Sarcopenia and type 2 diabetes mellitus: a bidirectional relationship

References

• Cho NH , Shaw JE , Karuranga S , et al. IDF diabetes atlas: global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res Clin Pract . 2018;138:271–281. doi:10.1016/j.diabres.2018.02.023 29496507
   PubMed Web of Science ®Google Scholar
• American Diabetes A. Diagnosis and classification of diabetes mellitus. Diabetes Care . 2009;32 Suppl 1(Suppl1):S62–S67. doi:10.2337/dc09-S062 19118289
   PubMed Web of Science ®Google Scholar
• Harreiter J , Kautzky-Willer A , Pacini G . Sex and gender differences in risk, pathophysiology and complications of type 2 diabetes mellitus. Endocr Rev . 2016;37(3):278–316. doi:10.1210/er.2015-1137 27159875
   PubMed Web of Science ®Google Scholar
• Briggs AM , Woolf AD , Dreinhöfer K , et al. Reducing the global burden of musculoskeletal conditions. Bull World Health Organ . 2018;96(5):366–368. doi:10.2471/BLT.17.204891 29875522
   PubMed Web of Science ®Google Scholar
• St-Onge M-P , Gallagher D . Body composition changes with aging: the cause or the result of alterations in metabolic rate and macronutrient oxidation? Nutrition . 2010;26(2):152–155. doi:10.1016/j.nut.2009.07.004 20004080
   PubMed Web of Science ®Google Scholar
• Hong S , Chang Y , Jung HS , Yun KE , Shin H , Ryu S . Relative muscle mass and the risk of incident type 2 diabetes: a cohort study. PLoS One . 2017;12(11):e0188650. doi:10.1371/journal.pone.0188650 29190709
   PubMed Web of Science ®Google Scholar
• Wang Y , Rimm EB , Stampfer MJ , Willett WC , Hu FB . Comparison of abdominal adiposity and overall obesity in predicting risk of type 2 diabetes among men. Am J Clin Nutr . 2005;81(3):555–563.15755822
   PubMed Web of Science ®Google Scholar
• Cruz-Jentoft AJ , Baeyens JP , Bauer JM , et al. Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People. Age Ageing . 2010;39(4):412–423.20392703
   PubMed Web of Science ®Google Scholar
• Cruz-Jentoft AJ , Bahat G , Bauer J , et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing . 2018;48(1):16–31. doi:10.1093/ageing/afy169
   Web of Science ®Google Scholar
• Studenski SA , Peters KW , Alley DE , et al. The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. J Gerontol A Biol Sci Med Sci . 2014;69(5):547–558. doi:10.1093/gerona/glu010 24737557
   PubMed Web of Science ®Google Scholar
• Fielding RA , Vellas B , Evans WJ , et al. Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc . 2011;12(4):249–256. doi:10.1016/j.jamda.2011.01.003 21527165
   PubMed Web of Science ®Google Scholar
• Chen LK , Liu LK , 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. doi:10.1016/j.jamda.2013.11.025 24461239
   PubMed Web of Science ®Google Scholar
• Scott D , de Courten B , Ebeling PR . Sarcopenia: a potential cause and consequence of type 2 diabetes in Australia’s ageing population? Med J Aust . 2016;205(7):329–333.27681976
   PubMed Web of Science ®Google Scholar
• Nowotny K , Jung T , Höhn A , Weber D , Grune T . Advanced glycation end products and oxidative stress in type 2 diabetes mellitus. Biomolecules . 2015;5:194–222. doi:10.3390/biom5010194 25786107
   PubMed Web of Science ®Google Scholar
• Amog K , Raina P , Mayhew AJ , et al. The prevalence of sarcopenia in community-dwelling older adults, an exploration of differences between studies and within definitions: a systematic review and meta-analyses. Age Ageing . 2018;48(1):48–56.
   Web of Science ®Google Scholar
• Shafiee G , Keshtkar A , Soltani A , Ahadi Z , Larijani B , Heshmat R . Prevalence of sarcopenia in the world: a systematic review and meta- analysis of general population studies. J Diabetes Metab Disord . 2017;16:21. doi:10.1186/s40200-017-0302-x 28523252
   PubMed Web of Science ®Google Scholar
• Murata Y , Kadoya Y , Yamada S , Sanke T . Sarcopenia in elderly patients with type 2 diabetes mellitus: prevalence and related clinical factors. Diabetol Int . 2018;9(2):136–142. doi:10.1007/s13340-017-0339-6 30603361
   PubMed Web of Science ®Google Scholar
• Wang T , Feng X , Zhou J , et al. Type 2 diabetes mellitus is associated with increased risks of sarcopenia and pre-sarcopenia in Chinese elderly. Sci Rep . 2016;6:38937. doi:10.1038/srep38937 27958337
   PubMed Web of Science ®Google Scholar
• Kim TN , Park MS , Yang SJ , et al. Prevalence and determinant factors of sarcopenia in patients with type 2 diabetes. Diabetes Care . 2010;33(7):1497. doi:10.2337/dc09-2310 20413515
   PubMed Web of Science ®Google Scholar
• Park SW , Goodpaster BH , Lee JS , et al. Excessive loss of skeletal muscle mass in older adults with type 2 diabetes. Diabetes Care . 2009;32(11):1993–1997. doi:10.2337/dc09-0264 19549734
   PubMed Web of Science ®Google Scholar
• Yang L , Smith L , Hamer M . Gender-specific risk factors for incident sarcopenia: 8-year follow-up of the English longitudinal study of ageing. J Epidemiol Community Health . 2019;73(1):86. doi:10.1136/jech-2018-211258 30368480
   PubMed Web of Science ®Google Scholar
• Son JW , Lee SS , Kim SR , et al. Low muscle mass and risk of type 2 diabetes in middle-aged and older adults: findings from the KoGES. Diabetologia . 2017;60(5):865–872. doi:10.1007/s00125-016-4196-9 28102434
   PubMed Web of Science ®Google Scholar
• Wu H , Liu M , Chi VTQ , et al. Handgrip strength is inversely associated with metabolic syndrome and its separate components in middle aged and older adults: a large-scale population-based study. Metabolism . 2019;93:61–67. doi:10.1016/j.metabol.2019.01.011 30690038
   PubMed Web of Science ®Google Scholar
• Thiebaud D , Jacot E , DeFronzo RA , Maeder E , Jequier E , Felber JP . The effect of graded doses of insulin on total glucose uptake, glucose oxidation, and glucose storage in man. Diabetes . 1982;31(11):957–963.6757014
