Association of smoking with abdominal adipose deposition and muscle composition in Coronary Artery Risk Development in Young Adults (CARDIA) participants at mid-life: A population-based cohort study
Autoři:
James G. Terry aff001; Katherine G. Hartley aff001; Lyn M. Steffen aff002; Sangeeta Nair aff001; Amy C. Alman aff003; Melissa F. Wellons aff001; David R. Jacobs, Jr. aff002; Hilary A. Tindle aff001; John Jeffrey Carr aff001
Působiště autorů:
Vanderbilt University Medicine Center, Nashville, Tennessee
aff001; University of Minnesota School of Public Health, Minneapolis, Minnesota
aff002; University of South Florida, Tampa, Florida
aff003; Geriatric Research Education and Clinical Centers (GRECC), Veterans Affairs Tennessee Valley Healthcare System, Nashville, Tennessee
aff004
Vyšlo v časopise:
Association of smoking with abdominal adipose deposition and muscle composition in Coronary Artery Risk Development in Young Adults (CARDIA) participants at mid-life: A population-based cohort study. PLoS Med 17(7): e32767. doi:10.1371/journal.pmed.1003223
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pmed.1003223
Souhrn
Background
Smokers have lower risk of obesity, which some consider a “beneficial” side effect of smoking. However, some studies suggest that smoking is simultaneously associated with higher central adiposity and, more specifically, ectopic adipose deposition. Little is known about the association of smoking with intermuscular adipose tissue (IMAT), an ectopic adipose depot associated with cardiovascular disease (CVD) risk and a key determinant of muscle quality and function. We tested the hypothesis that smokers have higher abdominal IMAT and lower lean muscle quality than never smokers.
Methods and findings
We measured abdominal muscle total, lean, and adipose volumes (in cubic centimeters) and attenuation (in Hounsfield units [HU]) along with subcutaneous (SAT) and visceral adipose tissue (VAT) volumes using computed tomography (CT) in 3,020 middle-aged Coronary Artery Risk Development in Young Adults (CARDIA) participants (age 42–58, 56.3% women, 52.6% white race) at the year 25 (Y25) visit. The longitudinal CARDIA study was initiated in 1985 with the recruitment of young adult participants (aged 18–30 years) equally balanced by female and male sex and black and white race at 4 field centers located in Birmingham, AL, Chicago, IL, Minneapolis, MN, and Oakland, CA. Multivariable linear models included potential confounders such as physical activity and dietary habits along with traditional CVD risk factors. Current smokers had lower BMI than never smokers. Nevertheless, in the fully adjusted multivariable model with potential confounders, including BMI and CVD risk factors, adjusted mean (95% CI) IMAT volume was 2.66 (2.55–2.76) cm3 in current smokers (n = 524), 2.36 (2.29–2.43) cm3 in former smokers (n = 944), and 2.23 (2.18–2.29) cm3 in never smokers (n = 1,552) (p = 0.007 for comparison of former versus never smoker, and p < 0.001 for comparison of current smoker versus never and former smoker). Moreover, compared to participants who never smoked throughout life (41.6 [41.3–41.9] HU), current smokers (40.4 [39.9–40.9] HU) and former smokers (40.8 [40.5–41.2] HU) had lower lean muscle attenuation suggesting lower muscle quality in the fully adjusted model (p < 0.001 for comparison of never smokers with either of the other two strata). Among participants who had ever smoked, pack-years of smoking exposure were directly associated with IMAT volume (β [95% CI]: 0.017 [0.010–0.025]) (p < 0.001). Despite having less SAT, current smokers also had higher VAT/SAT ratio than never smokers. These findings must be viewed with caution as residual confounding and/or reverse causation may contribute to these associations.
Conclusions
We found that, compared to those who never smoked, current and former smokers had abdominal muscle composition that was higher in adipose tissue volume, a finding consistent with higher CVD risk and age-related physical deconditioning. These findings challenge the belief that smoking-associated weight loss or maintenance confers a health benefit.
