MUSCLE MITOCHONDRIAL CAPACITY AND ENDURANCE IN ADULTS WITH TYPE 1 DIABETES
Main Article Content
Abstract
The impact of type 1 diabetes (T1D) on muscle endurance and oxidative capacity is currently unknown. Purpose: Measure muscle endurance and oxidative capacity of adults with T1D compared to controls. Methods: A cross-sectional study design with a control group was used. Subjects (19-37 years old) with T1D (n=17) and controls (n=17) were assessed with hemoglobin A1c (HbA1c) and casual glucose. Muscle endurance was measured with an accelerometer at stimulation frequencies of 2, 4, and 6 Hz for a total of nine minutes. Mitochondrial capacity was measured using near-infrared spectroscopy after exercise as the rate constant of the rate of recovery of oxygen consumption. Results: T1D and control groups were similar in age, sex, height, and race. The T1D group had slightly higher BMI values and adipose tissue thickness over the forearm muscles. Casual glucose was 150+70 mg/dL for T1D and 98+16 mg/dL for controls (P=0.006). HbA1c of T1D subjects was 7.1+0.9% and 5.0+0.4% for controls (P<0.01). Endurance indexes at 2, 4, and 6 Hz were 94.5+5.2%, 81.8+8.4%, and 68.6+13.5% for T1D and 94.6+4.1%, 85.9+6.3%, and 68.7+15.4% for controls (p = 0.97, 0.12, 0.99, respectively). There were no differences between groups in mitochondrial capacity (T1D= 1.9+0.5 min-1 and control=1.8+0.4 min-1, P=0.29) or reperfusion rate (T1D= 8.8+2.8s and control=10.3+3.0s, P=0.88). There were no significant correlations between HbA1c and either muscle endurance, mitochondrial capacity or reperfusion rate. Conclusions: Adults with T1D did not have reduced oxidative capacity, muscle endurance or muscle reperfusion rates compared to controls. HbA1c also did not correlate with muscle endurance, mitochondrial capacity or reperfusion rates. Future studies should extend these measurements to older people or people with poorly-controlled T1D.
Keywords:
Near Infrared Spectroscopy (NIRS), Electrical Stimulation, skeletal muscle, Fatigability
Article Details
How to Cite
HEWGLEY, Riley A et al.
MUSCLE MITOCHONDRIAL CAPACITY AND ENDURANCE IN ADULTS WITH TYPE 1 DIABETES.
Medical Research Archives, [S.l.], v. 8, n. 2, feb. 2020.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/2049>. Date accessed: 22 nov. 2024.
doi: https://doi.org/10.18103/mra.v8i2.2049.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
References
1. Horton WB, Subauste JS. Care of the Athlete With Type 1 Diabetes Mellitus: A Clinical Review. Int J Endocrinol Metab. 2016;14(2):e36091.
2. Vaid S, Hanks L, Griffin R, Ashraf AP. Body mass index and glycemic control influence lipoproteins in children with type 1 diabetes. J Clin Lipidol. 2016;10(5):1240-1247.
3. Chen X, Wei S, Yang F. Mitochondria in the pathogenesis of diabetes: a proteomic view. Protein Cell. 2012;3(9):648-660.
4. Cree-Green M, Newcomer BR, Brown MS, et al. Delayed skeletal muscle mitochondrial ADP recovery in youth with type 1 diabetes relates to muscle insulin resistance. Diabetes. 2015;64(2):383-392.
5. Zhao D, Yang J, Yang L. Insights for Oxidative Stress and mTOR Signaling in Myocardial Ischemia/Reperfusion Injury under Diabetes. Oxid Med Cell Longev. 2017;2017:6437467.
6. Menting J, Nikolaus S, van der Veld WM, Goedendorp MM, Tack CJ, Knoop H. Severe fatigue in type 1 diabetes: Exploring its course, predictors and relationship with HbA1c in a prospective study. Diabetes Res Clin Pract. 2016;121:127-134.
7. Amaral S, Oliveira PJ, Ramalho-Santos J. Diabetes and the impairment of reproductive function: possible role of mitochondria and reactive oxygen species. Curr Diabetes Rev. 2008;4(1):46-54.
8. Krause MP, Riddell MC, Hawke TJ. Effects of type 1 diabetes mellitus on skeletal muscle: clinical observations and physiological mechanisms. Pediatr Diabetes. 2011;12(4 Pt 1):345-364.