   PubMed Web of Science ®Google Scholar
• Lee CG , Boyko EJ , Strotmeyer ES , et al. Association between insulin resistance and lean mass loss and fat mass gain in older men without diabetes mellitus. J Am Geriatr Soc . 2011;59(7):1217–1224. doi:10.1111/j.1532-5415.2011.03472.x 21718263
   PubMed Web of Science ®Google Scholar
• Kuo CK , Lin LY , Yu YH , Wu KH , Kuo HK . Inverse association between insulin resistance and gait speed in nondiabetic older men: results from the U.S. National Health and Nutrition Examination Survey (NHANES) 1999-2002. BMC Geriatr . 2009;9:49. doi:10.1186/1471-2318-9-49 19922671
   PubMedGoogle Scholar
• Abbatecola AM , Ferrucci L , Ceda G , et al. Insulin resistance and muscle strength in older persons. J Gerontol A Biol Sci Med Sci . 2005;60(10):1278–1282.16282559
   PubMed Web of Science ®Google Scholar
• Sherwani SI , Khan HA , Ekhzaimy A , Masood A , Sakharkar MK . Significance of HbA1c test in diagnosis and prognosis of diabetic patients. Biomark Insights . 2016;11:95–104. doi:10.4137/BMI.S38440 27398023
   PubMed Web of Science ®Google Scholar
• Yoon JW , Ha Y-C , Kim KM , et al. Hyperglycemia is associated with impaired muscle quality in older men with diabetes: the Korean Longitudinal Study on Health and Aging. Diabetes Metab J . 2016;40(2):140–146. doi:10.4093/dmj.2016.40.2.140 27126884
   PubMed Web of Science ®Google Scholar
• Kalyani RR , Metter EJ , Egan J , Golden SH , Ferrucci L . Hyperglycemia predicts persistently lower muscle strength with aging. Diabetes Care . 2015;38(1):82–90. doi:10.2337/dc14-1166 25392294
   PubMed Web of Science ®Google Scholar
• Russell ST , Rajani S , Dhadda RS , Tisdale MJ . Mechanism of induction of muscle protein loss by hyperglycaemia. Exp Cell Res . 2009;315(1):16–25. doi:10.1016/j.yexcr.2008.10.002 18973755
   PubMed Web of Science ®Google Scholar
• Pereira S , Marliss EB , Morais JA , Chevalier S , Gougeon R . Insulin resistance of protein metabolism in type 2 diabetes. Diabetes . 2008;57(1):56. doi:10.2337/db07-0887 17940118
   PubMed Web of Science ®Google Scholar
• de Rekeneire N , Peila R , Ding J , et al. Diabetes, hyperglycemia, and inflammation in older individuals. Diabetes Care . 2006;29(8):1902. doi:10.2337/dc05-2327 16873800
   PubMed Web of Science ®Google Scholar
• Vozarova B , Weyer C , Lindsay RS , Pratley RE , Bogardus C , Tataranni PA . High white blood cell count is associated with a worsening of insulin sensitivity and predicts the development of type 2 diabetes. Diabetes . 2002;51(2):455. doi:10.2337/diabetes.51.2.455 11812755
   PubMed Web of Science ®Google Scholar
• Haddad F , Zaldivar F , Cooper DM , Adams GR . IL-6-induced skeletal muscle atrophy. J Appl Physiol . 2005;98(3):911–917. doi:10.1152/japplphysiol.01026.2004 15542570
   PubMed Web of Science ®Google Scholar
• Goyal R , Faizy AF , Siddiqui SS , Singhai M . Evaluation of TNF-α and IL-6 levels in obese and non-obese diabetics: pre- and postinsulin effects. N Am J Med Sci . 2012;4(4):180–184. doi:10.4103/1947-2714.94944 22536561
   PubMedGoogle Scholar
• King DE , Mainous AG , Buchanan TA , Pearson WS . C-reactive protein and glycemic control in adults with diabetes. Diabetes Care . 2003;26(5):1535. doi:10.2337/diacare.26.5.1535 12716818
   PubMed Web of Science ®Google Scholar
• Vozarova B , Weyer C , Hanson K , Tataranni PA , Bogardus C , Pratley RE . Circulating interleukin-6 in relation to adiposity, insulin action, and insulin secretion. Obes Res . 2001;9(7):414–417. doi:10.1038/oby.2001.54 11445664
   PubMedGoogle Scholar
• Makki K , Froguel P , Wolowczuk I . Adipose tissue in obesity-related inflammation and insulin resistance: cells, cytokines, and chemokines. ISRN Inflamm . 2013;2013:139239. doi:10.1155/2013/139239 24455420
   PubMedGoogle Scholar
• Mesinovic J , McMillan BL , Shore-Lorenti C , De Courten B , Ebeling RP , Scott D . Metabolic syndrome and its associations with components of sarcopenia in overweight and obese older adults. J Clin Med . 2019;8:2. doi:10.3390/jcm8020145
   Web of Science ®Google Scholar
• Bach E , Nielsen RR , Vendelbo MH , et al. Direct effects of TNF-α on local fuel metabolism and cytokine levels in the placebo-controlled, bilaterally infused human leg. Diabetes . 2013;62(12):4023. doi:10.2337/db12-0863 23835341
   PubMed Web of Science ®Google Scholar
• Carey AL , Steinberg GR , Macaulay SL , et al. Interleukin-6 increases insulin-stimulated glucose disposal in humans and glucose uptake and fatty acid oxidation in vitro via AMP-activated protein kinase. Diabetes . 2006;55(10):2688–2697. doi:10.2337/db05-1404 17003332
   PubMed Web of Science ®Google Scholar
• Serrano AL , Baeza-Raja B , Perdiguero E , Jardi M , Munoz-Canoves P . Interleukin-6 is an essential regulator of satellite cell-mediated skeletal muscle hypertrophy. Cell Metab . 2008;7(1):33–44. doi:10.1016/j.cmet.2007.11.011 18177723
   PubMed Web of Science ®Google Scholar
• Payette H , Roubenoff R , Jacques PF , et al. Insulin-like growth factor-1 and interleukin 6 predict sarcopenia in very old community-living men and women: the Framingham Heart Study. J Am Geriatr Soc . 2003;51(9):1237–1243.12919235
   PubMed Web of Science ®Google Scholar
• Alemán H , Esparza J , Ramirez FA , Astiazaran H , Payette H . Longitudinal evidence on the association between interleukin-6 and C-reactive protein with the loss of total appendicular skeletal muscle in free-living older men and women. Age Ageing . 2011;40(4):469–475. doi:10.1093/ageing/afr040 21565862
   PubMed Web of Science ®Google Scholar
• Park SW , Goodpaster BH , Strotmeyer ES , et al. Accelerated loss of skeletal muscle strength in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes Care . 2007;30(6):1507–1512. doi:10.2337/dc06-2537 17363749