Klíčová slova:
Abdominal muscles – Adipose tissue – Computed axial tomography – diabetes mellitus – Fats – Muscle analysis – Muscle tissue – Smoking habits
Zdroje
1. Boyd TC, Boyd CJ, Greenlee TB. A Means to an End: Slim Hopes and Cigarette Advertising. Health Educ. 2003; 4(3):266–77. doi: 10.1177/1524839903004003011 14610997
2. O’Keefe AM, Pollay RW. Deadly targeting of women in promoting cigarettes. Vol. 51, Journal-American Medical Womens Association. 1996. p. 67–69. [cited 2019 Dec 1]. Available from: http://www.columbia.edu/itc/hs/pubhealth/p9740/readings/okeefe.pdf.
3. Report MW. Women and smoking: a report of the Surgeon General. Executive summary. MMWR Recomm reports Morb Mortal Wkly report Recomm reports. 2002;51(RR-12):i–iv; 1–13. http://www.ncbi.nlm.nih.gov/pubmed/12222832
4. Meyers AW, Klesges RC, Winders SE, Ward KD, Peterson BA, Eck LH. Are weight concerns predictive of smoking cessation? A prospective analysis. J Consult Clin Psychol. 1997;65(3):448–52. doi: 10.1037//0022-006x.65.3.448 9170768
5. Dare S, Mackay DF, Pell JP. Relationship between Smoking and Obesity: A Cross-Sectional Study of 499,504 Middle-Aged Adults in the UK General Population. PLoS ONE. 2015;10(4):1–12. https://doi.org/10.1371/journal.pone.0123579
6. Travier N, Agudo A, May AM, Gonzalez C, Luan J, Wareham NJ, et al. Longitudinal changes in weight in relation to smoking cessation in participants of the EPIC-PANACEA study. Prev Med (Baltim). 2012;54(3):183–92. http://www.sciencedirect.com/science/article/pii/S0091743511003641
7. Aubin HJ, Farley A, Lycett D, Lahmek P, Aveyard P. Weight gain in smokers after quitting cigarettes: Meta-analysis. BMJ. 2012;345(7868):1–21.
8. Tian J, Venn A, Otahal P, Gall S. The association between quitting smoking and weight gain: a systemic review and meta-analysis of prospective cohort studies. Obes Rev. 2015 Oct;16(10):883–901. doi: 10.1111/obr.12304 26114839
9. Canoy D, Wareham N, Luben R, Welch A, Bingham S, Day N, et al. Cigarette smoking and fat distribution in 21,828 British men and women: a population-based study. Obes Res. 2005;13(8):1466–75. http://www.ncbi.nlm.nih.gov/pubmed/16129730%5Cnhttp://onlinelibrary.wiley.com/store/10.1038/oby.2005.177/asset/oby.2005.177.pdf?v=1&t=irjz2l17&s=55431dd59761c83c07cc4fa5d73e311f2de61ada doi: 10.1038/oby.2005.177 16129730
10. Morris RW, Taylor AE, Fluharty ME, Bjorngaard JH, Asvold BO, Elvestad Gabrielsen M, et al. Heavier smoking may lead to a relative increase in waist circumference: evidence for a causal relationship from a Mendelian randomisation meta-analysis. The CARTA consortium. BMJ Open. 2015 Aug;5(8):e008808. doi: 10.1136/bmjopen-2015-008808 26264275
11. Després J-P. Body fat distribution and risk of cardiovascular disease: an update. Circulation. 2012 Sep. 126(10):1301–13. http://www.ncbi.nlm.nih.gov/pubmed/22949540 doi: 10.1161/CIRCULATIONAHA.111.067264 22949540
12. Ding J, Kritchevsky SB, Hsu F-C, Harris TB, Burke GL, Detrano RC, et al. Association between non-subcutaneous adiposity and calcified coronary plaque: a substudy of the Multi-Ethnic Study of Atherosclerosis. Am J Clin Nutr. 2008 Sep 1. 88(3):645–50. http://ajcn.nutrition.org/cgi/content/long/88/3/645 doi: 10.1093/ajcn/88.3.645 18779279
