Low Muscle Mass and Radiodensity Associate with Impaired Pulmonary Function and Respiratory Complications in Patients with Esophageal Cancer.


Journal

Journal of the American College of Surgeons
ISSN: 1879-1190
Titre abrégé: J Am Coll Surg
Pays: United States
ID NLM: 9431305

Informations de publication

Date de publication:
01 04 2023
Historique:
pmc-release: 01 04 2024
pubmed: 3 2 2023
medline: 17 3 2023
entrez: 2 2 2023
Statut: ppublish

Résumé

Sixty percent of patients with esophageal cancer display signs of cachexia at diagnosis. Changes in body composition are common, and muscle mass and quality are measurable through imaging studies. Cachexia leads to functional impairments that complicate treatments, including surgery. We hypothesize that low muscle mass and quality associate with pulmonary function testing parameters, highlighting ventilatory deficits, and postoperative complications in patients receiving esophagectomy. We performed a retrospective review of patients receiving esophagectomy between 2012 and 2021 at our facility. PET/CT scans were used to quantify skeletal muscle at the L3 and T4 levels. Patient characteristics were recorded, including pulmonary function testing parameters. Regression models were created to characterize predictive associations. One hundred eight patients were identified. All were included in the final analysis. In linear regression adjusted for sex, age, and COPD status, low L3 muscle mass independently associated with low forced vital capacity (p < 0.005, β 0.354) and forced expiratory volume in 1 second (p < 0.001, β 0.392). Similarly, T4 muscle mass independently predicted forced vital capacity (p < 0.005, β 0.524) and forced expiratory volume in 1 second (p < 0.01, β 0.480). L3 muscle quality correlated with total lung capacity ( R 0.2463, p < 0.05). Twenty-six patients had pleural effusions postoperatively, associated with low muscle quality on L3 images (p < 0.05). Similarly, patients with hospitalization more than 2 weeks presented with lower muscle quality (p < 0.005). Cachexia and low muscle mass are common. Reduced muscle mass and quality independently associate with impaired forced vital capacity, forced expiratory volume in 1 second, and total lung capacity. We propose that respiratory muscle atrophy occurs with weight loss. Body composition analyses may aid in stratifying patients. Pulmonary function testing may also serve as a functional endpoint for clinical trials. These findings highlight the need to study mechanisms that lead to respiratory muscle pathology and dysfunction in tumor-bearing hosts.

Sections du résumé

BACKGROUND
Sixty percent of patients with esophageal cancer display signs of cachexia at diagnosis. Changes in body composition are common, and muscle mass and quality are measurable through imaging studies. Cachexia leads to functional impairments that complicate treatments, including surgery. We hypothesize that low muscle mass and quality associate with pulmonary function testing parameters, highlighting ventilatory deficits, and postoperative complications in patients receiving esophagectomy.
STUDY DESIGN
We performed a retrospective review of patients receiving esophagectomy between 2012 and 2021 at our facility. PET/CT scans were used to quantify skeletal muscle at the L3 and T4 levels. Patient characteristics were recorded, including pulmonary function testing parameters. Regression models were created to characterize predictive associations.
RESULTS
One hundred eight patients were identified. All were included in the final analysis. In linear regression adjusted for sex, age, and COPD status, low L3 muscle mass independently associated with low forced vital capacity (p < 0.005, β 0.354) and forced expiratory volume in 1 second (p < 0.001, β 0.392). Similarly, T4 muscle mass independently predicted forced vital capacity (p < 0.005, β 0.524) and forced expiratory volume in 1 second (p < 0.01, β 0.480). L3 muscle quality correlated with total lung capacity ( R 0.2463, p < 0.05). Twenty-six patients had pleural effusions postoperatively, associated with low muscle quality on L3 images (p < 0.05). Similarly, patients with hospitalization more than 2 weeks presented with lower muscle quality (p < 0.005).
CONCLUSIONS
Cachexia and low muscle mass are common. Reduced muscle mass and quality independently associate with impaired forced vital capacity, forced expiratory volume in 1 second, and total lung capacity. We propose that respiratory muscle atrophy occurs with weight loss. Body composition analyses may aid in stratifying patients. Pulmonary function testing may also serve as a functional endpoint for clinical trials. These findings highlight the need to study mechanisms that lead to respiratory muscle pathology and dysfunction in tumor-bearing hosts.

