Pectoralis muscle area and mortality in smokers without airflow obstruction

Alejandro A Diaz, Carlos H Martinez, Rola Harmouche, Thomas P Young, Merry-Lynn McDonald, James C Ross, Mei Lan Han, Russell Bowler, Barry Make, Elizabeth A Regan, Edwin K Silverman, James Crapo, Aladin M Boriek, Gregory L Kinney, John E Hokanson, Raul San Jose Estepar, George R Washko, Alejandro A Diaz, Carlos H Martinez, Rola Harmouche, Thomas P Young, Merry-Lynn McDonald, James C Ross, Mei Lan Han, Russell Bowler, Barry Make, Elizabeth A Regan, Edwin K Silverman, James Crapo, Aladin M Boriek, Gregory L Kinney, John E Hokanson, Raul San Jose Estepar, George R Washko

Abstract

Background: Low muscle mass is associated with increased mortality in the general population but its prognostic value in at-risk smokers, those without expiratory airflow obstruction, is unknown. We aimed to test the hypothesis that reduced muscle mass is associated with increased mortality in at-risk smokers.

Methods: Measures of both pectoralis and paravertebral erector spinae muscle cross-sectional area (PMA and PVMA, respectively) as well as emphysema on chest computed tomography (CT) scans were performed in 3705 current and former at-risk smokers (≥10 pack-years) aged 45-80 years enrolled into the COPDGene Study between 2008 and 2013. Vital status was ascertained through death certificate. The association between low muscle mass and mortality was assessed using Cox regression analysis.

Results: During a median of 6.5 years of follow-up, 212 (5.7%) at-risk smokers died. At-risk smokers in the lowest (vs. highest) sex-specific quartile of PMA but not PVMA had 84% higher risk of death in adjusted models for demographics, smoking, dyspnea, comorbidities, exercise capacity, lung function, emphysema on CT, and coronary artery calcium content (hazard ratio [HR] 1.85 95% Confidence interval [1.14-3.00] P = 0.01). Results were consistent when the PMA index (PMA/height2) was used instead of quartiles. The association between PMA and death was modified by smoking status (P = 0.04). Current smokers had a significantly increased risk of death (lowest vs. highest PMA quartile, HR 2.25 [1.25-4.03] P = 0.007) while former smokers did not.

Conclusions: Low muscle mass as measured on chest CT scans is associated with increased mortality in current smokers without airflow obstruction.

Trial registration: NCT00608764.

Keywords: CT; Paravertebral muscle mass; Pectoralis muscle mass; Smoking.

Conflict of interest statement

Ethics approval and consent to participate

This study was approved by institutional review board of each of the 21 participating and all participants gave written informed consent. The Partners HealthCare Research Committee approved the current analysis (2007P-000554).

Consent for publication

Not applicable.

Competing interests

Drs. AD, CM, RH, MM, JR, MH, RB, BM, ER, ES, JC, AB, GK, JH, RSJ, and GW and Mr. TY have no conflict of interest related to this work. Dr. AD has received speaker fees from Novartis Inc. unrelated to this work.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Flowchart showing the subjects selection
Fig. 2
Fig. 2
Kaplan-Meier curves for all-cause mortality by sex-specific quartiles of pectoralis muscle area (PMA) in at-risk smokers. The survival probabilities decrease with decreasing PMA quartiles

