Diabetes and sarcopenia often coexist in older adults, suggesting a possible bidirectional association. Available bedside measures of muscle mass consist of bedside ultrasound (MT, quadriceps muscle thickness) and Bioelectrical Impedance Analysis (BIA). We examined the association between ultrasound measures and BIA measures of muscle in older adults with measures of strength, performance and frailty in older adults with diabetes.
Cross-sectional study.
81 subjects (age ≥ 65; mean age 80.8 ± 0.6 years, 27 women, 53 men) were recruited sequentially from geriatric medicine clinics. Each subject had Lean Body Mass (LBM, by BIA, in kg), grip strength, gait speed, Cardiovascular Health Study index (frailty) and MT (in cm) measured. All initial models were adjusted for biological sex.
In our final parsimonious models, only MT (as opposed to LBM) showed a significant correlation with grip strength (Standardized β = 0.217 ± 0.078; p = 0.007) and frailty (Standardized β = 0.276 ± 0.109; p = 0.013). Neither MT or LBM showed a significant association with subject performance (gait speed).
Unlike BIA, bedside ultrasound measures of muscle thickness showed strong associations with both grip strength and frailty in the older adult population with diabetes, suggesting that bedside measures of MT might be a more clinically useful modality to assess muscularity in this patient population. Neither BIA or MT measures of subject muscularity showed any association with our performance indicator (gait speed).
Citation: Kenneth M. Madden, Boris Feldman, Shane Arishenkoff, Graydon S. Meneilly. Bedside tests of muscle mass in older adults with Type 2 diabetes[J]. AIMS Medical Science, 2022, 9(3): 433-446. doi: 10.3934/medsci.2022022
Diabetes and sarcopenia often coexist in older adults, suggesting a possible bidirectional association. Available bedside measures of muscle mass consist of bedside ultrasound (MT, quadriceps muscle thickness) and Bioelectrical Impedance Analysis (BIA). We examined the association between ultrasound measures and BIA measures of muscle in older adults with measures of strength, performance and frailty in older adults with diabetes.
Cross-sectional study.
81 subjects (age ≥ 65; mean age 80.8 ± 0.6 years, 27 women, 53 men) were recruited sequentially from geriatric medicine clinics. Each subject had Lean Body Mass (LBM, by BIA, in kg), grip strength, gait speed, Cardiovascular Health Study index (frailty) and MT (in cm) measured. All initial models were adjusted for biological sex.
In our final parsimonious models, only MT (as opposed to LBM) showed a significant correlation with grip strength (Standardized β = 0.217 ± 0.078; p = 0.007) and frailty (Standardized β = 0.276 ± 0.109; p = 0.013). Neither MT or LBM showed a significant association with subject performance (gait speed).
Unlike BIA, bedside ultrasound measures of muscle thickness showed strong associations with both grip strength and frailty in the older adult population with diabetes, suggesting that bedside measures of MT might be a more clinically useful modality to assess muscularity in this patient population. Neither BIA or MT measures of subject muscularity showed any association with our performance indicator (gait speed).