Identifiants

pubmed: 36728466
doi: 10.1097/XCS.0000000000000535
pii: 00019464-202304000-00026
pmc: PMC10023327
mid: NIHMS1862442
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

677-684

Subventions

Organisme : NIAMS NIH HHS
ID : R01 AR060209
Pays : United States

Informations de copyright

Copyright © 2023 by the American College of Surgeons. Published by Wolters Kluwer Health, Inc. All rights reserved.

Références

Rosemurgy A, Wilfong C, Craigg D, et al. The evolving landscape of esophageal cancer: a four-decade analysis. Am Surg 2019;85:944–948.
Trivers KF, Sabatino SA, Stewart SL. Trends in esophageal cancer incidence by histology, United States, 1998-2003. Int J Cancer 2008;123:1422–1428.
National Cancer Institute. Esophageal cancer. Available at: http://www.cancer.gov/pediatric-adult-rare-tumor/rare-tumors/rare-digestive-system-tumors/esophageal . Accessed November 30, 2022.
Eyck BM, van Lanschot JJB, Hulshof MCCM, et al. Ten-year outcome of neoadjuvant chemoradiotherapy plus surgery for esophageal cancer: the randomized controlled CROSS trial. J Clin Oncol 2021;39:1995–2004.
Mboumi IW, Reddy S, Lidor AO. Complications after esophagectomy. Surg Clin North Am 2019;99:501–510.
Atkins BZ, D’Amico TA. Respiratory complications after esophagectomy. Thorac Surg Clin 2006;16:35–48.
Colcord ME, Benbow JH, Trufan S, et al. Preoperative muscle strength is a predictor of outcomes after esophagectomy. J Gastrointest Surg 2021;25:3040–3048.
Avendano CE, Flume PA, Silvestri GA, et al. Pulmonary complications after esophgectomy. Ann Thorac Surg 2002;73:922–926.
Murayama S, Okamura A, Ishizuka N, et al. Airflow limitation predicts postoperative pneumonia after esophagectomy. World J Surg 2021;45:2492–2500.
Sugawara K, Mori K, Okumura Y, et al. Preoperative low vital capacity influences survival after esophagectomy for patients with esophageal carcinoma. World J Surg 2020;44:2305–2313.
Baracos VE, Martin L, Korc M, et al. Cancer-associated cachexia. Nat Rev Dis Primers 2018;18:17105.
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;9:629–635.
Fehrenbach U, Wuensch T, Gabriel P, et al. CT body composition of sarcopenia and sarcopenic obesity: predictors of postoperative complications and survival in patients with locally advanced esophageal adenocarcinoma. Cancers (Basel) 2021;13:2921.
Baracos VE, Arribas L. Sarcopenic obesity: hidden muscle wasting and its impact for survival and complications of cancer therapy. Ann Oncol 2018;29:ii1–ii9.
McDonald JJ, Fallon MT, Laird BJA. Meaningful measures in cancer cachexia: implications for practice and research. Curr Opin Support Palliat Care 2019;13:323–327.
Blauwhoff-Buskermolen S, Langius JAE, Becker A, et al. The influence of different muscle mass measurements on the diagnosis of cancer cachexia. J Cachexia Sarcopenia Muscle 2017;8:615–622.
Hagens ERC, Feenstra ML, van Egmond MA, et al. Influence of body composition and muscle strength on outcomes after multimodal oesophageal cancer treatment. J Cachexia Sarcopenia Muscle 2020;11:756–767.
Aubrey J, Esfandiari N, Baracos VE, et al. Measurement of skeletal muscle radiation attenuation and basis of its biological variation. Acta Physiol (Oxf) 2014;210:489–497.
Srpcic M, Jordan T, Popuri K, Sok M. Sarcopenia and myosteatosis at presentation adversely affect survival after esophagectomy for esophageal cancer. Radiol Oncol 2020;54:237–246.
Judge SM, Nosacka RL, Delitto D, et al. Skeletal muscle fibrosis in pancreatic cancer patients with respect to survival. JNCI Cancer Spectr 2018;2:pky043.
Shirai H, Kaido T, Hamaguchi Y, et al. Preoperative low muscle mass and low muscle quality negatively impact pulmonary function in patients undergoing hepatectomy for hepatocellular carcinoma. Liver Cancer 2018;7:76–89.