9. Andreassen CS, Jakobsen J, Flyvbjerg A, Andersen H. Expression of neurotrophic factors in diabetic muscle--relation to neuropathy and muscle strength. Brain. 2009;132(Pt 10):2724-2733.
10. Bossie HM, Willingham TB, Schoick RAV, O'Connor PJ, McCully KK. Mitochondrial capacity, muscle endurance, and low energy in friedreich ataxia. Muscle Nerve. 2017;56(4):773-779.
11. McCully KK, Prins P, Mistry K, Willingham TB. Muscle-specific endurance of the trapezius muscles using electrical twitch mechanomyography. Shoulder Elbow. 2018;10(2):136-143.
12. Willingham TB, McCully KK. Assessment of Muscle Fatigue during Twitch Electrical Stimulation using Accelerometer-based Mechanomyography. Advances in Skeletal Muscle Function Assessment. 2017;1(2):14-20.
13. Bystrom S, Kilbom A. Electrical stimulation of human forearm extensor muscles as an indicator of handgrip fatigue and recovery. Eur J Appl Physiol Occup Physiol. 1991;62(5):363-368.
14. Hamaoka T, McCully KK, Quaresima V, Yamamoto K, Chance B. Near-infrared spectroscopy/imaging for monitoring muscle oxygenation and oxidative metabolism in healthy and diseased humans. J Biomed Opt. 2007;12(6):062105.
15. Motobe M, Murase N, Osada T, et al. Noninvasive monitoring of deterioration in skeletal muscle function with forearm cast immobilization and the prevention of deterioration. Dyn Med. 2004;3(1):2.
16. Willingham TB, McCully KK. In Vivo Assessment of Mitochondrial Dysfunction in Clinical Populations using Near-Infrared Spectroscopy. Frontiers in Physiology. 2017;8(689):1-11.
17. DeBlasi R, Ferrari M, Natali A, Conti G, Mega A, Gasparetto A. Noninvasive measurement of forearm blood flow and oxygen consumption by near-infrared spectroscopy. Journal Applied Physiology. 1994;76:1388-1393.
18. Ryan TE, Erickson ML, Young HJ, McCully KK. Case report: endurance electrical stimulation training improves skeletal muscle oxidative capacity in chronic spinal cord injury. Arch Phys Med Rehabil. 2013;94(12):2559-2561.
19. McCully KK, Halber C, Posner JD. Exercise-induced changes in oxygen saturation in the calf muscles of elderly subjects with peripheral vascular disease. Journal of gerontology. 1994;49(3):B128-134.
20. Ryan TE, Brizendine JT, McCully KK. A comparison of exercise type and intensity on the noninvasive assessment of skeletal muscle mitochondrial function using near-infrared spectroscopy. J Appl Physiol. 2013;114(2):230-237.
21. Willingham TB, Southern WM, McCully KK. Measuring reactive hyperemia in the lower limb using near-infrared spectroscopy. J Biomed Opt. 2016;21(9):091302.
22. Southern WM, Ryan TE, Reynolds MA, McCully K. Reproducibility of near-infrared spectroscopy measurements of oxidative function and postexercise recovery kinetics in the medial gastrocnemius muscle. Appl Physiol Nutr Metab. 2014;39(5):521-529.
23. Zhu B, Martyn-Nemeth P, Ruggiero L, Park CG, Zhang Y, Fritschi C. Associations between fatigue, sleep disturbance and eating style in adults with type 2 diabetes: A correlational study. J Clin Nurs. 2019.
24. Park H, Park C, Quinn L, Fritschi C. Glucose control and fatigue in type 2 diabetes: the mediating roles of diabetes symptoms and distress. J Adv Nurs. 2015;71(7):1650-1660.
25. Fritschi C, Quinn L, Hacker ED, et al. Fatigue in women with type 2 diabetes. Diabetes Educ. 2012;38(5):662-672.
26. Fritschi C, Quinn L. Fatigue in patients with diabetes: a review. J Psychosom Res. 2010;69(1):33-41.
27. Kalra S, Sahay R. Diabetes Fatigue Syndrome. Diabetes Ther. 2018;9(4):1421-1429.
28. Monaco CMF, Gingrich MA, Hawke TJ. Considering Type 1 Diabetes as a Form of Accelerated Muscle Aging. Exerc Sport Sci Rev. 2019;47(2):98-107.