Dual-energy X-ray absorptiometry
Lean body mass
Bioelectrical impedance analysis
Cardiovascular health study Index
Quadriceps muscle tissue thickness
Akaike's Information Criterion
Glycated hemoglobin
Body mass index
[1] | Dent E, Morley JE, Cruz-Jentoft AJ, et al. (2018) International clinical practice guidelines for sarcopenia (ICFSR): screening, diagnosis and management. J Nutr Health Aging 22: 1148-1161. https://doi.org/10.1007/s12603-018-1139-9 |
[2] | Cruz-Jentoft AJ, Bahat G, Bauer J, et al. (2019) Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 48: 16-31. https://doi.org/10.1093/ageing/afy169 |
[3] | Cederholm T, Cruz-Jentoft AJ, Maggi S (2013) Sarcopenia and fragility fractures. Eur J Phys Rehabil Med 49: 111-117. |
[4] | Janssen I, Shepard DS, Katzmarzyk PT, et al. (2004) The healthcare costs of sarcopenia in the United States. J Am Geriatr Soc 52: 80-85. https://doi.org/10.1111/j.1532-5415.2004.52014.x |
[5] | Manini TM, Clark BC (2012) Dynapenia and aging: an update. J Gerontol A Biol Sci Med Sci 67: 28-40. https://doi.org/10.1093/gerona/glr010 |
[6] | Fielding RA, Vellas B, Evans WJ, et al. (2011) Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc 12: 249-256. https://doi.org/10.1016/j.jamda.2011.01.003 |
[7] | Cesari M, Landi F, Vellas B, et al. (2014) Sarcopenia and physical frailty: two sides of the same coin. Front Aging Neurosci 6: 192. https://doi.org/10.3389/fnagi.2014.00192 |
[8] | Ryerson B, Tierney EF, Thompson TJ, et al. (2003) Excess physical limitations among adults with diabetes in the US population, 1997–1999. Diabetes Care 26: 206-210. https://doi.org/10.2337/diacare.26.1.206 |
[9] | Kim TN, Park MS, Yang SJ, et al. (2010) Prevalence and determinant factors of sarcopenia in patients with type 2 diabetes: the Korean Sarcopenic Obesity Study (KSOS). Diabetes Care 33: 1497-1499. https://doi.org/10.2337/dc09-2310 |
[10] | Leenders M, Verdijk LB, van der Hoeven L, et al. (2013) Patients with type 2 diabetes show a greater decline in muscle mass, muscle strength, and functional capacity with aging. J Am Med Dir Assoc 14: 585-592. https://doi.org/10.1016/j.jamda.2013.02.006 |
[11] | Guglielmi G, Ponti F, Agostini M, et al. (2016) The role of DXA in sarcopenia. Aging Clin Exp Res 28: 1047-1060. https://doi.org/10.1007/s40520-016-0589-3 |
[12] | Derstine BA, Holcombe SA, Goulson RL, et al. (2017) Quantifying sarcopenia reference values using lumbar and thoracic muscle areas in a healthy population. J Nutr Health Aging 21: 180-185. https://doi.org/10.1007/s12603-017-0983-3 |
[13] | Madden KM, Feldman B, Arishenkoff S, et al. (2021) A rapid point-of-care ultrasound marker for muscle mass and muscle strength in older adults. Age Ageing 50: 505-510. https://doi.org/10.1093/ageing/afaa163 |
[14] | Gonzalez MC, Heymsfield SB (2017) Bioelectrical impedance analysis for diagnosing sarcopenia and cachexia: what are we really estimating?. J Cachexia Sarcopenia Muscle 8: 187-189. https://doi.org/10.1002/jcsm.12159 |
[15] | Kurinami N, Sugiyama S, Morita A, et al. (2018) Ratio of muscle mass to fat mass assessed by bioelectrical impedance analysis is significantly correlated with liver fat accumulation in patients with type 2 diabetes mellitus. Diabetes Res Clin Pract 139: 122-130. https://doi.org/10.1016/j.diabres.2018.02.009 |
[16] | Omura-Ohata Y, Son C, Makino H, et al. (2019) Efficacy of visceral fat estimation by dual bioelectrical impedance analysis in detecting cardiovascular risk factors in patients with type 2 diabetes. Cardiovasc Diabetol 18: 137. https://doi.org/10.1186/s12933-019-0941-y |