13. Ding J, Hsu F-C, Harris TB, Liu Y, Kritchevsky SB, Szklo M, et al. The association of pericardial fat with incident coronary heart disease: the Multi-Ethnic Study of Atherosclerosis (MESA). Am J Clin Nutr. 2009 Sep 1. 90(3):499–504. http://ajcn.nutrition.org/cgi/content/long/90/3/499 doi: 10.3945/ajcn.2008.27358 19571212
14. Abraham TM, Pedley A, Massaro JM, Hoffmann U, Fox CS. Association between visceral and subcutaneous adipose depots and incident cardiovascular disease risk factors. Circulation. 2015;132(17):1639–47. doi: 10.1161/CIRCULATIONAHA.114.015000 26294660
15. Alman AC, Jacobs DRJ, Lewis CE, Snell-Bergeon JK, Carnethon MR, Terry JG, et al. Higher pericardial adiposity is associated with prevalent diabetes: The Coronary Artery Risk Development in Young Adults study. Nutr Metab Cardiovasc Dis. 2016 Apr;26(4):326–32. doi: 10.1016/j.numecd.2015.12.011 26803596
16. Terry JG, Shay CM, Schreiner PJ, Jacobs DRJ, Sanchez OA, Reis JP, et al. Intermuscular Adipose Tissue and Subclinical Coronary Artery Calcification in Midlife: The CARDIA Study (Coronary Artery Risk Development in Young Adults). Arterioscler Thromb Vasc Biol. 2017 Dec;37(12):2370–8. doi: 10.1161/ATVBAHA.117.309633 29025708
17. VanWagner LB, Ning H, Lewis CE, Shay CM, Wilkins J, Carr JJ, et al. Associations between nonalcoholic fatty liver disease and subclinical atherosclerosis in middle-aged adults: the Coronary Artery Risk Development in Young Adults Study. Atherosclerosis. 2014 Aug;235(2):599–605. doi: 10.1016/j.atherosclerosis.2014.05.962 24956534
18. Granados A, Gebremariam A, Gidding SS, Terry JG, Carr JJ, Steffen LM, et al. Association of abdominal muscle composition with prediabetes and diabetes: The CARDIA study. Diabetes, Obes Metab. 2018;(August):1–9.
19. Miljkovic I, Kuipers AL, Cauley JA, Prasad T, Lee CG, Ensrud KE, et al. Greater Skeletal Muscle Fat Infiltration Is Associated With Higher All-Cause and Cardiovascular Mortality in Older Men. Journals Gerontol Ser A Biol Sci Med Sci. 2015 Apr 2; http://biomedgerontology.oxfordjournals.org/content/early/2015/04/01/gerona.glv027.abstract
20. Kim JH, Shim KW, Yoon YS, Lee SY, Kim SS, Oh SW. Cigarette Smoking Increases Abdominal and Visceral Obesity but Not Overall Fatness: An Observational Study. PLoS ONE. 2012;7(9):1–5. https://doi.org/10.1371/journal.pone.0045815
21. Nakanishi K, Nishida M, Ohama T, Moriyama T, Yamauchi-Takihara K. Smoking associates with visceral fat accumulation especially in women. Circ J. 2014;78(5):1259–63. doi: 10.1253/circj.cj-13-1134 24621566
22. Onat A, Ayhan E, Hergenç G, Can G, Barlan MM. Smoking inhibits visceral fat accumulation in Turkish women: Relation of visceral fat and body fat mass to atherogenic dyslipidemia, inflammatory markers, insulin resistance, and blood pressure. Metabolism. 2009;58(7):963–70. http://www.sciencedirect.com/science/article/pii/S0026049509000924 doi: 10.1016/j.metabol.2009.02.029 19411085
23. Molenaar EA, Massaro JM, Jacques PF, Pou KM, Ellison RC, Hoffmann U, et al. Association of Lifestyle Factors With Abdominal Subcutaneous and Visceral Adiposity. Diabetes Care. 2009 Feb 26;32(3):505 LP–510. http://care.diabetesjournals.org/content/32/3/505.abstract
24. Dennison EM, Sayer AA, Cooper C. Epidemiology of sarcopenia and insight into possible therapeutic targets. Nat Rev Rheumatol. 2017 Jun;13(6):340–7. doi: 10.1038/nrrheum.2017.60 28469267
