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Erschienen in: European Journal of Applied Physiology 11/2017

01.09.2017 | Original Article

Skeletal muscle mitochondrial mass is linked to lipid and metabolic profile in individuals with spinal cord injury

verfasst von: Laura C. O’Brien, Qun Chen, Jeannie Savas, Edward J. Lesnefsky, Ashraf S. Gorgey

Erschienen in: European Journal of Applied Physiology | Ausgabe 11/2017

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Abstract

Purpose

Changes in metabolism and body composition after spinal cord injury (SCI) predispose individuals to obesity, type II diabetes, and cardiovascular disease. A link between lean mass and skeletal muscle mitochondrial mass has been reported but it is unknown how skeletal muscle mitochondrial mass and activity impact metabolic health. This study examined the relationship between skeletal muscle mitochondrial mass, activity and metabolic profile in individuals with chronic SCI.

Methods

Twenty-two men with motor complete SCI participated in the study. Citrate synthase (CS) and complex III (CIII) activity was measured in vastus lateralis biopsies. Metabolic profile was assessed by intravenous glucose tolerance test, basal metabolic rate (BMR), maximum oxygen uptake (VO2 peak) and blood lipid profile.

Results

Skeletal muscle CS activity was negatively related to the cholesterol:high density lipoprotein cholesterol (HDL-C) ratio and triglycerides (r = −0.60, p = 0.009; r = −0.64, p = 0.004, respectively). CS activity was positively related to insulin sensitivity and BMR (r = 0.67, p = 0.006; r = 0.64, p = 0.005, respectively). Similar relationships were found for CIII and metabolic profile, but not CIII normalized to CS. Many of the relationships between CS and metabolism remained significant when age, level of injury, or time since injury were accounted for. They also remained significant when CS activity was normalized to total lean mass.

