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Low muscle mass is associated with carotid atherosclerosis in patients with type 2 diabetes

      Highlights

      • Patients with type 2 diabetes mellitus (T2DM) and carotid atherosclerosis had lower skeletal muscle mass.
      • Low skeletal muscle mass was associated with increased risk of carotid atherosclerosis in both men and women with T2DM.
      • The risk of atherosclerosis may be modified by skeletal muscle mass maintenance in patients with T2DM.

      Abstract

      Background and aims

      Sarcopenia leads to metabolic and vascular abnormalities. However, little is known regarding the independent relationship between skeletal muscle mass and atherosclerosis in patients with type 2 diabetes mellitus (T2DM). This study aimed to evaluate the association between skeletal muscle mass and carotid atherosclerosis in men and women with T2DM.

      Methods

      In this cross-sectional study, a total of 8202 patients with T2DM were recruited from the Seoul Metabolic Syndrome cohort. Skeletal muscle mass was estimated using bioimpedance analysis, while skeletal muscle mass index (SMI, %) was defined as total skeletal muscle mass (kg)/body weight (kg) × 100. Both carotid arteries were examined by B-mode ultrasound. Carotid atherosclerosis was defined by having a carotid plaque or mean carotid intima-media thickness (IMT) ≥1.1 mm.

      Results

      Among the entire population, 4299 (52.4%) subjects had carotid atherosclerosis. The prevalence of carotid atherosclerosis increased with decreasing SMI quartiles for both sexes. The odds ratios for carotid atherosclerosis were 2.33 (95% confidence interval [CI], 1.17–4.63) and 2.24 (95% CI, 1.06–4.741) in the lowest versus highest SMI quartile in men and women, respectively, after the adjustment for clinical risk factors. In men, the risk of atherosclerosis increased linearly with decreasing SMI quartiles (p for trend = 0.036).

      Conclusions

      Low skeletal muscle mass was independently associated with the presence of carotid atherosclerosis in men and women with T2DM.