25. Follis S, Cook A, Bea JW, Going SB, Laddu D, Cauley JA, et al. Association Between Sarcopenic Obesity and Falls in a Multiethnic Cohort of Postmenopausal Women. J Am Geriatr Soc. 2018;1–7. http://doi.wiley.com/10.1111/jgs.15613
26. Szulc P, Duboeuf F, Marchand F, Delmas PD. Hormonal and lifestyle determinants of appendicular skeletal muscle mass in men: the MINOS study. Am J Clin Nutr. 2004 Aug;80(2):496–503. doi: 10.1093/ajcn/80.2.496 15277176
27. Castillo EM, Goodman-Gruen D, Kritz-Silverstein D, Morton DJ, Wingard DL, Barrett-Connor E. Sarcopenia in elderly men and women: The Rancho Bernardo study. Am J Prev Med. 2003;25(3):226–31. doi: 10.1016/s0749-3797(03)00197-1 14507529
28. Ma J, Fox CS, Jacques PF, Speliotes EK, Hoffmann U, Smith CE, et al. Sugar-sweetened beverage, diet soda, and fatty liver disease in the Framingham Heart Study cohorts. J Hepatol. 2015 Aug;63(2):462–9. doi: 10.1016/j.jhep.2015.03.032 26055949
29. Larsen BA, Allison MA, Kang E, Saad S, Laughlin GA, Araneta MRG, et al. Associations of physical activity and sedentary behavior with regional fat deposition. Med Sci Sports Exerc. 2014 Mar;46(3):520–8. doi: 10.1249/MSS.0b013e3182a77220 23924920
30. Liu J, Hickson DA, Musani SK, Talegawkar SA, Carithers TC, Tucker KL, et al. Dietary Patterns, Abdominal Visceral Adipose Tissue and Cardiometabolic Risk Factors in African Americans: the Jackson Heart Study. Obesity (Silver Spring). 2013 Mar;21(3):doi: 10.1002/oby.20265 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3478414/ 23592674
31. Friedman GD, Cutter GR, Donahue RP, Hughes GH, Hulley SB, Jacobs DRJ, et al. CARDIA: study design, recruitment, and some characteristics of the examined subjects. J Clin Epidemiol. 1988;41(11):1105–16. doi: 10.1016/0895-4356(88)90080-7 3204420
32. Wagenknecht LE, Burke GL, Perkins LL, Haley NJ, Friedman GD. Misclassification of smoking status in the CARDIA study: A comparison of self-report with serum cotinine levels. Am J Public Health. 1992;82(1):33–6. doi: 10.2105/ajph.82.1.33 1536331
33. Wagenknecht LE, Cutter GR, Haley NJ, Sidney S, Manolio TA, Hughes GH, et al. Racial differences in serum cotinine levels among smokers in the Coronary Artery Risk Development in (Young) Adults study. Am J Public Health. 1990 Sep;80(9):1053–6. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1404871/ doi: 10.2105/ajph.80.9.1053 2382740
34. Jarvis MJ, Tunstall-Pedoe H, Feyerabend C, Vesey C, Saloojee Y. Comparison of tests used to distinguish smokers from nonsmokers. Am J Public Health. 1987;77(11):1435–8. doi: 10.2105/ajph.77.11.1435 3661797
35. Cummings SR, Richard RJ. Optimum cutoff points for biochemical validation of smoking status. Am J Public Health. 1988 May;78(5):574–5. https://www.ncbi.nlm.nih.gov/pubmed/3354745 doi: 10.2105/ajph.78.5.574 3354745
36. Jacobs DR, Hahn LP, Haskell WL, Pirie P, Sidney S. Validity and Reliability of Short Physical Activity History: Cardia and the Minnesota Heart Health Program. J Cardiopulm Rehabil Prev. 1989;9(11):448–59. http://journals.lww.com/jcrjournal/Fulltext/1989/11000/Validity_and_Reliability_of_Short_Physical.3.aspx
37. Carr JJ, Nelson JC, Wong ND, McNitt-Gray M, Arad Y, David R. Jacobs J, et al. Calcified Coronary Artery Plaque Measurement with Cardiac CT in Population-based Studies: Standardized Protocol of Multi-Ethnic Study of Atherosclerosis (MESA) and Coronary Artery Risk Development in Young Adults (CARDIA) Study. Radiology. 2005;234(1):35–43. http://dx.doi.org/10.1148/radiol.2341040439 15618373