[17] | Tsui EY, Gao XJ, Zinman B (1998) Bioelectrical impedance analysis (BIA) using bipolar foot electrodes in the assessment of body composition in Type 2 diabetes mellitus. Diabet Med 15: 125-128. https://doi.org/10.1002/(SICI)1096-9136(199802)15:2<125::AID-DIA532>3.0.CO;2-N |
[18] | Madden KM, Feldman B, Arishenkoff S, et al. (2021) Point-of-care ultrasound measures of muscle and frailty measures. Eur Geriatr Med 12: 161-166. https://doi.org/10.1007/s41999-020-00401-3 |
[19] | American Diabetes Association.2. Classification and Diagnosis of Diabetes: Standards of Medical Care in Diabetes-2021. Diabetes Care (2021) 44: S15-S33. https://doi.org/10.2337/dc21-S002 |
[20] | Perkisas S, Baudry S, Bauer J, et al. (2018) Application of ultrasound for muscle assessment in sarcopenia: towards standardized measurements. Eur Geriatr Med 9: 739-757. https://doi.org/10.1007/s41999-018-0104-9 |
[21] | Strasser EM, Draskovits T, Praschak M, et al. (2013) Association between ultrasound measurements of muscle thickness, pennation angle, echogenicity and skeletal muscle strength in the elderly. Age 35: 2377-2388. https://doi.org/10.1007/s11357-013-9517-z |
[22] | Mirón Mombiela R, Facal de Castro F, Moreno P, et al. (2017) Ultrasonic echo intensity as a new noninvasive in vivo biomarker of frailty. J Am Geriatr Soc 65: 2685-2690. https://doi.org/10.1111/jgs.15002 |
[23] | Fried LP, Tangen CM, Walston J, et al. (2001) Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci 56: M146-M157. https://doi.org/10.1093/gerona/56.3.M146 |
[24] | Crawley MJ (2011) Statistics: An Introduction using R. West Sussex: Wiley. |
[25] | R Core TeamR: A language and environment for statistical computing (2019). Available from: https://www.r-project.org/ |
[26] | Craney TA, Surles JG (2002) Model-dependent variance inflation factor cutoff values. Qual Eng 14: 391-403. https://doi.org/10.1081/QEN-120001878 |
[27] | Park SW, Goodpaster BH, Lee JS, et al. (2009) Excessive loss of skeletal muscle mass in older adults with type 2 diabetes. Diabetes Care 32: 1993-1997. https://doi.org/10.2337/dc09-0264 |
[28] | Pereira S, Marliss EB, Morais JA, et al. (2008) Insulin resistance of protein metabolism in type 2 diabetes. Diabetes 57: 56-63. https://doi.org/10.2337/db07-0887 |
[29] | Mesinovic J, Zengin A, De Courten B, et al. (2019) Sarcopenia and type 2 diabetes mellitus: a bidirectional relationship. Diabetes Metab Syndr Obes 12: 1057-1072. https://doi.org/10.2147/DMSO.S186600 |
[30] | Morley JE, Malmstrom TK, Rodriguez-Mañas L, et al. (2014) Frailty, sarcopenia and diabetes. J Am Med Dir Assoc 15: 853-859. https://doi.org/10.1016/j.jamda.2014.10.001 |
[31] | van den Berg PJ, Daoudi K, Moens HJB, et al. (2017) Feasibility of photoacoustic/ultrasound imaging of synovitis in finger joints using a point-of-care system. Photoacoustics 8: 8-14. https://doi.org/10.1016/j.pacs.2017.08.002 |
[32] | Stawicki SP, Braslow BM, Panebianco NL, et al. (2009) Intensivist use of hand-carried ultrasonography to measure IVC collapsibility in estimating intravascular volume status: correlations with CVP. J Am Coll Surg 209: 55-61. https://doi.org/10.1016/j.jamcollsurg.2009.02.062 |
[33] | Lee M, Roberts JM, Chen L, et al. (2014) Estimation of spleen size with hand-carried ultrasound. J Ultrasound Med 33: 1225-1230. https://doi.org/10.7863/ultra.33.7.1225 |
