Diabetes Metab J > Volume 40(3); 2016 > Article
Yoon and Jang: Response: Hyperglycemia Is Associated with Impaired Muscle Quality in Older Men with Diabetes: The Korean Longitudinal Study on Health and Aging (Diabetes Metab J 2016;40:140-6)
We thank Dr. Moon for his comments in response to our study, "Hyperglycemia is associated with impaired muscle quality in older men with diabetes: The Korean Longitudinal Study on Health and Aging" [1].
The definition of muscle quality is still incompletely established, with various definitions such as: muscle strength per unit muscle mass/cross sectional area (CSA) [2,3], the degree of intramuscular or intermuscular adipose tissue [4,5], muscle fiber type change [6], or histological changes (including myofibrosis and myosteatosis) [7]. Even though it has not reached a consensus yet, muscle strength per muscle mass/area has been widely used as a definition of functional muscle quality in previous studies [2,3,8,9]. As Dr. Moon mentioned, since intramuscular or intermuscular adipose tissue is associated with decreased muscle strength as well as insulin resistance [10,11,12], it is possible that the relationship between severe hyperglycemia and muscle quality impairment is not a cause and effect. Therefore, we performed further analyses in order to evaluate the relationships between muscular fat, insulin resistance, blood glucose level and muscle quality using data from 217 subjects who took a mid-thigh computed tomography scan. The mid-thigh fat (perimuscular subcutaneous fat+intermuscular fat) CSA, not intermuscular fat area or intramuscular fat, was the only measurement available. The mid-thigh muscle-to-fat CSA ratio showed a significant negative correlation with HOMA-IR (r=-0.169, P=0.013), but did not have a significant relationship with fasting blood glucose or glycosylated hemoglobin (HbA1c; r=0.066, P=0.332; r=-0.025, P=0.713, respectively). Moreover, there was no significant association between the mid-thigh muscle-fat ratio and muscle quality (r=0.004, P=0.954). With these results, it is less likely that intermuscular fat confounded the relationship between hyperglycemia and poor muscle quality in our study.
As pointed out by Dr. Moon, diabetic complications may contribute to the deterioration of muscle quality. Unfortunately, diabetic complications like peripheral artery disease and diabetic neuropathy were not evaluated in our study participants, and therefore the effects of these conditions could not be excluded. However, we investigated the history of angina pectoris and myocardial infarction, which could reflect the macrovascular complication status. Among the subjects with a history of myocardial infarction or angina pectoris, one (4.8%) was in HbA1c <6.5% group, three (9.7%) were in 6.5% ≤HbA1c <7.5% group, but no one was in 7.5% ≤ HbA1c<8.5% or HbA1c ≥8.5% group, in which the differences in prevalence were statistically insignificant. Subjects with a history of cerebrovascular disease were excluded from the analysis. Also, diabetic complications tend to increase with duration of the disease. According to an analysis of variance analysis, the duration of diabetes significantly differed among the groups with different glycemic control status; however, in the post-hoc analysis, the duration of diabetes mellitus in the subjects with HbA1c ≥8.5% (mean±standard deviation, 110±112 months) was not significantly different compared with that in the subjects with 6.5%≤HbA1c<7.5% (111±120 months) and 7.5%≤HbA1c<8.5% (171±199 months). Therefore, confounding by diabetic complication status is possible but may not be serious in our study.
Also, we hope a future study will demonstrate the clinical consequences of muscle quality impairment in the near future. We appreciate Dr. Moon for the valuable comments and suggestions.


CONFLICTS OF INTEREST: No potential conflict of interest relevant to this article was reported.


1. Yoon JW, Ha YC, Kim KM, Moon JH, Choi SH, Lim S, Park YJ, Lim JY, Kim KW, Park KS, Jang HC. Hyperglycemia is associated with impaired muscle quality in older men with diabetes: The Korean Longitudinal Study on Health and Aging. Diabetes Metab J 2016;40:140-146.
Article  PubMed  PMC 
2. Park SW, Goodpaster BH, Strotmeyer ES, de Rekeneire N, Harris TB, Schwartz AV, Tylavsky FA, Newman AB. Decreased muscle strength and quality in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes 2006;55:1813-1818.
Article  PubMed 
3. Kasai T, Ishiguro N, Matsui Y, Harada A, Takemura M, Yuki A, Kato Y, Otsuka R, Ando F, Shimokata H. Sex- and age-related differences in mid-thigh composition and muscle quality determined by computed tomography in middle-aged and elderly Japanese. Geriatr Gerontol Int 2015;15:700-706.
Article  PubMed 
4. Bang E, Tanabe K, Yokoyama N, Chijiki S, Kuno S. Relationship between thigh intermuscular adipose tissue accumulation and number of metabolic syndrome risk factors in middle-aged and older Japanese adults. Exp Gerontol 2016;79:26-30.
5. Therkelsen KE, Pedley A, Hoffmann U, Fox CS, Murabito JM. Intramuscular fat and physical performance at the Framingham Heart Study. Age (Dordr) 2016;38:31
PubMed  PMC 
6. van de Bool C, Gosker HR, van den Borst B, Op den Kamp CM, Slot IG, Schols AM. Muscle quality is more impaired in sarcopenic patients with chronic obstructive pulmonary disease. J Am Med Dir Assoc 2016;17:415-420.
Article  PubMed 
7. Zoico E, Corzato F, Bambace C, Rossi AP, Micciolo R, Cinti S, Harris TB, Zamboni M. Myosteatosis and myofibrosis: relationship with aging, inflammation and insulin resistance. Arch Gerontol Geriatr 2013;57:411-416.
PubMed  PMC 
8. Francis P, Toomey C, Mc Cormack W, Lyons M, Jakeman P. Measurement of maximal isometric torque and muscle quality of the knee extensors and flexors in healthy 50- to 70-year-old women. Clin Physiol Funct Imaging 2016 1 7 [Epub].
9. Senechal M, Johannsen NM, Swift DL, Earnest CP, Lavie CJ, Blair SN, Church TS. Association between changes in muscle quality with exercise training and changes in cardiorespiratory fitness measures in individuals with type 2 diabetes mellitus: results from the HART-D study. PLoS One 2015;10:e0135057
PubMed  PMC 
10. Brumbaugh DE, Crume TL, Nadeau K, Scherzinger A, Dabelea D. Intramyocellular lipid is associated with visceral adiposity, markers of insulin resistance, and cardiovascular risk in prepubertal children: the EPOCH study. J Clin Endocrinol Metab 2012;97:E1099-E1105.
11. Ryan AS, Buscemi A, Forrester L, Hafer-Macko CE, Ivey FM. Atrophy and intramuscular fat in specific muscles of the thigh: associated weakness and hyperinsulinemia in stroke survivors. Neurorehabil Neural Repair 2011;25:865-872.
12. Rahemi H, Nigam N, Wakeling JM. The effect of intramuscular fat on skeletal muscle mechanics: implications for the elderly and obese. J R Soc Interface 2015;12:20150365

Editorial Office
101-2104, Lotte Castle President, 109 Mapo-daero, Mapo-gu, Seoul 04146, Korea​
Tel: +82-2-714-9064    Fax: +82-2-714-9084    E-mail: diabetes@kams.or.kr                

Copyright © 2022 by Korean Diabetes Association.

Developed in M2PI

Close layer