38. Carr JJ, Jacobs DR, Terry JG, Shay CM, Sidney S, Liu K, et al. Association of coronary artery calcium in adults aged 32 to 46 years with incident coronary heart disease and death. JAMA Cardiol. 2017;2(4):391–9. doi: 10.1001/jamacardio.2016.5493 28196265
39. Reis JP, Loria CM, Lewis CE, Powell-Wiley TM, Wei GS, Carr JJ, et al. Association between duration of overall and abdominal obesity beginning in young adulthood and coronary artery calcification in middle age. JAMA. 2013 Jul 17;310(3):280–8. http://www.ncbi.nlm.nih.gov/pubmed/23860986 doi: 10.1001/jama.2013.7833 23860986
40. Agatston AS, Janowitz WR, Hildner FJ, Zusmer NR, Viamonte M, Detrano R. Quantification of coronary artery calcium using ultrafast computed tomography. J Am Coll Cardiol. 1990;15(4):827–32. doi: 10.1016/0735-1097(90)90282-t 2407762
41. Jacobs DR and Gottenborg S. Smoking and weight: The Minnesota Lipid Research Clinic. 1981;71:391–396.
42. Carreras-Torres R, Johansson M, Haycock PC, Relton CL, Smith GD, Brennan P, et al. Role of Obesity in smoking behaviour: Mendelian randomisation study in UK Biobank. BMJ 2018;361:k1767. doi: 10.1136/bmj.k1767 29769355
43. Komiya H, Mori Y, Yokose T, Tajima N. Smoking as a Risk Factor for Visceral Fat Accumulation in Japanese Men. Tohoku J Exp Med. 2006;208(2):123–32. http://joi.jlc.jst.go.jp/JST.JSTAGE/tjem/208.123?from=CrossRef doi: 10.1620/tjem.208.123 16434835
44. Steffl M, Bohannon RW, Petr M, Kohlikova E, Holmerova I. Relation between cigarette smoking and sarcopenia: Meta-analysis. Physiol Res. 2015;64(3):419–26. doi: 10.33549/physiolres.932802 25536323
45. Marty E, Liu Y, Samuel A, Or O, Lane J. A review of sarcopenia: Enhancing awareness of an increasingly prevalent disease. Bone. 2017 Dec;105:276–86. doi: 10.1016/j.bone.2017.09.008 28931495
46. Kuipers AL, Zmuda JM, Carr JJ, Terry JG, Nair S, Cvejkus R, et al. Association of ectopic fat with abdominal aorto-illiac and coronary artery calcification in african ancestry men. Atherosclerosis. 2017;263:198–204. http://dx.doi.org/10.1016/j.atherosclerosis.2017.06.030 28651187
47. Miljkovic I, Cauley JA, Wang PY, Holton KF, Lee CG, Sheu Y, et al. Abdominal myosteatosis is independently associated with hyperinsulinemia and insulin resistance among older men without diabetes. Obesity (Silver Spring). 2013 Oct;21(10):2118–25. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3661705&tool=pmcentrez&rendertype=abstract
48. Addison O, Marcus RL, Lastayo PC, Ryan AS. Intermuscular fat: A review of the consequences and causes. Int J Endocrinol. 2014;2014:34–6.
49. Delmonico MJ, Harris TB, Visser M, Park SW, Conroy MB, Velasquez-Mieyer P, et al. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr. 2009;90(6):1579–85. doi: 10.3945/ajcn.2009.28047 19864405
50. Marques EA, Elbejjani M, Frank-Wilson A, Gudnason V, Sigurdsson G, Lang T, et al. Cigarette smoking is associated with lower quadriceps cross-sectional area and attenuation in older adults. Nicotine Tob Res. 2019 22(6):935–941. doi: 10.1093/ntr/ntz081 31091312
51. Maddatu J, Anderson-Baucum E, Evans-Molina C. Smoking and the risk of type 2 diabetes. Transl Res. 2017;184:101–7. doi: 10.1016/j.trsl.2017.02.004 28336465
52. Willi C, Bodenmann P, Ghali WA, Faris PD, Cornuz J. Active smoking and the risk of type 2 diabetes. J Am Med Assoc. 2007;298(22):2654–64.