      Graphical abstract

      Keywords

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      References

        • Batsis Ja B.S.
        Sarcopenia, sarcopenic obesity and insulin resistance.
        in: Croniger C. Medical Complications of Type 2 Diabetes. InTech, 2011: 233-256
        • Cho N.H.
        • et al.
        IDF Diabetes Atlas: global estimates of diabetes prevalence for 2017 and projections for 2045.
        Diabetes Res. Clin. Pract. 2018; 138: 271-281
        • Shafiee G.
        • et al.
        Prevalence of sarcopenia in the world: a systematic review and meta- analysis of general population studies.
        J. Diabetes Metab. Disord. 2017; 16: 21
        • Han K.
        • et al.
        Sarcopenia as a determinant of blood pressure in older Koreans: findings from the Korea national Health and nutrition examination surveys (KNHANES) 2008-2010.
        PloS One. 2014; 9e86902
        • Rolland Y.
        • et al.
        Sarcopenia: its assessment, etiology, pathogenesis, consequences and future perspectives.
        J. Nutr. Health Aging. 2008; 12: 433-450
        • Ochi M.
        • et al.
        Arterial stiffness is associated with low thigh muscle mass in middle-aged to elderly men.
        Atherosclerosis. 2010; 212: 327-332
        • Chin S.O.
        • et al.
        Sarcopenia is independently associated with cardiovascular disease in older Korean adults: the Korea National Health and Nutrition Examination Survey (KNHANES) from 2009.
        PloS One. 2013; 8e60119
        • Scott D.
        • de Courten B.
        • Ebeling P.R.
        Sarcopenia: a potential cause and consequence of type 2 diabetes in Australia's ageing population?.
        Med. J. Aust. 2016; 205: 329-333
        • Garcia M.J.
        • et al.
        Morbidity and mortality in diabetics in the Framingham population. Sixteen year follow-up study.
        Diabetes. 1974; 23: 105-111
        • Herrington W.
        • et al.
        Epidemiology of atherosclerosis and the potential to reduce the global burden of atherothrombotic disease.
        Circ. Res. 2016; 118: 535-546
        • Santos-Gallego C.G.
        • Picatoste B.
        • Badimon J.J.
        Pathophysiology of acute coronary syndrome.
        Curr. Atherosclerosis Rep. 2014; 16: 401
        • Amato M.
        • et al.
        Carotid plaque-thickness and common carotid IMT show additive value in cardiovascular risk prediction and reclassification.
        Atherosclerosis. 2017; 263: 412-419
        • Lorenz M.W.
        • et al.
        Predictive value for cardiovascular events of common carotid intima media thickness and its rate of change in individuals at high cardiovascular risk - results from the PROG-IMT collaboration.
        PloS One. 2018; 13e0191172
        • Sibal L.
        • Agarwal S.C.
        • Home P.D.
        Carotid intima-media thickness as a surrogate marker of cardiovascular disease in diabetes.
        Diabetes Metab Syndr Obes. 2011; 4: 23-34
        • Ko B.J.
        • et al.
        Relationship between low relative muscle mass and coronary artery calcification in healthy adults.
        Arterioscler. Thromb. Vasc. Biol. 2016; 36: 1016-1021
        • Campos A.M.
        • et al.
        Sarcopenia, but not excess weight or increased caloric intake, is associated with coronary subclinical atherosclerosis in the very elderly.
        Atherosclerosis. 2017; 258: 138-144
        • Heo J.E.
        • et al.
        Association of appendicular skeletal muscle mass with carotid intima-media thickness according to body mass index in Korean adults.
        Epidemiol Health. 2018; 40e2018049
        • Cruz-Jentoft A.J.
        • et al.
        Sarcopenia: European consensus on definition and diagnosis: report of the European working group on sarcopenia in older people.
        Age Ageing. 2010; 39: 412-423
        • Akinmokun A.
        • et al.
        The short insulin tolerance test for determination of insulin sensitivity: a comparison with the euglycaemic clamp.
        Diabet. Med. 1992; 9: 432-437
        • Kim S.K.
        • et al.
        Ratio of waist-to-calf circumference and carotid atherosclerosis in Korean patients with type 2 diabetes.
        Diabetes Care. 2011; 34: 2067-2071
        • Touboul P.J.
        • et al.
        Mannheim carotid intima-media thickness and plaque consensus (2004-2006-2011).
        in: An Update on Behalf of the Advisory Board of the 3rd, 4th and 5th Watching the Risk Symposia, at the 13th, 15th and 20th European Stroke Conferences, Mannheim, Germany. 2004: 290-296 (Brussels, Belgium, 2006, and Hamburg, Germany, 2011. Cerebrovasc Dis, 2012. 34(4))
        • Katakami N.
        • Kaneto H.
        • Shimomura I.
        Carotid ultrasonography: a potent tool for better clinical practice in diagnosis of atherosclerosis in diabetic patients.
        J Diabetes Investig. 2014; 5: 3-13
        • Lorenz M.W.
        • et al.
        Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis.
        Circulation. 2007; 115: 459-467