Conclusions

These results suggest that an increase in skeletal muscle mitochondrial mass is associated with improved metabolic health independent of age, level of injury, or time since injury in individuals with chronic SCI. This highlights the importance of maintaining and improving mitochondrial health in individuals with SCI.
Literatur
Zurück zum Zitat Bauman WA, Spungen AM (1994) Disorders of carbohydrate and lipid metabolism in veterans with paraplegia or quadriplegia: a model of premature aging. Metabolism 43:749–756CrossRefPubMed Bauman WA, Spungen AM (1994) Disorders of carbohydrate and lipid metabolism in veterans with paraplegia or quadriplegia: a model of premature aging. Metabolism 43:749–756CrossRefPubMed
Zurück zum Zitat Bauman WA, Spungen AM (2001) Carbohydrate and lipid metabolism in chronic spinal cord injury. J Spinal Cord Med 24:266–277CrossRefPubMed Bauman WA, Spungen AM (2001) Carbohydrate and lipid metabolism in chronic spinal cord injury. J Spinal Cord Med 24:266–277CrossRefPubMed
Zurück zum Zitat Bauman WA, Spungen AM, Zhong YG, Rothstein JL, Petry C, Gordon SK (1992) Depressed serum high density lipoprotein cholesterol levels in veterans with spinal cord injury. Paraplegia 30:697–703. doi:10.1038/sc.1992.136 PubMed Bauman WA, Spungen AM, Zhong YG, Rothstein JL, Petry C, Gordon SK (1992) Depressed serum high density lipoprotein cholesterol levels in veterans with spinal cord injury. Paraplegia 30:697–703. doi:10.​1038/​sc.​1992.​136 PubMed
Zurück zum Zitat Bharadwaj MS, Tyrrell DJ, Lyles MF, Demons JL, Rogers GW, Molina AJ (2015) Preparation and respirometric assessment of mitochondria isolated from skeletal muscle tissue obtained by percutaneous needle biopsy. J Vis Exp. doi:10.3791/52350 PubMedPubMedCentral Bharadwaj MS, Tyrrell DJ, Lyles MF, Demons JL, Rogers GW, Molina AJ (2015) Preparation and respirometric assessment of mitochondria isolated from skeletal muscle tissue obtained by percutaneous needle biopsy. J Vis Exp. doi:10.​3791/​52350 PubMedPubMedCentral
Zurück zum Zitat Boston RC, Stefanovski D, Moate PJ, Sumner AE, Watanabe RM, Bergman RN (2003) MINMOD Millennium: a computer program to calculate glucose effectiveness and insulin sensitivity from the frequently sampled intravenous glucose tolerance test. Diabetes Technol Ther 5:1003–1015. doi:10.1089/152091503322641060 CrossRefPubMed Boston RC, Stefanovski D, Moate PJ, Sumner AE, Watanabe RM, Bergman RN (2003) MINMOD Millennium: a computer program to calculate glucose effectiveness and insulin sensitivity from the frequently sampled intravenous glucose tolerance test. Diabetes Technol Ther 5:1003–1015. doi:10.​1089/​1520915033226410​60 CrossRefPubMed
Zurück zum Zitat Brass EP, Hiatt WR, Gardner AW, Hoppel CL (2001) Decreased NADH dehydrogenase and ubiquinol-cytochrome c oxidoreductase in peripheral arterial disease. Am J Physiol Heart Circ Physiol 280:H603–H609PubMed Brass EP, Hiatt WR, Gardner AW, Hoppel CL (2001) Decreased NADH dehydrogenase and ubiquinol-cytochrome c oxidoreductase in peripheral arterial disease. Am J Physiol Heart Circ Physiol 280:H603–H609PubMed
Zurück zum Zitat Brown MS, Goldstein JL (1984) How LDL receptors influence cholesterol and atherosclerosis. Sci Am 251:58–66CrossRefPubMed Brown MS, Goldstein JL (1984) How LDL receptors influence cholesterol and atherosclerosis. Sci Am 251:58–66CrossRefPubMed
Zurück zum Zitat Buchholz AC, McGillivray CF, Pencharz PB (2003) Differences in resting metabolic rate between paraplegic and able-bodied subjects are explained by differences in body composition. Am J Clin Nutr 77:371–378PubMed Buchholz AC, McGillivray CF, Pencharz PB (2003) Differences in resting metabolic rate between paraplegic and able-bodied subjects are explained by differences in body composition. Am J Clin Nutr 77:371–378PubMed
Zurück zum Zitat Castro MJ, Apple DF Jr, Staron RS, Campos GE, Dudley GA (1999) Influence of complete spinal cord injury on skeletal muscle within 6 mo of injury. J Appl Physiol (1985) 86:350–358 Castro MJ, Apple DF Jr, Staron RS, Campos GE, Dudley GA (1999) Influence of complete spinal cord injury on skeletal muscle within 6 mo of injury. J Appl Physiol (1985) 86:350–358