[34] | Stringer HJ, Wilson D (2018) The role of ultrasound as a diagnostic tool for sarcopenia. J Frailty Aging 7: 258-261. https://doi.org/10.14283/jfa.2018.24 |
[35] | Leone AF, Schumacher SM, Krotish DE, et al. (2012) Geriatricians' interest to learn bedside portable ultrasound (GEBUS) for application in the clinical practice and in education. J Am Med Dir Assoc 13: 308.e7-308.e10. https://doi.org/10.1016/j.jamda.2011.06.002 |
[36] | Perez-Sousa MA, Venegas-Sanabria LC, Chavarro-Carvajal DA, et al. (2019) Gait speed as a mediator of the effect of sarcopenia on dependency in activities of daily living. J Cachexia Sarcopenia Muscle 10: 1009-1015. https://doi.org/10.1002/jcsm.12444 |
[37] | Toots ATM, Taylor ME, Lord SR, et al. (2019) Associations between gait speed and cognitive domains in older people with cognitive impairment. J Alzheimers Dis 71: S15-S21. https://doi.org/10.3233/JAD-181173 |
[38] | Pinter D, Ritchie SJ, Gattringer T, et al. (2018) Predictors of gait speed and its change over three years in community-dwelling older people. Aging 10: 144-153. https://doi.org/10.18632/aging.101365 |
[39] | Lipsitz LA, Manor B, Habtemariam D, et al. (2018) The pace and prognosis of peripheral sensory loss in advanced age: association with gait speed and falls. BMC Geriatr 18: 274. https://doi.org/10.1186/s12877-018-0970-5 |
[40] | Raspovic A (2013) Gait characteristics of people with diabetes-related peripheral neuropathy, with and without a history of ulceration. Gait Posture 38: 723-728. https://doi.org/10.1016/j.gaitpost.2013.03.009 |
[41] | White DK, Neogi T, Nevitt MC, et al. (2013) Trajectories of gait speed predict mortality in well-functioning older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci 68: 456-464. https://doi.org/10.1093/gerona/gls197 |
[42] | Veronese N, Stubbs B, Volpato S, et al. (2018) Association between gait speed with mortality, cardiovascular disease and cancer: a systematic review and meta-analysis of prospective cohort studies. J Am Med Dir Assoc 19: 981-988.e7. https://doi.org/10.1016/j.jamda.2018.06.007 |
[43] | Moisey LL, Mourtzakis M, Cotton BA, et al. (2013) Skeletal muscle predicts ventilator-free days, ICU-free days, and mortality in elderly ICU patients. Crit Care 17: R206. https://doi.org/10.1186/cc12901 |
[44] | Arango-Lopera VE, Arroyo P, Gutiérrez-Robledo LM, et al. (2013) Mortality as an adverse outcome of sarcopenia. J Nutr Health Aging 17: 259-262. https://doi.org/10.1007/s12603-012-0434-0 |
[45] | Tsekoura M, Kastrinis A, Katsoulaki M, et al. (2017) Sarcopenia and its impact on quality of life. Adv Exp Med Biol 987: 213-218. https://doi.org/10.1007/978-3-319-57379-3_19 |
[46] | Mithal A, Bonjour JP, Boonen S, et al. (2013) Impact of nutrition on muscle mass, strength, and performance in older adults. Osteoporos Int 24: 1555-1566. https://doi.org/10.1007/s00198-012-2236-y |
[47] | Deutz NE, Bauer JM, Barazzoni R, et al. (2014) Protein intake and exercise for optimal muscle function with aging: recommendations from the ESPEN Expert Group. Clin Nutr 33: 929-936. https://doi.org/10.1016/j.clnu.2014.04.007 |
[48] | Camporez JPG, Petersen MC, Abudukadier A, et al. (2016) Anti-myostatin antibody increases muscle mass and strength and improves insulin sensitivity in old mice. Proc Natl Acad Sci U S A 113: 2212-2217. https://doi.org/10.1073/pnas.1525795113 |
[49] | Bertakis KD, Azari R, Helms LJ, et al. (2000) Gender differences in the utilization of health care services. J Fam Pract 49: 147-152. |