   PubMed Web of Science ®Google Scholar
• Visser M , Pahor M , Taaffe DR , et al. Relationship of interleukin-6 and tumor necrosis factor-alpha with muscle mass and muscle strength in elderly men and women: the Health ABC Study. J Gerontol A Biol Sci Med Sci . 2002;57(5):M326–M332.11983728
   PubMed Web of Science ®Google Scholar
• Hamer M , Molloy GJ . Association of C-reactive protein and muscle strength in the English Longitudinal Study of Ageing. Age (Dordr) . 2009;31(3):171–177. doi:10.1007/s11357-009-9097-0 19466582
   PubMedGoogle Scholar
• Gomes MJ , Martinez PF , Pagan LU , et al. Skeletal muscle aging: influence of oxidative stress and physical exercise. Oncotarget . 2017;8(12):20428–20440. doi:10.18632/oncotarget.14670 28099900
   PubMedGoogle Scholar
• Asmat U , Abad K , Ismail K . Diabetes mellitus and oxidative stress—A concise review. Saudi Pharm J . 2016;24(5):547–553. doi:10.1016/j.jsps.2015.03.013 27752226
   PubMed Web of Science ®Google Scholar
• Aragno M , Mastrocola R , Catalano MG , Brignardello E , Danni O , Boccuzzi G . Oxidative stress impairs skeletal muscle repair in diabetic rats. Diabetes . 2004;53(4):1082.15047625
   PubMed Web of Science ®Google Scholar
• Zacarias-Flores M , Sanchez-Rodriguez MA , Garcia-Anaya OD , Correa-Munoz E , Mendoza-Nunez VM . Relationship between oxidative stress and muscle mass loss in early postmenopause: an exploratory study. Endocrinol Diabetes Nutr . 2018;65(6):328–334. doi:10.1016/j.endinu.2018.01.009 29650435
   PubMed Web of Science ®Google Scholar
• Scicchitano BM , Pelosi L , Sica G , Musarò A . The physiopathologic role of oxidative stress in skeletal muscle. Mech Ageing Dev . 2018;170:37–44. doi:10.1016/j.mad.2017.08.009 28851603
   PubMed Web of Science ®Google Scholar
• Short KR , Bigelow ML , Kahl J , et al. Decline in skeletal muscle mitochondrial function with aging in humans. Proc Natl Acad Sci U S A . 2005;102(15):5618–5623. doi:10.1073/pnas.0501559102 15800038
   PubMed Web of Science ®Google Scholar
• Abbatecola AM , Paolisso G , Fattoretti P , et al. Discovering pathways of sarcopenia in older adults: a role for insulin resistance on mitochondria dysfunction. J Nutr Health Aging . 2011;15(10):890–895. doi:10.1007/s12603-011-0366-0 22159778
   PubMed Web of Science ®Google Scholar
• Conley KE , Jubrias SA , Esselman PC . Oxidative capacity and ageing in human muscle. J Physiol . 2000;526 Pt 1(Pt1):203–210.10878112
   PubMed Web of Science ®Google Scholar
• Bua E , Johnson J , Herbst A , et al. Mitochondrial DNA-deletion mutations accumulate intracellularly to detrimental levels in aged human skeletal muscle fibers. Am J Hum Genet . 2006;79(3):469–480. doi:10.1086/507132 16909385
   PubMed Web of Science ®Google Scholar
• Schrauwen-Hinderling VB , Kooi ME , Hesselink MK , et al. Impaired in vivo mitochondrial function but similar intramyocellular lipid content in patients with type 2 diabetes mellitus and BMI-matched control subjects. Diabetologia . 2007;50(1):113–120. doi:10.1007/s00125-006-0475-1 17093944
   PubMed Web of Science ®Google Scholar
• Morino K , Petersen KF , Dufour S , et al. Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents. J Clin Invest . 2005;115(12):3587–3593. doi:10.1172/JCI25151 16284649
   PubMed Web of Science ®Google Scholar
• Singh R , Barden A , Mori T , Beilin L . Advanced glycation end-products: a review. Diabetologia . 2001;44(2):129–146. doi:10.1007/s001250051591 11270668
   PubMed Web of Science ®Google Scholar
• Haus JM , Carrithers JA , Trappe SW , Trappe TA . Collagen, cross-linking, and advanced glycation end products in aging human skeletal muscle. J Appl Physiol . 2007;103(6):2068–2076. doi:10.1152/japplphysiol.00670.2007 17901242
   PubMed Web of Science ®Google Scholar
• Forbes JM , Sourris KC , de Courten MPJ , et al. Advanced glycation end products (AGEs) are cross-sectionally associated with insulin secretion in healthy subjects. Amino Acids . 2014;46(2):321–326. doi:10.1007/s00726-013-1542-9 23832534
   PubMed Web of Science ®Google Scholar
• Mulder DJ , Water TV , Lutgers HL , et al. Skin autofluorescence, a novel marker for glycemic and oxidative stress-derived advanced glycation endproducts: an overview of current clinical studies, evidence, and limitations. Diabetes Technol Ther . 2006;8(5):523–535. doi:10.1089/dia.2006.8.523 17037967
   PubMed Web of Science ®Google Scholar
• Mori H , Kuroda A , Ishizu M , et al. Association of accumulated advanced glycation end products with a high prevalence of sarcopenia and dynapenia in patients with type 2 diabetes. J Diabetes Investig . 2019;35:731–737. doi:10.1111/jdi.13014
   Web of Science ®Google Scholar
• Momma H , Niu K , Kobayashi Y , et al. Skin advanced glycation end product accumulation and muscle strength among adult men. Eur J Appl Physiol . 2011;111(7):1545–1552. doi:10.1007/s00421-010-1779-x 21188413
   PubMed Web of Science ®Google Scholar
• Tabara Y , Ikezoe T , Yamanaka M , et al. Advanced Glycation End Product Accumulation Is Associated with Low Skeletal Muscle Mass, Weak Muscle Strength, and Reduced Bone Density: The Nagahama Study. J Gerontol A Biol Sci Med Sci 2018. doi:10.1093/gerona/gly233
   Google Scholar
• Chaudhri S , Fan S , Davenport A . Pitfalls in the measurement of skin autofluorescence to determine tissue advanced glycosylation content in haemodialysis patients. Nephrology . 2013;18(10):671–675. doi:10.1111/nep.12118 23815495
   PubMed Web of Science ®Google Scholar
• Noordzij MJ , Lefrandt JD , Graaff R , Smit AJ . Dermal factors influencing measurement of skin autofluorescence. Diabetes Technol Ther . 2011;13(2):165–170.21284484
   PubMed Web of Science ®Google Scholar
• Fowler MJ . Microvascular and macrovascular complications of diabetes. Clin Diabetes . 2008;26(2):77.