References

    1. Jamal A, Homa DM, O'Connor E, Babb SD, Caraballo RS, Singh T, Hu SS, King BA. Current cigarette smoking among adults - United States, 2005-2014. MMWR Morb Mortal Wkly Rep. 2015;64(44):1233–1240. doi: 10.15585/mmwr.mm6444a2.
    1. Woodruff PG, Barr RG, Bleecker E, Christenson SA, Couper D, Curtis JL, Gouskova NA, Hansel NN, Hoffman EA, Kanner RE, et al. Clinical significance of symptoms in smokers with preserved pulmonary function. N Engl J Med. 2016;374(19):1811–1821. doi: 10.1056/NEJMoa1505971.
    1. Regan EA, Lynch DA, Curran-Everett D, Curtis JL, Austin JH, Grenier PA, Kauczor HU, Bailey WC, DeMeo DL, Casaburi RH, et al. Clinical and radiologic disease in smokers with normal spirometry. JAMA Intern Med. 2015;175(9):1539–1549. doi: 10.1001/jamainternmed.2015.2735.
    1. Rom O, Kaisari S, Aizenbud D, Reznick AZ. Sarcopenia and smoking: a possible cellular model of cigarette smoke effects on muscle protein breakdown. Ann N Y Acad Sci. 2012;1259:47–53. doi: 10.1111/j.1749-6632.2012.06532.x.
    1. Diaz AA, Morales A, Diaz JC, Ramos C, Klaassen J, Saldias F, Aravena C, Diaz R, Lisboa C, Washko GR, et al. CT and physiologic determinants of dyspnea and exercise capacity during the six-minute walk test in mild COPD. Respir Med. 2013;107(4):570–579. doi: 10.1016/j.rmed.2012.12.011.
    1. Kok MO, Hoekstra T, Twisk JW. The longitudinal relation between smoking and muscle strength in healthy adults. Eur Addict Res. 2012;18(2):70–75. doi: 10.1159/000333600.
    1. bvan den Borst B, Koster A, Yu B, Gosker HR, Meibohm B, Bauer DC, Kritchevsky SB, Liu Y, Newman AB, Harris TB, et al. Is age-related decline in lean mass and physical function accelerated by obstructive lung disease or smoking? Thorax. 2011;66(11):961–969. doi: 10.1136/thoraxjnl-2011-200010.
    1. Montes de Oca M, Loeb E, Torres SH, De Sanctis J, Hernandez N, Talamo C. Peripheral muscle alterations in non-COPD smokers. Chest. 2008;133(1):13–18. doi: 10.1378/chest.07-1592.
    1. Kim JH, Lim S, Choi SH, Kim KM, Yoon JW, Kim KW, Lim JY, Park KS, Jang HC. Sarcopenia: an independent predictor of mortality in community-dwelling older Korean men. J Gerontol A Biol Sci Med Sci. 2014;69(10):1244–1252. doi: 10.1093/gerona/glu050.
    1. Brown JC, Harhay MO, Harhay MN. Sarcopenia and mortality among a population-based sample of community-dwelling older adults. J Cachexia Sarcopenia Muscle. 2016;7(3):290–298. doi: 10.1002/jcsm.12073.
    1. Landi F, Liperoti R, Fusco D, Mastropaolo S, Quattrociocchi D, Proia A, Tosato M, Bernabei R, Onder G. Sarcopenia and mortality among older nursing home residents. J Am Med Dir Assoc. 2012;13(2):121–126. doi: 10.1016/j.jamda.2011.07.004.
    1. Batsis JA, Mackenzie TA, Barre LK, Lopez-Jimenez F, Bartels SJ. Sarcopenia, sarcopenic obesity and mortality in older adults: results from the National Health and nutrition examination survey III. Eur J Clin Nutr. 2014;68(9):1001–1007. doi: 10.1038/ejcn.2014.117.
    1. Vestbo J, Prescott E, Almdal T, Dahl M, Nordestgaard BG, Andersen T, Sorensen TI, Lange P. Body mass, fat-free body mass, and prognosis in patients with chronic obstructive pulmonary disease from a random population sample: findings from the Copenhagen City heart study. Am J Respir Crit Care Med. 2006;173(1):79–83.
    1. Maltais F, Decramer M, Casaburi R, Barreiro E, Burelle Y, Debigare R, Dekhuijzen PN, Franssen F, Gayan-Ramirez G, Gea J, et al. An official American Thoracic Society/European Respiratory Society statement: update on limb muscle dysfunction in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2014;189(9):e15–e62. doi: 10.1164/rccm.201402-0373ST.
    1. Soler-Cataluna JJ, Sanchez-Sanchez L, Martinez-Garcia MA, Sanchez PR, Salcedo E, Navarro M. Mid-arm muscle area is a better predictor of mortality than body mass index in COPD. Chest. 2005;128(4):2108–2115. doi: 10.1378/chest.128.4.2108.