Zurück zum Zitat Chilibeck PD et al (1999) Functional electrical stimulation exercise increases GLUT-1 and GLUT-4 in paralyzed skeletal muscle. Metabolism 48:1409–1413CrossRefPubMed Chilibeck PD et al (1999) Functional electrical stimulation exercise increases GLUT-1 and GLUT-4 in paralyzed skeletal muscle. Metabolism 48:1409–1413CrossRefPubMed
Zurück zum Zitat Chomentowski P, Coen PM, Radikova Z, Goodpaster BH, Toledo FG (2011) Skeletal muscle mitochondria in insulin resistance: differences in intermyofibrillar versus subsarcolemmal subpopulations and relationship to metabolic flexibility. J Clin Endocrinol Metab 96:494–503. doi:10.1210/jc.2010-0822 CrossRefPubMed Chomentowski P, Coen PM, Radikova Z, Goodpaster BH, Toledo FG (2011) Skeletal muscle mitochondria in insulin resistance: differences in intermyofibrillar versus subsarcolemmal subpopulations and relationship to metabolic flexibility. J Clin Endocrinol Metab 96:494–503. doi:10.​1210/​jc.​2010-0822 CrossRefPubMed
Zurück zum Zitat DeFronzo RA, Jacot E, Jequier E, Maeder E, Wahren J, Felber JP (1981) The effect of insulin on the disposal of intravenous glucose. Results from indirect calorimetry and hepatic and femoral venous catheterization. Diabetes 30:1000–1007CrossRefPubMed DeFronzo RA, Jacot E, Jequier E, Maeder E, Wahren J, Felber JP (1981) The effect of insulin on the disposal of intravenous glucose. Results from indirect calorimetry and hepatic and femoral venous catheterization. Diabetes 30:1000–1007CrossRefPubMed
Zurück zum Zitat Distefano G et al (2016) Chronological age does not influence ex-vivo mitochondrial respiration and quality control in skeletal muscle. J Gerontol A Biol Sci Med Sci. doi:10.1093/gerona/glw102 Distefano G et al (2016) Chronological age does not influence ex-vivo mitochondrial respiration and quality control in skeletal muscle. J Gerontol A Biol Sci Med Sci. doi:10.​1093/​gerona/​glw102
Zurück zum Zitat Duckworth WC, Solomon SS, Jallepalli P, Heckemeyer C, Finnern J, Powers A (1980) Glucose intolerance due to insulin resistance in patients with spinal cord injuries. Diabetes 29:906–910CrossRefPubMed Duckworth WC, Solomon SS, Jallepalli P, Heckemeyer C, Finnern J, Powers A (1980) Glucose intolerance due to insulin resistance in patients with spinal cord injuries. Diabetes 29:906–910CrossRefPubMed
Zurück zum Zitat Essén B, Jansson E, Henriksson J, Taylor AW, Saltin B (1975) Metabolic characteristics of fibre types in human skeletal muscle. Acta Physiol Scand 95(2):153–165CrossRefPubMed Essén B, Jansson E, Henriksson J, Taylor AW, Saltin B (1975) Metabolic characteristics of fibre types in human skeletal muscle. Acta Physiol Scand 95(2):153–165CrossRefPubMed
Zurück zum Zitat Essén-Gustavsson B, Henriksson J (1984) Enzyme levels in pools of microdissected human muscle fibers of identified type. Adaptive response to exercise. Acta Physiol Scand 120(4):505–515CrossRefPubMed Essén-Gustavsson B, Henriksson J (1984) Enzyme levels in pools of microdissected human muscle fibers of identified type. Adaptive response to exercise. Acta Physiol Scand 120(4):505–515CrossRefPubMed
Zurück zum Zitat Gorgey AS, Gater DR (2011) Regional and relative adiposity patterns in relation to carbohydrate and lipid metabolism in men with spinal cord injury. Appl Physiol Nutr Metab 36(1):107–114CrossRefPubMed Gorgey AS, Gater DR (2011) Regional and relative adiposity patterns in relation to carbohydrate and lipid metabolism in men with spinal cord injury. Appl Physiol Nutr Metab 36(1):107–114CrossRefPubMed
Zurück zum Zitat Gorgey AS, Lawrence J (2016) Acute responses of functional electrical stimulation cycling on the ventilation-to-CO2 production ratio and substrate utilization after spinal cord injury. PMR 8(3):225–234CrossRef Gorgey AS, Lawrence J (2016) Acute responses of functional electrical stimulation cycling on the ventilation-to-CO2 production ratio and substrate utilization after spinal cord injury. PMR 8(3):225–234CrossRef