        • Yaron M.
        • et al.
        Effect of testosterone replacement therapy on arterial stiffness in older hypogonadal men.
        Eur. J. Endocrinol. 2009; 160: 839-846
        • Janssen I.
        • et al.
        Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr.
        J. Appl. Physiol. 1985; 89 (2000): 81-88
        • Gheller B.J.
        • et al.
        Understanding age-related changes in skeletal muscle metabolism: differences between females and males.
        Annu. Rev. Nutr. 2016; 36: 129-156
        • Kirchengast S.
        • Huber J.
        Gender and age differences in lean soft tissue mass and sarcopenia among healthy elderly.
        Anthropol. Anzeiger. 2009; 67: 139-151
        • Silva A.M.
        • et al.
        Ethnicity-related skeletal muscle differences across the lifespan.
        Am. J. Hum. Biol. 2010; 22: 76-82
        • Auyeung T.W.
        • et al.
        Age-associated decline of muscle mass, grip strength and gait speed: a 4-year longitudinal study of 3018 community-dwelling older Chinese.
        Geriatr. Gerontol. Int. 2014; 14: 76-84
        • El Assar M.
        • Angulo J.
        • Rodriguez-Manas L.
        Oxidative stress and vascular inflammation in aging.
        Free Radic. Biol. Med. 2013; 65: 380-401
        • Asano R.Y.
        • et al.
        Acute effects of physical exercise in type 2 diabetes: a review.
        World J. Diabetes. 2014; 5: 659-665
        • Starkie R.
        • et al.
        Exercise and IL-6 infusion inhibit endotoxin-induced TNF-alpha production in humans.
        Faseb. J. 2003; 17: 884-886
        • Wannamethee S.G.
        • et al.
        Physical activity and hemostatic and inflammatory variables in elderly men.
        Circulation. 2002; 105: 1785-1790
        • Cleasby M.E.
        • Jamieson P.M.
        • Atherton P.J.
        Insulin resistance and sarcopenia: mechanistic links between common co-morbidities.
        J. Endocrinol. 2016; 229: R67-R81
        • Guillet C.
        • Boirie Y.
        Insulin resistance: a contributing factor to age-related muscle mass loss?.
        Diabetes Metab. 2005; 31 Spec: 5s20-5s26
        • Cersosimo E.
        • DeFronzo R.A.
        Insulin resistance and endothelial dysfunction: the road map to cardiovascular diseases.
        Diabetes Metab Res Rev. 2006; 22: 423-436
        • Lim S.
        • et al.
        Sarcopenic obesity: prevalence and association with metabolic syndrome in the Korean Longitudinal Study on Health and Aging (KLoSHA).
        Diabetes Care. 2010; 33: 1652-1654
        • Park M.H.
        • et al.
        Age-related inflammation and insulin resistance: a review of their intricate interdependency.
        Arch Pharm. Res. (Seoul). 2014; 37: 1507-1514
        • Batsis J.A.
        • Villareal D.T.
        Sarcopenic obesity in older adults: aetiology, epidemiology and treatment strategies.
        Nat. Rev. Endocrinol. 2018; 14: 513-537
        • Abizanda P.
        • et al.
        Energetics of aging and frailty: the FRADEA study.
        J Gerontol A Biol Sci Med Sci. 2016; 71: 787-796
        • Cruz-Jentoft A.J.
        • et al.
        Prevalence of and interventions for sarcopenia in ageing adults: a systematic review. Report of the International Sarcopenia Initiative (EWGSOP and IWGS).
        Age Ageing. 2014; 43: 748-759
        • Farmer R.E.
        • et al.
        Associations between measures of sarcopenic obesity and risk of cardiovascular disease and mortality: a cohort study and mendelian randomization analysis using the UK biobank.
        J Am Heart Assoc. 2019; 8e011638
        • Kim J.H.
        • Cho J.J.
        • Park Y.S.
        Relationship between sarcopenic obesity and cardiovascular disease risk as estimated by the Framingham risk score.
        J. Kor. Med. Sci. 2015; 30: 264-271
        • Chung J.Y.
        • et al.
        Body composition and its association with cardiometabolic risk factors in the elderly: a focus on sarcopenic obesity.
        Arch. Gerontol. Geriatr. 2013; 56: 270-278
        • Janssen I.
        • et al.
        Body mass index and waist circumference independently contribute to the prediction of nonabdominal, abdominal subcutaneous, and visceral fat.
        Am. J. Clin. Nutr. 2002; 75: 683-688
        • Park S.
        • Ham J.O.
        • Lee B.K.
        A positive association between stroke risk and sarcopenia in men aged >/= 50 years, but not women: results from the Korean National Health and Nutrition Examination Survey 2008-2010.
        J. Nutr. Health Aging. 2014; 18: 806-812
        • Ebrahim S.
        • et al.
        Carotid plaque, intima media thickness, cardiovascular risk factors, and prevalent cardiovascular disease in men and women: the British Regional Heart Study.
        Stroke. 1999; 30: 841-850
        • Stewart S.P.
        • et al.
        Estimation of body composition from bioelectrical impedance of body segments: comparison with dual-energy X-ray absorptiometry.
        Br. J. Nutr. 1993; 69: 645-655