   Google Scholar
• McDermott MM , Criqui MH , Greenland P , et al. Leg strength in peripheral arterial disease: associations with disease severity and lower-extremity performance. J Vasc Surg . 2004;39(3):523–530.14981443
   PubMed Web of Science ®Google Scholar
• Nomura T , Ishiguro T , Ohira M , Ikeda Y . Diabetic polyneuropathy is a risk factor for decline of lower extremity strength in patients with type 2 diabetes. J Diabetes Investig . 2018;9(1):186–192.
   PubMed Web of Science ®Google Scholar
• Andersen H , Gjerstad MD , Jakobsen J . Atrophy of foot muscles. Diabetes Care . 2004;27(10):2382.15451904
   PubMed Web of Science ®Google Scholar
• Strotmeyer ES , de Rekeneire N , Schwartz AV , et al. The relationship of reduced peripheral nerve function and diabetes with physical performance in older white and black adults. Diabetes Care . 2008;31(9):1767.18535192
   PubMed Web of Science ®Google Scholar
• Gupta P , Aravindhan A , Gand ATL , et al. Association between the severity of diabetic retinopathy and falls in an asian population with diabetes: the Singapore Epidemiology of Eye Diseases Study. JAMA Ophthalmol . 2017;135(12):1410–1416.29145583
   PubMed Web of Science ®Google Scholar
• Haddad YK , Bergen G , Florence CS . Estimating the economic burden related to older adult falls by state. J Public Health Manag Pract . 2019;25(2):E17–E24.
   PubMed Web of Science ®Google Scholar
• Haagsma JA , Graetz N , Bolliger I , et al. The global burden of injury: incidence, mortality, disability-adjusted life years and time trends from the Global Burden of Disease study 2013. Injury Prevention . 2016;22(1):3.26635210
   PubMed Web of Science ®Google Scholar
• Fukuda T , Bouchi R , Takeuchi T , et al. Association of diabetic retinopathy with both sarcopenia and muscle quality in patients with type 2 diabetes: a cross-sectional study. BMJ Open Diabetes Res Care . 2017;5(1):e000404.
   Web of Science ®Google Scholar
• Collins AJ , Foley RN , Gilbertson DT , Chen S-C . United States renal data system public health surveillance of chronic kidney disease and end-stage renal disease. Kidney Int Suppl . 2015;5(1):2–7.
   PubMed Web of Science ®Google Scholar
• Wang XH , Mitch WE . Mechanisms of muscle wasting in chronic kidney disease. Nat Rev Nephrol . 2014;10(9):504–516.24981816
   PubMed Web of Science ®Google Scholar
• Fung FY , Koh YLE , Malhotra R , et al. Prevalence of and factors associated with sarcopenia among multi-ethnic ambulatory older Asians with type 2 diabetes mellitus in a primary care setting. BMC Geriatr . 2019;19(1):122.31035928
   PubMed Web of Science ®Google Scholar
• VAd S , Oliveira D , Barbosa SR , et al. Sarcopenia in patients with chronic kidney disease not yet on dialysis: analysis of the prevalence and associated factors. PLoS One . 2017;12(4):e0176230–e0176230.28448584
   PubMed Web of Science ®Google Scholar
• Pereira RA , Cordeiro AC , Avesani CM , et al. Sarcopenia in chronic kidney disease on conservative therapy: prevalence and association with mortality. Nephrol Dial Transplant . 2015;30(10):1718–1725.25999376
   PubMed Web of Science ®Google Scholar
• Zhou Y , Hellberg M , Svensson P , Hoglund P , Clyne N . Sarcopenia and relationships between muscle mass, measured glomerular filtration rate and physical function in patients with chronic kidney disease stages 3-5. Nephrol Dial Transplant . 2018;33(2):342–348.28340152
   PubMed Web of Science ®Google Scholar
• Gamboa JL , Billings F , Bojanowski MT , et al. Mitochondrial dysfunction and oxidative stress in patients with chronic kidney disease. Physiol Rep . 2016;4(9):e12780.27162261
   PubMed Web of Science ®Google Scholar
• Martín-Timón I , Sevillano-Collantes C , Segura-Galindo A , Del Cañizo-Gómez FJ . Type 2 diabetes and cardiovascular disease: have all risk factors the same strength? World J Diabetes . 2014;5(4):444–470.25126392
   PubMedGoogle Scholar
• Singleton JR , Smith AG , Russell JW , Feldman EL . Microvascular complications of impaired glucose tolerance. Diabetes . 2003;52(12):2867.14633845
   PubMed Web of Science ®Google Scholar
• McMaster William G , Kirabo A , Madhur Meena S , Harrison David G . Inflammation, immunity, and hypertensive end-organ damage. Circ Res . 2015;116(6):1022–1033.25767287
   PubMed Web of Science ®Google Scholar
• Doğan MH , Karadag B , Ozyigit T , Kayaoglu S , Ozturk AO , Altuntas Y . Correlations between sarcopenia and hypertensive target organ damage in a Turkish cohort. Acta Clin Belg . 2012;67(5):328–332.23189539
   PubMed Web of Science ®Google Scholar
• Butcher Joshua T , Mintz James D , Larion S , et al. Increased muscle mass protects against hypertension and renal injury in obesity. J Am Heart Assoc . 2018;7(16):e009358.30369309
   PubMed Web of Science ®Google Scholar