Zurück zum Zitat Gorgey AS, Chiodo AE, Zemper ED, Hornyak JE, Rodriguez GM, Gater DR (2010) Relationship of spasticity to soft tissue body composition and the metabolic profile in persons with chronic motor complete spinal cord injury. J Spinal Cord Med 33:6–15CrossRefPubMedPubMedCentral Gorgey AS, Chiodo AE, Zemper ED, Hornyak JE, Rodriguez GM, Gater DR (2010) Relationship of spasticity to soft tissue body composition and the metabolic profile in persons with chronic motor complete spinal cord injury. J Spinal Cord Med 33:6–15CrossRefPubMedPubMedCentral
Zurück zum Zitat Gorgey AS, Poarch HJ, Dolbow DD, Castillo T, Gater DR (2014) Effect of adjusting pulse durations of functional electrical stimulation cycling on energy expenditure and fatigue after spinal cord injury. J Rehabil Res Dev 51:1455–1468. doi:10.1682/JRRD.2014.02.0054 CrossRefPubMed Gorgey AS, Poarch HJ, Dolbow DD, Castillo T, Gater DR (2014) Effect of adjusting pulse durations of functional electrical stimulation cycling on energy expenditure and fatigue after spinal cord injury. J Rehabil Res Dev 51:1455–1468. doi:10.​1682/​JRRD.​2014.​02.​0054 CrossRefPubMed
Zurück zum Zitat Gorgey AS, Khalil RE, Gill R, O’Brien LC, Lais T, Castillo T, Cifu DX, Savas J, Khan R, Cardozo C, Lesnefsky EJ, Gater DR, Adler RA (2017) Effects of testosterone and evoked resistance exercise after spinal cord injury (TEREX-SCI): study protocol for a randomized controlled trial. BMJ Open 7:e014125. doi:10.1136/bmjopen-2016-014125 CrossRefPubMedPubMedCentral Gorgey AS, Khalil RE, Gill R, O’Brien LC, Lais T, Castillo T, Cifu DX, Savas J, Khan R, Cardozo C, Lesnefsky EJ, Gater DR, Adler RA (2017) Effects of testosterone and evoked resistance exercise after spinal cord injury (TEREX-SCI): study protocol for a randomized controlled trial. BMJ Open 7:e014125. doi:10.​1136/​bmjopen-2016-014125 CrossRefPubMedPubMedCentral
Zurück zum Zitat Grimby G, Broberg C, Krotkiewska I, Krotkiewski M (1976) Muscle fiber composition in patients with traumatic cord lesion. Scand J Rehabil Med 8:37–42PubMed Grimby G, Broberg C, Krotkiewska I, Krotkiewski M (1976) Muscle fiber composition in patients with traumatic cord lesion. Scand J Rehabil Med 8:37–42PubMed
Zurück zum Zitat Hutchison SK, Teede HJ, Rachon D, Harrison CL, Strauss BJ, Stepto NK (2012) Effect of exercise training on insulin sensitivity, mitochondria and computed tomography muscle attenuation in overweight women with and without polycystic ovary syndrome. Diabetologia 55:1424–1434. doi:10.1007/s00125-011-2442-8 CrossRefPubMed Hutchison SK, Teede HJ, Rachon D, Harrison CL, Strauss BJ, Stepto NK (2012) Effect of exercise training on insulin sensitivity, mitochondria and computed tomography muscle attenuation in overweight women with and without polycystic ovary syndrome. Diabetologia 55:1424–1434. doi:10.​1007/​s00125-011-2442-8 CrossRefPubMed
Zurück zum Zitat Kelley DE, He J, Menshikova EV, Ritov VB (2002) Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51:2944–2950CrossRefPubMed Kelley DE, He J, Menshikova EV, Ritov VB (2002) Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51:2944–2950CrossRefPubMed
Zurück zum Zitat Kirkwood SP, Zurlo F, Larson K, Ravussin E (1991) Muscle mitochondrial morphology, body composition, and energy expenditure in sedentary individuals. Am J Physiol 260:E89–E94PubMed Kirkwood SP, Zurlo F, Larson K, Ravussin E (1991) Muscle mitochondrial morphology, body composition, and energy expenditure in sedentary individuals. Am J Physiol 260:E89–E94PubMed
Zurück zum Zitat Kjaer M, Mohr T, Biering-Sorensen F, Bangsbo J (2001) Muscle enzyme adaptation to training and tapering-off in spinal-cord-injured humans. Eur J Appl Physiol 84:482–486CrossRefPubMed Kjaer M, Mohr T, Biering-Sorensen F, Bangsbo J (2001) Muscle enzyme adaptation to training and tapering-off in spinal-cord-injured humans. Eur J Appl Physiol 84:482–486CrossRefPubMed