    1. Gea J, Pascual S, Casadevall C, Orozco-Levi M, Barreiro E. Muscle dysfunction in chronic obstructive pulmonary disease: update on causes and biological findings. J Thorac Dis. 2015;7(10):E418–E438.
    1. Schols AM, Broekhuizen R, Weling-Scheepers CA, Wouters EF. Body composition and mortality in chronic obstructive pulmonary disease. Am J Clin Nutr. 2005;82(1):53–59. doi: 10.1093/ajcn/82.1.53.
    1. Psutka SP, Carrasco A, Schmit GD, Moynagh MR, Boorjian SA, Frank I, Stewart SB, Thapa P, Tarrell RF, Cheville JC, et al. Sarcopenia in patients with bladder cancer undergoing radical cystectomy: impact on cancer-specific and all-cause mortality. Cancer. 2014;120(18):2910–2918. doi: 10.1002/cncr.28798.
    1. Hronek M, Kovarik M, Aimova P, Koblizek V, Pavlikova L, Salajka F, Zadak Z. Skinfold anthropometry--the accurate method for fat free mass measurement in COPD. Copd. 2013;10(5):597–603. doi: 10.3109/15412555.2013.781151.
    1. Nyberg A, Saey D, Maltais F. Why and how limb muscle mass and function should be measured in patients with chronic obstructive pulmonary disease. Ann Am Thorac Soc. 2015;12(9):1269–1277. doi: 10.1513/AnnalsATS.201505-278PS.
    1. Jones SE, Maddocks M, Kon SS, Canavan JL, Nolan CM, Clark AL, Polkey MI, Man WD. Sarcopenia in COPD: prevalence, clinical correlates and response to pulmonary rehabilitation. Thorax. 2015;70(3):213–218. doi: 10.1136/thoraxjnl-2014-206440.
    1. McDonald ML, Diaz AA, Ross JC, San Jose Estepar R, Zhou L, Regan EA, Eckbo E, Muralidhar N, Come CE, Cho MH, et al. Quantitative computed tomography measures of pectoralis muscle area and disease severity in chronic obstructive pulmonary disease. A cross-sectional study. Ann Am Thor Soc. 2014;11(3):326–334. doi: 10.1513/AnnalsATS.201307-229OC.
    1. Tanimura K, Sato S, Fuseya Y, Hasegawa K, Uemasu K, Sato A, Oguma T, Hirai T, Mishima M, Muro S. Quantitative assessment of erector spinae muscles in patients with chronic obstructive pulmonary disease. Novel chest computed tomography-derived index for prognosis. Ann Am Thor Soc. 2016;13(3):334–341. doi: 10.1513/AnnalsATS.201507-446OC.
    1. Marquis K, Debigare R, Lacasse Y, LeBlanc P, Jobin J, Carrier G, Maltais F. Midthigh muscle cross-sectional area is a better predictor of mortality than body mass index in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2002;166(6):809–813. doi: 10.1164/rccm.2107031.
    1. Martinez CH, Diaz AA, Meldrum CA, McDonald MN, Murray S, Kinney GL, Hokanson JE, Curtis JL, Bowler RP, Han MK, et al. Handgrip strength in chronic obstructive pulmonary disease. Associations with acute exacerbations and body composition. Ann Am Thor Soc. 2017;14(11):1638–1645. doi: 10.1513/AnnalsATS.201610-821OC.
    1. McDonald MN, Diaz AA, Rutten E, Lutz SM, Harmouche R, San Jose Estepar R, Kinney G, Hokanson JE, Gower BA, Wouters EFM et al: Chest computed tomography-derived low fat-free mass index and mortality in COPD. Eur Respir J. 2017;50(6).
    1. Diaz AA, Zhou L, Young TP, McDonald ML, Harmouche R, Ross JC, San Jose Estepar R, Wouters EF, Coxson HO, MacNee W, et al. Chest CT measures of muscle and adipose tissue in COPD: gender-based differences in content and in relationships with blood biomarkers. Acad Radiol. 2014;21(10):1255–1261. doi: 10.1016/j.acra.2014.05.013.
    1. Regan EA, Hokanson JE, Murphy JR, Make B, Lynch DA, Beaty TH, Curran-Everett D, Silverman EK, Crapo JD. Genetic epidemiology of COPD (COPDGene) study design. Copd. 2010;7(1):32–43. doi: 10.3109/15412550903499522.
    1. Diaz AA, Come CE, Ross JC, San Jose Estepar R, Han MK, Loring SH, Silverman EK, Washko GR. Association between airway caliber changes with lung inflation and emphysema assessed by volumetric CT scan in subjects with COPD. Chest. 2012;141(3):736–744. doi: 10.1378/chest.11-1026.
    1. Gevenois PA, De Vuyst P, de Maertelaer V, Zanen J, Jacobovitz D, Cosio MG, Yernault JC. Comparison of computed density and microscopic morphometry in pulmonary emphysema. Am J Respir Crit Care Med. 1996;154(1):187–192. doi: 10.1164/ajrccm.154.1.8680679.