• Lange S , Diehm C , Darius H , et al. High prevalence of peripheral arterial disease and low treatment rates in elderly primary care patients with diabetes. Exp Clin Endocrinol Diabetes . 2004;112(10):566–573.15578331
   PubMed Web of Science ®Google Scholar
• Dziubek W , Bulińska K , Stefańska M , et al. Peripheral arterial disease decreases muscle torque and functional walking capacity in elderly. Maturitas . 2015;81(4):480–486.26119244
   PubMed Web of Science ®Google Scholar
• McDermott Mary M . Lower extremity manifestations of peripheral artery disease. Circ Res . 2015;116(9):1540–1550.25908727
   PubMed Web of Science ®Google Scholar
• Boettcher M , Machann J , Stefan N , et al. Intermuscular adipose tissue (IMAT): association with other adipose tissue compartments and insulin sensitivity. J Magn Reson Imaging . 2009;29(6):1340–1345.19422021
   PubMed Web of Science ®Google Scholar
• Scott D , Shore-Lorenti C , McMillan LB , et al. Calf muscle density is independently associated with physical function in overweight and obese older adults. J Musculoskelet Neuronal Interact . 2018;18(1):9–17.29504574
   PubMed Web of Science ®Google Scholar
• Marcus RL , Addison O , Dibble LE , Foreman KB , Morrell G , LaStayo P . Intramuscular adipose tissue, sarcopenia, and mobility function in older individuals. J Aging Res . 2012. doi:10.1155/2012/629637
   Google Scholar
• Goodpaster BH , Thaete FL , Kelley DE . Thigh adipose tissue distribution is associated with insulin resistance in obesity and in type 2 diabetes mellitus. Am J Clin Nutr . 2000;71(4):885–892.10731493
   PubMed Web of Science ®Google Scholar
• Gallagher D , Kelley DE , Yim J-E , et al. Adipose tissue distribution is different in type 2 diabetes. Am J Clin Nutr . 2009;89(3):807–814.19158213
   PubMed Web of Science ®Google Scholar
• Scott D , Johansson J , McMillan LB , Ebeling PR , Nordstrom A , Nordstrom P . Mid-calf skeletal muscle density and its associations with physical activity, bone health and incident 12-month falls in older adults: the Healthy Ageing Initiative. Bone . 2018;120:446–451. doi:10.1016/j.bone.2018.12.004
   Web of Science ®Google Scholar
• Frank-Wilson AW , Farthing JP , Chilibeck PD , et al. Lower leg muscle density is independently associated with fall status in community-dwelling older adults. Osteoporos Int . 2016;27(7):2231–2240.26879201
   PubMed Web of Science ®Google Scholar
• Bittel DC , Bittel AJ , Tuttle LJ , et al. Adipose tissue content, muscle performance and physical function in obese adults with type 2 diabetes mellitus and peripheral neuropathy. J Diabetes Complications . 2015;29(2):250–257. doi:10.1016/j.jdiacomp.2014.11.003 25547717
   PubMed Web of Science ®Google Scholar
• Skundric DS , Lisak RP . Role of neuropoietic cytokines in development and progression of diabetic polyneuropathy: from glucose metabolism to neurodegeneration. Exp Diabesity Res . 2003;4(4):303–312. doi:10.1155/EDR.2003.303 14668051
   PubMedGoogle Scholar
• Csapo R , Malis V , Sinha U , Du J , Sinha S . Age-associated differences in triceps surae muscle composition and strength – an MRI-based cross-sectional comparison of contractile, adipose and connective tissue. BMC Musculoskelet Disord . 2014;15(1):209. doi:10.1186/1471-2474-15-209 24939372
   PubMed Web of Science ®Google Scholar
• Musi N , Hirshman MF , Nygren J , et al. Metformin increases AMP-activated protein kinase activity in skeletal muscle of subjects with type 2 diabetes. Diabetes . 2002;51(7):2074–2081. doi:10.2337/diabetes.51.7.2074 12086935
   PubMed Web of Science ®Google Scholar
• Mihaylova MM , Shaw RJ . The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat Cell Biol . 2011;13(9):1016–1023. doi:10.1038/ncb2329 21892142
   PubMed Web of Science ®Google Scholar
• Long DE , Peck BD , Martz JL , et al. Metformin to Augment Strength Training Effective Response in Seniors (MASTERS): study protocol for a randomized controlled trial. Trials . 2017;18(1):192. doi:10.1186/s13063-017-1932-5 28441958
   PubMed Web of Science ®Google Scholar
• Lee CG , Boyko EJ , Barrett-Connor E , et al. Insulin sensitizers may attenuate lean mass loss in older men with diabetes. Diabetes Care . 2011;34(11):2381. doi:10.2337/dc11-1032 21926282
   PubMed Web of Science ®Google Scholar
• Cetrone M , Mele A , Tricarico D . Effects of the antidiabetic drugs on the age-related atrophy and sarcopenia associated with diabetes type II. Curr Diabetes Rev . 2014;10(4):231–237.25245021
   PubMedGoogle Scholar
• Fanzani A , Conraads VM , Penna F , Martinet W . Molecular and cellular mechanisms of skeletal muscle atrophy: an update. J Cachexia Sarcopenia Muscle . 2012;3(3):163–179. doi:10.1007/s13539-012-0074-6 22673968
   PubMed Web of Science ®Google Scholar