Zurück zum Zitat Magnusson G, Kaijser L, Rong H, Isberg B, Sylven C, Saltin B (1996) Exercise capacity in heart failure patients: relative importance of heart and skeletal muscle. Clin Physiol 16:183–195CrossRefPubMed Magnusson G, Kaijser L, Rong H, Isberg B, Sylven C, Saltin B (1996) Exercise capacity in heart failure patients: relative importance of heart and skeletal muscle. Clin Physiol 16:183–195CrossRefPubMed
Zurück zum Zitat Maki KC, Briones ER, Langbein WE, Inman-Felton A, Nemchausky B, Welch M, Burton J (1995) Associations between serum lipids and indicators of adiposity in men with spinal cord injury. Paraplegia 33:102–109. doi:10.1038/sc.1995.24 PubMed Maki KC, Briones ER, Langbein WE, Inman-Felton A, Nemchausky B, Welch M, Burton J (1995) Associations between serum lipids and indicators of adiposity in men with spinal cord injury. Paraplegia 33:102–109. doi:10.​1038/​sc.​1995.​24 PubMed
Zurück zum Zitat Mogensen M, Sahlin K, Fernstrom M, Glintborg D, Vind BF, Beck-Nielsen H, Hojlund K (2007) Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 56:1592–1599. doi:10.2337/db06-0981 CrossRefPubMed Mogensen M, Sahlin K, Fernstrom M, Glintborg D, Vind BF, Beck-Nielsen H, Hojlund K (2007) Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 56:1592–1599. doi:10.​2337/​db06-0981 CrossRefPubMed
Zurück zum Zitat Ravussin E, Bogardus C (1992) A brief overview of human energy metabolism and its relationship to essential obesity. Am J Clin Nutr 55:242S–245SPubMed Ravussin E, Bogardus C (1992) A brief overview of human energy metabolism and its relationship to essential obesity. Am J Clin Nutr 55:242S–245SPubMed
Zurück zum Zitat Reaven GM, Chen N, Hollenbeck C, Chen YD (1989) Effect of age on glucose tolerance and glucose uptake in healthy individuals. J Am Geriatr Soc 37:735–740CrossRefPubMed Reaven GM, Chen N, Hollenbeck C, Chen YD (1989) Effect of age on glucose tolerance and glucose uptake in healthy individuals. J Am Geriatr Soc 37:735–740CrossRefPubMed
Zurück zum Zitat Schrauwen-Hinderling VB et al (2007) Impaired in vivo mitochondrial function but similar intramyocellular lipid content in patients with type 2 diabetes mellitus and BMI-matched control subjects. Diabetologia 50:113–120. doi:10.1007/s00125-006-0475-1 CrossRefPubMed Schrauwen-Hinderling VB et al (2007) Impaired in vivo mitochondrial function but similar intramyocellular lipid content in patients with type 2 diabetes mellitus and BMI-matched control subjects. Diabetologia 50:113–120. doi:10.​1007/​s00125-006-0475-1 CrossRefPubMed
Zurück zum Zitat Spungen AM, Adkins RH, Stewart CA, Wang J, Pierson RN Jr, Waters RL, Bauman WA (2003) Factors influencing body composition in persons with spinal cord injury: a cross-sectional study. J Appl Physiol (1985) 95:2398–2407. doi:10.1152/japplphysiol.00729.2002 CrossRef Spungen AM, Adkins RH, Stewart CA, Wang J, Pierson RN Jr, Waters RL, Bauman WA (2003) Factors influencing body composition in persons with spinal cord injury: a cross-sectional study. J Appl Physiol (1985) 95:2398–2407. doi:10.​1152/​japplphysiol.​00729.​2002 CrossRef
Zurück zum Zitat St-Jean-Pelletier F et al (2016) The impact of ageing, physical activity, and pre-frailty on skeletal muscle phenotype, mitochondrial content, and intramyocellular lipids in men. J Cachexia Sarcopenia Muscle. doi:10.1002/jcsm.12139 PubMedPubMedCentral St-Jean-Pelletier F et al (2016) The impact of ageing, physical activity, and pre-frailty on skeletal muscle phenotype, mitochondrial content, and intramyocellular lipids in men. J Cachexia Sarcopenia Muscle. doi:10.​1002/​jcsm.​12139 PubMedPubMedCentral
Metadaten
Titel
Skeletal muscle mitochondrial mass is linked to lipid and metabolic profile in individuals with spinal cord injury
verfasst von
Laura C. O’Brien
Qun Chen
Jeannie Savas
Edward J. Lesnefsky
Ashraf S. Gorgey
Publikationsdatum
01.09.2017
Verlag
Springer Berlin Heidelberg
Erschienen in
European Journal of Applied Physiology / Ausgabe 11/2017
Print ISSN: 1439-6319
Elektronische ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-017-3687-9

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