29. Ryan TE, Southern WM, Reynolds MA, McCully KK. A cross-validation of near-infrared spectroscopy measurements of skeletal muscle oxidative capacity with phosphorus magnetic resonance spectroscopy. J Appl Physiol (1985). 2013;115(12):1757-1766.
30. Hill NE, Campbell C, Buchanan P, Knight M, Godsland IF, Oliver NS. Biochemical, Physiological and Psychological Changes During Endurance Exercise in People With Type 1 Diabetes. J Diabetes Sci Technol. 2017;11(3):529-536.
31. Harmer AR, Ruell PA, Hunter SK, et al. Effects of type 1 diabetes, sprint training and sex on skeletal muscle sarcoplasmic reticulum Ca2+ uptake and Ca2+-ATPase activity. J Physiol. 2014;592(3):523-535.
32. Babar GS, Zidan H, Widlansky ME, et al. Impaired Endothelial Function in Preadolescent Children With Type 1 Diabetes. Diabetes Care. 2011.
33. Bjarnegard N, Arnqvist HJ, Lindstrom T, Jonasson L, Jonsson A, Lanne T. Long-term hyperglycaemia impairs vascular smooth muscle cell function in women with type 1 diabetes mellitus. Diab Vasc Dis Res. 2009;6(1):25-31.
34. McCully K, Halber C, Posner J. Exercise-induced changes in oxygen saturation in the calf muscles of elderly subjects with peripheral vascular disease. Journal of Gerontology. 1994;49(3):B128-B134.
35. McCully K, Landsberg L, Suarez M, Hofmann M, Posner J. Identification of peripheral vascular disease in elderly subjects with optical spectroscopy. Journal of Gerontology: Biological Sciences. 1997;52A:B159-B165.
36. Cameron JD, Bulpitt CJ, Pinto ES, Rajkumar C. The Aging of Elastic and Muscular Arteries: A comparison of diabetic and nondiabetic subjects. Diabetes Care. 2003;26(7):2133-2138.
37. Ce GV, Rohde LE, Silva AM, Coutinho MK, Castro AC, Bertoluci MC. Endothelial Dysfunction Is Related to Poor Glycemic Control in Adolescents with Type 1 Diabetes under 5 Years of Disease: Evidence of Metabolic Memory. J Clin Endocrinol Metab. 2011.
38. Bazzano LA, Serdula MK, Liu S. Dietary intake of fruits and vegetables and risk of cardiovascular disease. Curr Atheroscler Rep. 2003;5(6):492-499.
39. Black PH. The inflammatory response is an integral part of the stress response: Implications for atherosclerosis, insulin resistance, type II diabetes and metabolic syndrome X. Brain, Behavior, and Immunity. 2003;17(5):350-364.
40. Ryan TE, Erickson ML, Brizendine JT, Young HJ, McCully KK. Noninvasive evaluation of skeletal muscle mitochondrial capacity with near-infrared spectroscopy: correcting for blood volume changes. J Appl Physiol. 2012;113(2):175-183.
41. Erickson ML, Ryan TE, Young HJ, McCully KK. Near-infrared assessments of skeletal muscle oxidative capacity in persons with spinal cord injury. Eur J Appl Physiol. 2013;113(9):2275-2283.
42. Befroy DE, Falk Petersen K, Rothman DL, Shulman GI. Assessment of in vivo mitochondrial metabolism by magnetic resonance spectroscopy. Methods Enzymol. 2009;457:373-393.
43. Ryan TE, Southern WM, Brizendine JT, McCully KK. Activity-induced changes in skeletal muscle metabolism measured with optical spectroscopy. Med Sci Sports Exerc. 2013;45(12):2346-2352.
1. Horton WB, Subauste JS. Care of the Athlete With Type 1 Diabetes Mellitus: A Clinical Review. Int J Endocrinol Metab. 2016;14(2):e36091.
2. Vaid S, Hanks L, Griffin R, Ashraf AP. Body mass index and glycemic control influence lipoproteins in children with type 1 diabetes. J Clin Lipidol. 2016;10(5):1240-1247.
3. Chen X, Wei S, Yang F. Mitochondria in the pathogenesis of diabetes: a proteomic view. Protein Cell. 2012;3(9):648-660.
4. Cree-Green M, Newcomer BR, Brown MS, et al. Delayed skeletal muscle mitochondrial ADP recovery in youth with type 1 diabetes relates to muscle insulin resistance. Diabetes. 2015;64(2):383-392.