53. Morley JE, Malmstrom TK, Rodriguez-Mañas L, Sinclair AJ. Frailty, Sarcopenia and Diabetes. J Am Med Dir Assoc. 2014;15(12):853–9. doi: 10.1016/j.jamda.2014.10.001 25455530
54. Miljkovic I, Zmuda JM. Epidemiology of myosteatosis. Curr Opin Clin Nutr Metab Care. 2010 May;13(3):260–4. doi: 10.1097/MCO.0b013e328337d826 20179586
55. Degens H, Gayan-Ramirez G, van Hees HWH. Smoking-induced skeletal muscle dysfunction: from evidence to mechanisms. Am J Respir Crit Care Med. 2015 Mar;191(6):620–5. doi: 10.1164/rccm.201410-1830PP 25581779
56. Montes De Oca M, Loeb E, Torres SH, De Sanctis J, Hernández N, Tálamo C. Peripheral muscle alterations in non-COPD smokers. Chest. 2008;133(1):13–8. doi: 10.1378/chest.07-1592 18187741
57. Wust RCI, Jaspers RT, van der Laarse WJ, Degens H. Skeletal muscle capillarization and oxidative metabolism in healthy smokers. Appl Physiol Nutr Metab. 2008 Dec;33(6):1240–5. doi: 10.1139/H08-116 19088783
58. Nakatani T, Nakashima T, Kita T, Ishihara A. Responses of Exposure to Cigarette Smoke at Three Dosage Levels on Soleus Muscle Fibers in Wistar-Kyoto and Spontaneously Hypertensive Rats. Jpn J Pharmacol. 2002;90(2):157–63. doi: 10.1254/jjp.90.157 12419886
59. 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(1):47–53.
60. Degens H. The role of systemic inflammation in age-related muscle weakness and wasting: Review. Scand J Med Sci Sport. 2010;20(1):28–38.
61. Sinha-Hikim I, Friedman TC, Shin C-S, Lee D, Ivey R, Sinha-Hikim AP. Nicotine in combination with a high-fat diet causes intramyocellular mitochondrial abnormalities in male mice. Endocrinology. 2014 Mar;155(3):865–72. http://www.ncbi.nlm.nih.gov/pubmed/24424058 doi: 10.1210/en.2013-1795 24424058
62. Kalinkovich A, Livshits G. Sarcopenic obesity or obese sarcopenia: A cross talk between age-associated adipose tissue and skeletal muscle inflammation as a main mechanism of the pathogenesis. Ageing Res Rev. 2017;35:200–21. doi: 10.1016/j.arr.2016.09.008 27702700
Článek vyšel v časopise
PLOS Medicine
2020 Číslo 7
- S diagnostikou Parkinsonovy nemoci může nově pomoci AI nástroj pro hodnocení mrkacího reflexu
- Proč při poslechu některé muziky prostě musíme tančit?
- Chůze do schodů pomáhá prodloužit život a vyhnout se srdečním chorobám
- „Jednohubky“ z klinického výzkumu – 2024/44
- Je libo čepici místo mozkového implantátu?
Nejčtenější v tomto čísle
- Obesity, clinical, and genetic predictors for glycemic progression in Chinese patients with type 2 diabetes: A cohort study using the Hong Kong Diabetes Register and Hong Kong Diabetes Biobank
- Participation in adherence clubs and on-time drug pickup among HIV-infected adults in Zambia: A matched-pair cluster randomized trial
- Estimation of SARS-CoV-2 mortality during the early stages of an epidemic: A modeling study in Hubei, China, and six regions in Europe
- Neonatal outcome in 29 pregnant women with COVID-19: A retrospective study in Wuhan, China
