ijzermans JNM. Systematic review of sarcopenia in patients operated on for gastrointestinal and hepatopancreatobiliary malignancies. Br J Surg. 2015;102(12):1448-58.CrossRefPubMed Levolger S, van Vugt JLA, de Bruin RWF, Ijzermans JNM. Systematic review of sarcopenia in patients operated on for gastrointestinal and hepatopancreatobiliary malignancies. Br J Surg. 2015;102(12):1448-58.CrossRefPubMed
37.
go back to reference Yip C, Goh V, Davies A, et al. Assessment of sarcopenia and changes in body composition after neoadjuvant chemotherapy and associations with clinical outcomes in oesophageal cancer. Eur Radiol. 2014;24(5):998–1005.CrossRefPubMed Yip C, Goh V, Davies A, et al. Assessment of sarcopenia and changes in body composition after neoadjuvant chemotherapy and associations with clinical outcomes in oesophageal cancer. Eur Radiol. 2014;24(5):998–1005.CrossRefPubMed
38.
go back to reference Daly JM, Fry WA, Little AG, Winchester DP, McKee RF, Stewart AK, et al. Esophageal cancer: results of an American College of Surgeons patient care evaluation study. J Am Coll Surg. 2000;190(5):562–72.CrossRefPubMed Daly JM, Fry WA, Little AG, Winchester DP, McKee RF, Stewart AK, et al. Esophageal cancer: results of an American College of Surgeons patient care evaluation study. J Am Coll Surg. 2000;190(5):562–72.CrossRefPubMed
39.
go back to reference Leong DP, Teo KK, Rangarajan S, et al. Prognostic value of grip strength: findings from the prospective urban rural epidemiology (PURE) study. Lancet. 2015;386(9990):266–73.CrossRefPubMed Leong DP, Teo KK, Rangarajan S, et al. Prognostic value of grip strength: findings from the prospective urban rural epidemiology (PURE) study. Lancet. 2015;386(9990):266–73.CrossRefPubMed
42.
go back to reference Bowrey DJ, Baker M, Halliday V, et al. A randomised controlled trial of 6 weeks of home enteral nutrition versus standard care after oesophagectomy or total gastrectomy for cancer: report on a pilot and feasibility study. Trials. 2015;16:531.CrossRefPubMedPubMedCentral Bowrey DJ, Baker M, Halliday V, et al. A randomised controlled trial of 6 weeks of home enteral nutrition versus standard care after oesophagectomy or total gastrectomy for cancer: report on a pilot and feasibility study. Trials. 2015;16:531.CrossRefPubMedPubMedCentral
Metadata
Title
Impact of Sarcopenia on Unplanned Readmission and Survival After Esophagectomy in Patients with Esophageal Cancer
Authors
Daisuke Makiura, PhD
Rei Ono, PhD
Junichiro Inoue, PhD
Akimasa Fukuta, RPT
Miyuki Kashiwa, MSc
Yasushi Miura, PhD
Taro Oshikiri, PhD
Tetsu Nakamura, PhD
Yoshihiro Kakeji, PhD
Yoshitada Sakai, PhD
Publication date
01-02-2018
Publisher
Springer International Publishing
Published in
Annals of Surgical Oncology / Issue 2/2018
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-017-6294-4

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