    1. Budoff MJ, Nasir K, Kinney GL, Hokanson JE, Barr RG, Steiner R, Nath H, Lopez-Garcia C, Black-Shinn J, Casaburi R. Coronary artery and thoracic calcium on noncontrast thoracic CT scans: comparison of ungated and gated examinations in patients from the COPD gene cohort. J Cardiovasc Comput Tomogr. 2011;5(2):113–118. doi: 10.1016/j.jcct.2010.11.002.
    1. Budoff MJ, Gul KM. Expert review on coronary calcium. Vasc Health Risk Manag. 2008;4(2):315–324. doi: 10.2147/VHRM.S1160.
    1. McClelland RL, Chung H, Detrano R, Post W, Kronmal RA. Distribution of coronary artery calcium by race, gender, and age: results from the multi-ethnic study of atherosclerosis (MESA) Circulation. 2006;113(1):30–37. doi: 10.1161/CIRCULATIONAHA.105.580696.
    1. Williams MC, Murchison JT, Edwards LD, Agusti A, Bakke P, Calverley PM, Celli B, Coxson HO, Crim C, Lomas DA, et al. Coronary artery calcification is increased in patients with COPD and associated with increased morbidity and mortality. Thorax. 2014;69(8):718–723. doi: 10.1136/thoraxjnl-2012-203151.
    1. Agatston AS, Janowitz WR, Hildner FJ, Zusmer NR, Viamonte M, Jr, Detrano R. Quantification of coronary artery calcium using ultrafast computed tomography. J Am Coll Cardiol. 1990;15(4):827–832. doi: 10.1016/0735-1097(90)90282-T.
    1. Diaz AA, Hardin ME, Come CE, San Jose Estepar R, Ross JC, Kurugol S, Okajima Y, Han MK, Kim V, Ramsdell J, et al. Childhood-onset asthma in smokers. Association between CT measures of airway size, lung function, and chronic airflow obstruction. Ann Am Thor Soc. 2014;11(9):1371–1378. doi: 10.1513/AnnalsATS.201403-095OC.
    1. Putcha N, Puhan MA, Hansel NN, Drummond MB, Boyd CM. Impact of co-morbidities on self-rated health in self-reported COPD: an analysis of NHANES 2001-2008. Copd. 2013;10(3):324–332. doi: 10.3109/15412555.2012.744963.
    1. Romero-Corral A, Montori VM, Somers VK, Korinek J, Thomas RJ, Allison TG, Mookadam F, Lopez-Jimenez F. Association of bodyweight with total mortality and with cardiovascular events in coronary artery disease: a systematic review of cohort studies. Lancet. 2006;368(9536):666–678. doi: 10.1016/S0140-6736(06)69251-9.
    1. ATS statement: guidelines for the six-minute walk test. Am J Respir Crit Care Med. 2002;166(1):111–117.
    1. Standardization of Spirometry, 1994 Update. American Thoracic Society. Am J Respir Crit Care Med 1995, 152(3):1107–1136.
    1. 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(1):179–187. doi: 10.1164/ajrccm.159.1.9712108.
    1. Rabe KF, Hurd S, Anzueto A, Barnes PJ, Buist SA, Calverley P, Fukuchi Y, Jenkins C, Rodriguez-Roisin R, van Weel C, et al. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary. Am J Respir Crit Care Med. 2007;176(6):532–555. doi: 10.1164/rccm.200703-456SO.
    1. Chang SF, Lin PL. Systematic literature review and meta-analysis of the Association of Sarcopenia with Mortality. Worldviews Evid-Based Nurs. 2016;13(2):153–162. doi: 10.1111/wvn.12147.
    1. Oelsner EC, Hoffman EA, Folsom AR, Carr JJ, Enright PL, Kawut SM, Kronmal R, Lederer D, Lima JA, Lovasi GS, et al. Association between emphysema-like lung on cardiac computed tomography and mortality in persons without airflow obstruction: a cohort study. Ann Intern Med. 2014;161(12):863–873. doi: 10.7326/M13-2570.
    1. Russ DW, Gregg-Cornell K, Conaway MJ, Clark BC. Evolving concepts on the age-related changes in "muscle quality". J Cachexia Sarcopenia Muscle. 2012;3(2):95–109. doi: 10.1007/s13539-011-0054-2.
    1. Delmonico MJ, Harris TB, Visser M, Park SW, Conroy MB, Velasquez-Mieyer P, Boudreau R, Manini TM, Nevitt M, Newman AB, et al. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr. 2009;90(6):1579–1585. doi: 10.3945/ajcn.2009.28047.

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