5. Zhao D, Yang J, Yang L. Insights for Oxidative Stress and mTOR Signaling in Myocardial Ischemia/Reperfusion Injury under Diabetes. Oxid Med Cell Longev. 2017;2017:6437467.
6. Menting J, Nikolaus S, van der Veld WM, Goedendorp MM, Tack CJ, Knoop H. Severe fatigue in type 1 diabetes: Exploring its course, predictors and relationship with HbA1c in a prospective study. Diabetes Res Clin Pract. 2016;121:127-134.
7. Amaral S, Oliveira PJ, Ramalho-Santos J. Diabetes and the impairment of reproductive function: possible role of mitochondria and reactive oxygen species. Curr Diabetes Rev. 2008;4(1):46-54.
8. Krause MP, Riddell MC, Hawke TJ. Effects of type 1 diabetes mellitus on skeletal muscle: clinical observations and physiological mechanisms. Pediatr Diabetes. 2011;12(4 Pt 1):345-364.
9. Andreassen CS, Jakobsen J, Flyvbjerg A, Andersen H. Expression of neurotrophic factors in diabetic muscle--relation to neuropathy and muscle strength. Brain. 2009;132(Pt 10):2724-2733.
10. Bossie HM, Willingham TB, Schoick RAV, O'Connor PJ, McCully KK. Mitochondrial capacity, muscle endurance, and low energy in friedreich ataxia. Muscle Nerve. 2017;56(4):773-779.
11. McCully KK, Prins P, Mistry K, Willingham TB. Muscle-specific endurance of the trapezius muscles using electrical twitch mechanomyography. Shoulder Elbow. 2018;10(2):136-143.
12. Willingham TB, McCully KK. Assessment of Muscle Fatigue during Twitch Electrical Stimulation using Accelerometer-based Mechanomyography. Advances in Skeletal Muscle Function Assessment. 2017;1(2):14-20.
13. Bystrom S, Kilbom A. Electrical stimulation of human forearm extensor muscles as an indicator of handgrip fatigue and recovery. Eur J Appl Physiol Occup Physiol. 1991;62(5):363-368.
14. Hamaoka T, McCully KK, Quaresima V, Yamamoto K, Chance B. Near-infrared spectroscopy/imaging for monitoring muscle oxygenation and oxidative metabolism in healthy and diseased humans. J Biomed Opt. 2007;12(6):062105.
15. Motobe M, Murase N, Osada T, et al. Noninvasive monitoring of deterioration in skeletal muscle function with forearm cast immobilization and the prevention of deterioration. Dyn Med. 2004;3(1):2.
16. Willingham TB, McCully KK. In Vivo Assessment of Mitochondrial Dysfunction in Clinical Populations using Near-Infrared Spectroscopy. Frontiers in Physiology. 2017;8(689):1-11.
17. DeBlasi R, Ferrari M, Natali A, Conti G, Mega A, Gasparetto A. Noninvasive measurement of forearm blood flow and oxygen consumption by near-infrared spectroscopy. Journal Applied Physiology. 1994;76:1388-1393.
18. Ryan TE, Erickson ML, Young HJ, McCully KK. Case report: endurance electrical stimulation training improves skeletal muscle oxidative capacity in chronic spinal cord injury. Arch Phys Med Rehabil. 2013;94(12):2559-2561.
19. McCully KK, Halber C, Posner JD. Exercise-induced changes in oxygen saturation in the calf muscles of elderly subjects with peripheral vascular disease. Journal of gerontology. 1994;49(3):B128-134.
20. Ryan TE, Brizendine JT, McCully KK. A comparison of exercise type and intensity on the noninvasive assessment of skeletal muscle mitochondrial function using near-infrared spectroscopy. J Appl Physiol. 2013;114(2):230-237.
21. Willingham TB, Southern WM, McCully KK. Measuring reactive hyperemia in the lower limb using near-infrared spectroscopy. J Biomed Opt. 2016;21(9):091302.
22. Southern WM, Ryan TE, Reynolds MA, McCully K. Reproducibility of near-infrared spectroscopy measurements of oxidative function and postexercise recovery kinetics in the medial gastrocnemius muscle. Appl Physiol Nutr Metab. 2014;39(5):521-529.
23. Zhu B, Martyn-Nemeth P, Ruggiero L, Park CG, Zhang Y, Fritschi C. Associations between fatigue, sleep disturbance and eating style in adults with type 2 diabetes: A correlational study. J Clin Nurs. 2019.