• Mele A , Calzolaro S , Cannone G , Cetrone M , Conte D , Tricarico D . Database search of spontaneous reports and pharmacological investigations on the sulfonylureas and glinides-induced atrophy in skeletal muscle. Pharmacol Res Perspect . 2014;2(1):e00028–e00028. doi:10.1002/prp2.28 25505577
   PubMedGoogle Scholar
• Diabetes Prevention Program Research G. Long-term safety, tolerability, and weight loss associated with metformin in the Diabetes Prevention Program Outcomes Study. Diabetes Care . 2012;35(4):731–737. doi:10.2337/dc11-1299 22442396
   PubMed Web of Science ®Google Scholar
• van Dieren S , Czernichow S , Chalmers J , et al. Weight changes and their predictors amongst 11 140 patients with type 2 diabetes in the ADVANCE trial. Diabetes Obes Metab . 2012;14(5):464–469. doi:10.1111/j.1463-1326.2012.01556.x 22226008
   PubMed Web of Science ®Google Scholar
• Fujita S , Rasmussen BB , Cadenas JG , Grady JJ , Volpi E . Effect of insulin on human skeletal muscle protein synthesis is modulated by insulin-induced changes in muscle blood flow and amino acid availability. Am J Physiol Endocrinol Metab . 2006;291(4):E745–E754. doi:10.1152/ajpendo.00271.2005 16705054
   PubMed Web of Science ®Google Scholar
• Raz I , Chen Y , Wu M , et al. Efficacy and safety of sitagliptin added to ongoing metformin therapy in patients with type 2 diabetes. Curr Med Res Opin . 2008;24(2):537–550. doi:10.1185/030079908X260925 18194595
   PubMed Web of Science ®Google Scholar
• Scheen AJ . Pharmacodynamics, efficacy and Safety of Sodium–glucose Co-Transporter Type 2 (SGLT2) inhibitors for the treatment of type 2 diabetes mellitus. Drugs . 2015;75(1):33–59. doi:10.1007/s40265-014-0337-y 25488697
   PubMed Web of Science ®Google Scholar
• Zinman B , Hoogwerf BJ , Duran Garcia S , et al. The effect of adding exenatide to a thiazolidinedione in suboptimally controlled type 2 diabetes: a randomized trial. Ann Intern Med . 2007;146(7):477–485.17404349
   PubMed Web of Science ®Google Scholar
• Atkinson RA , Srinivas-Shankar U , Roberts SA , et al. Effects of testosterone on skeletal muscle architecture in intermediate-frail and frail elderly men. J Gerontol A Biol Sci Med Sci . 2010;65(11):1215–1219. doi:10.1093/gerona/glq118 20601412
   PubMed Web of Science ®Google Scholar
• Dalton JT , Barnette KG , Bohl CE , et al. The selective androgen receptor modulator GTx-024 (enobosarm) improves lean body mass and physical function in healthy elderly men and postmenopausal women: results of a double-blind, placebo-controlled phase II trial. J Cachexia Sarcopenia Muscle . 2011;2(3):153–161. doi:10.1007/s13539-011-0034-6 22031847
   PubMed Web of Science ®Google Scholar
• Papanicolaou DA , Ather SN , Zhu H , et al. A phase IIA randomized, placebo-controlled clinical trial to study the efficacy and safety of the selective androgen receptor modulator (SARM), MK-0773 in female participants with sarcopenia. J Nutr Health Aging . 2013;17(6):533–543. doi:10.1007/s12603-013-0335-x 23732550
   PubMed Web of Science ®Google Scholar
• Neto WK , Gama EF , Rocha LY , et al. Effects of testosterone on lean mass gain in elderly men: systematic review with meta-analysis of controlled and randomized studies. Age (Dordr) . 2015;37(1):9742. doi:10.1007/s11357-014-9742-0 25637335
   PubMedGoogle Scholar
• Narayanan R , Coss CC , Dalton JT . Development of selective androgen receptor modulators (SARMs). Mol Cell Endocrinol . 2018;465:134–142. doi:10.1016/j.mce.2017.06.013 28624515
   PubMed Web of Science ®Google Scholar
• Becker C , Lord SR , Studenski SA , et al. Myostatin antibody (LY2495655) in older weak fallers: a proof-of-concept, randomised, phase 2 trial. Lancet Diabetes Endocrinol . 2015;3(12):948–957. doi:10.1016/S2213-8587(15)00298-3 26516121
   PubMed Web of Science ®Google Scholar
• Lv Q , Yuan L , Deng J , et al. Efficient generation of myostatin gene mutated rabbit by CRISPR/Cas9. Sci Rep . 2016;6:25029. doi:10.1038/srep25029 27113799
   PubMed Web of Science ®Google Scholar
• Knowler WC , Barrett-Connor E , Fowler SE , et al. Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med . 2002;346(6):393–403. doi:10.1056/NEJMoa012512 11832527
   PubMed Web of Science ®Google Scholar
• Gregg EW , Chen H , Wagenknecht LE , et al. Association of an intensive lifestyle intervention with remission of type 2 diabetes. JAMA . 2012;308(23):2489–2496. doi:10.1001/jama.2012.67929 23288372
   PubMed Web of Science ®Google Scholar
• Steffl M , Bohannon RW , Sontakova L , Tufano JJ , Shiells K , Holmerova I . Relationship between sarcopenia and physical activity in older people: a systematic review and meta-analysis. Clin Interv Aging . 2017;12:835–845. doi:10.2147/CIA.S132940 28553092
   PubMed Web of Science ®Google Scholar
• Houston DK , Neiberg RH , Miller ME , et al. Physical function following a long-term lifestyle intervention among middle aged and older adults with type 2 diabetes: the look AHEAD study. J Gerontol Series A . 2018;73(11):1552–1559. doi:10.1093/gerona/glx204