Mishra A, Bigam KD, Extermann M, et al. Sarcopenia and low muscle radiodensity associate with impaired FEV 1 in allogeneic haematopoietic stem cell transplant recipients. J Cachexia Sarcopenia Muscle 2020;11:1570–1579.
Roberts BM, Ahn B, Smuder AJ, et al. Diaphragm and ventilatory dysfunction during cancer cachexia. FASEB J 2013;27:2600–2610.
Fields DP, Roberts BM, Simon AK, et al. Cancer cachexia impairs neural respiratory drive in hypoxia but not hypercapnia. J Cachexia Sarcopenia Muscle 2019;10:63–72.
Hankinson JL, Odencrantz JR, Fedan KB. Spirometric reference values from a sample of the general U.S. population. Am J Respir Crit Care Med 1999;159:179–187.
BMJ Best Practice. Global Initiative for Chronic Obstructive Lung Disease (GOLD) criteria. Available at: http://bestpractice.bmj.com/topics/en-us/7 . Accessed November 30, 2022.
Cameron ME, Underwood PW, Williams IE, et al. Osteopenia is associated with wasting in pancreatic adenocarcinoma and predicts survival after surgery. Cancer Med 2022;11:50–60.
Rigiroli F, Zhang D, Molinger J, et al. Automated versus manual analysis of body composition measures on computed tomography in patients with bladder cancer. Eur J Radiol 2022;154:110413.
Shen W, Punyanitya M, Wang Z, et al. Visceral adipose tissue: relations between single-slice areas and total volume. Am J Clin Nutr 2004;80:271–278.
Martin L, Senesse P, Gioulbasanis I, et al. Diagnostic criteria for the classification of cancer-associated weight loss. J Clin Oncol 2015;33:90–99.
Nambura M, Miki Y, Tamura T, et al. The optimal definition of sarcopenia for predicting postoperative pneumonia after esophagectomy in patients with esophageal cancer. World J Surg 2021;45:3108–3118.
Harada T, Tatematsu N, Ueno J, et al. Prognostic impact of postoperative loss of skeletal muscle mass in patients aged 70 years of older with esophageal cancer. Ann Surg Oncol 2022;29:5638–5645.
Nagata K, Tsujimoto H, Nagata H, et al. Impact of reduced skeletal muscle volume on clinical outcome after esophagectomy for esophageal cancer: a retrospective study. Medicine (Baltimore) 2018;97:e11450.
Murnane LC, Forsyth AK, Koukounaras J, et al. Low muscularity increases the risk for post-operative pneumonia and delays recovery from complications after oesophago-gastric cancer resection. ANZ J Surg 2021;91:2683–2689.
Pin F, Barreto R, Couch ME, et al. Cachexia induced by cancer and chemotherapy yield distinct perturbations to energy metabolism. J Cachexia Sarcopenia Muscle 2019;10:140–154.
VanderVeen BN, Cardaci TD, Madero SS, et al. 5-Fluorouracil disrupts skeletal muscle immune cells and impairs skeletal muscle repair and remodeling. J Appl Physiol (1985) 2022;133:834–849.
de Jong C, Chargi N, Herder GJM, et al. The association between skeletal muscle measures and chemotherapy-induced toxicity in non-small cell lung cancer patients. J Cachexia Sarcopenia Muscle 2022;13:1554–1564.

Auteurs

Miles E Cameron (ME)

From the Department of Physical Therapy (Cameron, SM Judge, AR Judge), University of Florida, Gainesville, FL.
MD-PhD Training Program (Cameron), University of Florida, Gainesville, FL.

Alexander L Ayzengart (AL)

the Department of Surgery, University of Nevada, Reno, NV (Ayzengart).
Nevada Surgical Associates, Reno, NV (Ayzengart).

Olusola Oduntan (O)

Department of Surgery (Oduntan), University of Florida, Gainesville, FL.

Sarah M Judge (SM)

From the Department of Physical Therapy (Cameron, SM Judge, AR Judge), University of Florida, Gainesville, FL.

Andrew R Judge (AR)

From the Department of Physical Therapy (Cameron, SM Judge, AR Judge), University of Florida, Gainesville, FL.

Ziad T Awad (ZT)

the Department of Surgery, University of Florida, Jacksonville, FL (Awad).

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