24. Park H, Park C, Quinn L, Fritschi C. Glucose control and fatigue in type 2 diabetes: the mediating roles of diabetes symptoms and distress. J Adv Nurs. 2015;71(7):1650-1660.
25. Fritschi C, Quinn L, Hacker ED, et al. Fatigue in women with type 2 diabetes. Diabetes Educ. 2012;38(5):662-672.
26. Fritschi C, Quinn L. Fatigue in patients with diabetes: a review. J Psychosom Res. 2010;69(1):33-41.
27. Kalra S, Sahay R. Diabetes Fatigue Syndrome. Diabetes Ther. 2018;9(4):1421-1429.
28. Monaco CMF, Gingrich MA, Hawke TJ. Considering Type 1 Diabetes as a Form of Accelerated Muscle Aging. Exerc Sport Sci Rev. 2019;47(2):98-107.
29. Ryan TE, Southern WM, Reynolds MA, McCully KK. A cross-validation of near-infrared spectroscopy measurements of skeletal muscle oxidative capacity with phosphorus magnetic resonance spectroscopy. J Appl Physiol (1985). 2013;115(12):1757-1766.
30. Hill NE, Campbell C, Buchanan P, Knight M, Godsland IF, Oliver NS. Biochemical, Physiological and Psychological Changes During Endurance Exercise in People With Type 1 Diabetes. J Diabetes Sci Technol. 2017;11(3):529-536.
31. Harmer AR, Ruell PA, Hunter SK, et al. Effects of type 1 diabetes, sprint training and sex on skeletal muscle sarcoplasmic reticulum Ca2+ uptake and Ca2+-ATPase activity. J Physiol. 2014;592(3):523-535.
32. Babar GS, Zidan H, Widlansky ME, et al. Impaired Endothelial Function in Preadolescent Children With Type 1 Diabetes. Diabetes Care. 2011.
33. Bjarnegard N, Arnqvist HJ, Lindstrom T, Jonasson L, Jonsson A, Lanne T. Long-term hyperglycaemia impairs vascular smooth muscle cell function in women with type 1 diabetes mellitus. Diab Vasc Dis Res. 2009;6(1):25-31.
34. McCully K, Halber C, Posner J. Exercise-induced changes in oxygen saturation in the calf muscles of elderly subjects with peripheral vascular disease. Journal of Gerontology. 1994;49(3):B128-B134.
35. McCully K, Landsberg L, Suarez M, Hofmann M, Posner J. Identification of peripheral vascular disease in elderly subjects with optical spectroscopy. Journal of Gerontology: Biological Sciences. 1997;52A:B159-B165.
36. Cameron JD, Bulpitt CJ, Pinto ES, Rajkumar C. The Aging of Elastic and Muscular Arteries: A comparison of diabetic and nondiabetic subjects. Diabetes Care. 2003;26(7):2133-2138.
37. Ce GV, Rohde LE, Silva AM, Coutinho MK, Castro AC, Bertoluci MC. Endothelial Dysfunction Is Related to Poor Glycemic Control in Adolescents with Type 1 Diabetes under 5 Years of Disease: Evidence of Metabolic Memory. J Clin Endocrinol Metab. 2011.
38. Bazzano LA, Serdula MK, Liu S. Dietary intake of fruits and vegetables and risk of cardiovascular disease. Curr Atheroscler Rep. 2003;5(6):492-499.
39. Black PH. The inflammatory response is an integral part of the stress response: Implications for atherosclerosis, insulin resistance, type II diabetes and metabolic syndrome X. Brain, Behavior, and Immunity. 2003;17(5):350-364.
40. Ryan TE, Erickson ML, Brizendine JT, Young HJ, McCully KK. Noninvasive evaluation of skeletal muscle mitochondrial capacity with near-infrared spectroscopy: correcting for blood volume changes. J Appl Physiol. 2012;113(2):175-183.
41. Erickson ML, Ryan TE, Young HJ, McCully KK. Near-infrared assessments of skeletal muscle oxidative capacity in persons with spinal cord injury. Eur J Appl Physiol. 2013;113(9):2275-2283.
42. Befroy DE, Falk Petersen K, Rothman DL, Shulman GI. Assessment of in vivo mitochondrial metabolism by magnetic resonance spectroscopy. Methods Enzymol. 2009;457:373-393.
43. Ryan TE, Southern WM, Brizendine JT, McCully KK. Activity-induced changes in skeletal muscle metabolism measured with optical spectroscopy. Med Sci Sports Exerc. 2013;45(12):2346-2352.