   PubMed Web of Science ®Google Scholar
• Pan B , Ge L , Xun Y-Q , et al. Exercise training modalities in patients with type 2 diabetes mellitus: a systematic review and network meta-analysis. Int J Behav Nutr Phys Act . 2018;15(1):72. doi:10.1186/s12966-018-0703-3 30045740
   PubMed Web of Science ®Google Scholar
• Dai X , Zhai L , Chen Q , et al. Two-year-supervised resistance training prevented diabetes incidence in people with prediabetes: a randomised control trial. Diabetes Metab Res Rev . 2019;e3143. doi:10.1002/dmrr.3143 30768758
   PubMed Web of Science ®Google Scholar
• Vlietstra L , Hendrickx W , Waters DL . Exercise interventions in healthy older adults with sarcopenia: a systematic review and meta-analysis. Australas J Ageing . 2018;37(3):169–183. doi:10.1111/ajag.12521 29638028
   PubMed Web of Science ®Google Scholar
• Hovanec N , Sawant A , Overend TJ , Petrella RJ , Vandervoort AA . Resistance training and older adults with type 2 diabetes mellitus: strength of the evidence. J Aging Res . 2012;2012:284635. doi:10.1155/2012/284635 22988507
   PubMedGoogle Scholar
• Sardeli A , Komatsu T , Mori M , Gáspari A , Chacon-Mikahil M . Resistance training prevents muscle loss induced by caloric restriction in obese elderly individuals: a systematic review and meta-analysis. Nutrients . 2018;10(4):423. doi:10.3390/nu10040423
   Web of Science ®Google Scholar
• Villareal DT , Aguirre L , Gurney AB , et al. Aerobic or resistance exercise, or both, in dieting obese older adults. N Engl J Med . 2017;376(20):1943–1955. doi:10.1056/NEJMoa1616338 28514618
   PubMed Web of Science ®Google Scholar
• Beavers KM , Ambrosius WT , Rejeski WJ , et al. Effect of exercise type during intentional weight loss on body composition in older adults with obesity. Obesity (Silver Spring) . 2017;25(11):1823–1829. doi:10.1002/oby.21977 29086504
   PubMed Web of Science ®Google Scholar
• Greco M , Chiefari E , Montalcini T , et al. Early effects of a hypocaloric, mediterranean diet on laboratory parameters in obese individuals. Mediators Inflamm . 2014;2014:750860. doi:10.1155/2014/750860 24729662
   PubMed Web of Science ®Google Scholar
• Taylor R , Al-Mrabeh A , Zhyzhneuskaya S , et al. Remission of human type 2 diabetes requires decrease in liver and pancreas fat content but is dependent upon capacity for β cell recovery. Cell Metab . 2018;28(4):547–556. doi:10.1016/j.cmet.2018.07.003 30078554
   PubMed Web of Science ®Google Scholar
• Phillips S , Chevalier S , Leidy H . Protein “Requirements” beyond the RDA: Implications for Optimizing Health. Appl Physiol Nutr Metab 2016;41(5): 565–572. doi:10.1139/apnm-2015-0550
   Google Scholar
• Trumbo P , Schlicker S , Yates AA , Poos M . Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein and amino acids. J Am Diet Assoc . 2002;102(11):1621–1630.12449285
   PubMed Web of Science ®Google Scholar
• Nowson C , O’Connell S . Protein requirements and recommendations for older people: a review. Nutrients . 2015;7(8):6874–6899. doi:10.3390/nu7085311 26287239
   PubMed Web of Science ®Google Scholar
• Health ABCS , Newman AB , Nicklas BJ , et al. Dietary protein intake is associated with lean mass change in older, community-dwelling adults: the Health, Aging, and Body Composition (Health ABC) Study. Am J Clin Nutr . 2008;87(1):150–155. doi:10.1093/ajcn/87.1.150 18175749
   PubMed Web of Science ®Google Scholar
• Shang X , Scott D , Sanders KM , et al. Dietary protein intake and risk of type 2 diabetes: results from the Melbourne Collaborative Cohort Study and a meta-analysis of prospective studies. Am J Clin Nutr . 2016;104(5):1352–1365. doi:10.3945/ajcn.116.140954 27629053
   PubMed Web of Science ®Google Scholar
• van Vliet S , Burd NA , van Loon LJC . The skeletal muscle anabolic response to plant- versus animal-based protein consumption. J Nutr . 2015;145(9):1981–1991. doi:10.3945/jn.114.204305 26224750
   PubMed Web of Science ®Google Scholar
• Morton RW , Murphy KT , McKellar SR , et al. A systematic review, meta-analysis and meta-regression of the effect of protein supplementation on resistance training-induced gains in muscle mass and strength in healthy adults. Br J Sports Med . 2018;52(6):376.28698222
   PubMed Web of Science ®Google Scholar
• Beaudart C , Dawson A , Shaw SC , et al. Nutrition and physical activity in the prevention and treatment of sarcopenia: systematic review. Osteoporos Int . 2017;28(6):1817–1833. doi:10.1007/s00198-017-3980-9 28251287
   PubMed Web of Science ®Google Scholar
• Dang M , Shore-Lorenti C , McMillan BL , et al. Associations of serum 25-hydroxyvitamin D with physical performance and bone health in overweight and obese older adults. Int J Environ Res Public Health . 2019;16(3). doi:10.3390/ijerph16030509.
   Web of Science ®Google Scholar
• Mirhosseini N , Vatanparast H , Mazidi M , Kimball SM . Vitamin D supplementation, glycemic control, and insulin resistance in prediabetics: a meta-analysis. J Endocr Soc . 2018;2(7):687–709. doi:10.1210/js.2017-00472 29951596
   PubMed Web of Science ®Google Scholar
• Shea MK , Fielding RA , Dawson-Hughes B . The effect of vitamin D supplementation on lower-extremity power and function in older adults: a randomized controlled trial. Am J Clin Nutr . 2019;109(2):369–379. doi:10.1093/ajcn/nqy290 30715090
   PubMed Web of Science ®Google Scholar
• Stockton KA , Mengersen K , Paratz JD , Kandiah D , Bennell KL . Effect of vitamin D supplementation on muscle strength: a systematic review and meta-analysis. Osteoporos Int . 2011;22(3):859–871. doi:10.1007/s00198-010-1407-y 20924748
   PubMed Web of Science ®Google Scholar
• Rabenda V , Buckinx F , Slomian J , et al. The effects of vitamin D on skeletal muscle strength, muscle mass, and muscle power: a systematic review and meta-analysis of randomized controlled trials. J Clin Endocrinol Metab . 2014;99(11):4336–4345. doi:10.1210/jc.2014-1742 25033068
   PubMed Web of Science ®Google Scholar
• Antoniak AE , Greig CA . The effect of combined resistance exercise training and vitamin D(3) supplementation on musculoskeletal health and function in older adults: a systematic review and meta-analysis. BMJ Open . 2017;7(7):e014619–e014619. doi:10.1136/bmjopen-2016-014619
   Web of Science ®Google Scholar
• Mousa A , Naderpoor N , de Courten MP , et al. Vitamin D supplementation has no effect on insulin sensitivity or secretion in vitamin D-deficient, overweight or obese adults: a randomized placebo-controlled trial. Am J Clin Nutr . 2017;105(6):1372–1381. doi:10.3945/ajcn.117.152736 28490514
   PubMed Web of Science ®Google Scholar
• Gulseth HL , Wium C , Angel K , Eriksen EF , Birkeland KI . Effects of vitamin D supplementation on insulin sensitivity and insulin secretion in subjects with type 2 diabetes and vitamin D deficiency: a randomized controlled trial. Diabetes Care . 2017;40(7):872–878. doi:10.2337/dc16-2302 28468770
   PubMed Web of Science ®Google Scholar
• Lee CJ , Iyer G , Liu Y , et al. The effect of vitamin D supplementation on glucose metabolism in type 2 diabetes mellitus: a systematic review and meta-analysis of intervention studies. J Diabetes Complications . 2017;31(7):1115–1126. doi:10.1016/j.jdiacomp.2017.04.019 28483335
   PubMed Web of Science ®Google Scholar
• Wu C , Qiu S , Zhu X , Li L . Vitamin D supplementation and glycemic control in type 2 diabetes patients: a systematic review and meta-analysis. Metabolism . 2017;73:67–76. doi:10.1016/j.metabol.2017.05.006 28732572
   PubMed Web of Science ®Google Scholar
• Hu Z , Chen J , Sun X , Wang L , Wang A . Efficacy of vitamin D supplementation on glycemic control in type 2 diabetes patients: a meta-analysis of interventional studies. Medicine (Baltimore) . 2019;98(14):e14970. doi:10.1097/MD.0000000000014970 30946322
   PubMed Web of Science ®Google Scholar
• Jamka M , Woźniewicz M , Jeszka J , Mardas M , Bogdański P , Stelmach-Mardas M . The effect of vitamin D supplementation on insulin and glucose metabolism in overweight and obese individuals: systematic review with meta-analysis. Sci Rep . 2015;5:16142. doi:10.1038/srep16142 26543018
   PubMed Web of Science ®Google Scholar
• Smith GI , Atherton P , Reeds DN , et al. Dietary omega-3 fatty acid supplementation increases the rate of muscle protein synthesis in older adults: a randomized controlled trial. Am J Clin Nutr . 2011;93(2):402–412. doi:10.3945/ajcn.110.005611 21159787
   PubMed Web of Science ®Google Scholar
• Kiecolt-Glaser JK , Belury MA , Andridge R , Malarkey WB , Hwang BS , Glaser R . Omega-3 supplementation lowers inflammation in healthy middle-aged and older adults: A randomized controlled trial. Brain Behav Immun . 2012;26(6):988–995. doi:10.1016/j.bbi.2012.05.011 22640930
   PubMed Web of Science ®Google Scholar
• Hutchins-Wiese HL , Kleppinger A , Annis K , et al. The impact of supplemental n-3 long chain polyunsaturated fatty acids and dietary antioxidants on physical performance in postmenopausal women. J Nutr Health Aging . 2013;17(1):76–80. doi:10.1007/s12603-012-0415-3 23299384
   PubMed Web of Science ®Google Scholar
• Smith GI , Julliand S , Reeds DN , Sinacore DR , Klein S , Mittendorfer B . Fish oil-derived n-3 PUFA therapy increases muscle mass and function in healthy older adults. Am J Clin Nutr . 2015;102(1):115–122. doi:10.3945/ajcn.114.105833 25994567
   PubMed Web of Science ®Google Scholar
• Krzyminska-Siemaszko R , Czepulis N , Lewandowicz M , et al. The effect of a 12-week omega-3 supplementation on body composition, muscle strength and physical performance in elderly individuals with decreased muscle mass. Int J Environ Res Public Health . 2015;12(9):10558–10574. doi:10.3390/ijerph120910558 26343698
   PubMed Web of Science ®Google Scholar
• Sneddon AA , Tsofliou F , Fyfe CL , et al. Effect of a conjugated linoleic acid and omega-3 fatty acid mixture on body composition and adiponectin. Obesity (Silver Spring) . 2008;16(5):1019–1024. doi:10.1038/oby.2008.41 18356842
   PubMed Web of Science ®Google Scholar
• Cornish SM , Chilibeck PD . Alpha-linolenic acid supplementation and resistance training in older adults. Appl Physiol Nutr Metab . 2009;34(1):49–59. doi:10.1139/H08-136 19234585
   PubMed Web of Science ®Google Scholar
• Gharekhani A , Dashti-Khavidaki S , Lessan-Pezeshki M , Khatami MR . Potential effects of omega-3 fatty acids on insulin resistance and lipid profile in maintenance hemodialysis patients: a randomized placebo-controlled trial. Iran J Kidney Dis . 2016;10(5):310–318.27721230
   PubMed Web of Science ®Google Scholar
• Wu JHY , Micha R , Imamura F , et al. Omega-3 fatty acids and incident type 2 diabetes: a systematic review and meta-analysis. Br J Nutr . 2012;107 Suppl 2(0 2):S214–S227. doi:10.1017/S0007114512001602 22591895
   PubMed Web of Science ®Google Scholar