Muscle Oxidative Capacity in the Arms and Legs of Various Types of Endurance Trained Athletes Muscle Oxidative Capacity in Endurance Trained Athletes
Main Article Content
Abstract
Our study used near-infrared spectroscopy (NIRS) to measure muscle oxidative capacity (mVmax) in the medial gastrocnemius, vastus lateralis, biceps brachii, and wrist flexor muscles in Cross-country (LEG-T) and Swimmer/Rowers (WHOLE-T) and controls. Young male adults: cross-country LEG-Tners (n=6) and swimmers/rowers (n=5), moderately fit (CONTROL, n=7) were tested. mVmax was measured as the rate of post-exercise recovery of oxygen consumption after a short bout of exercise using NIRS. Whole-body peak oxygen uptake (VO2peak) was determined during a continuous treadmill protocol. The lower limb muscles had 42% higher mVmax than upper limb muscles in all subjects, with significant differences in 10 of 12 pairwise comparisons (p< 0.05). The LEG-T group had higher mVmax values in both legs than CONTROL group (p< 0.05), while the WHOLE-T group had higher mVmax in the vastus lateralis (p = 0.048). There were no differences in the arm muscles of between the groups. The combined mVmax of both leg muscles in all groups correlated with VO2peak (r2=0.597). Muscle oxidative capacity was consistent with training status, and leg mitochondrial capacity correlated with maximal whole body oxidative capacity. These results support the use of NIRS measurements to characterize oxidative capacity in skeletal muscles of athletic populations.
Keywords:
Mitochondrial Capacity, Endurance Training, Maximal Oxygen Uptake, Competitive Athletes
Article Details
How to Cite
MEYER, Patrick Hunter; MISSAO, Eduardo Toshiyuki; MCCULLY, Kevin.
Muscle Oxidative Capacity in the Arms and Legs of Various Types of Endurance Trained Athletes.
Medical Research Archives, [S.l.], v. 9, n. 7, july 2021.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/2505>. Date accessed: 22 nov. 2024.
doi: https://doi.org/10.18103/mra.v9i7.2505.
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
1. Holloszy JO, Booth FW. Biochemical adaptations to endurance exercise in muscle. Annu Rev Physiol. 1976;38:273-91. doi:10.1146/annurev.ph.38.030176.001421
2. Holloszy JO, Coyle EF. Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. Journal of applied physiology: respiratory, environmental and exercise physiology. Apr 1984;56(4):831-8.
3. Bickel CS, Slade JM, Haddad F, Adams GR, Dudley GA. Acute molecular responses of skeletal muscle to resistance exercise in able-bodied and spinal cord-injured subjects. J Appl Physiol. Jun 2003;94(6):2255-62. doi:10.1152/japplphysiol.00014.2003
00014.2003 [pii]
4. Castro MJ, Apple DF, Jr., Hillegass EA, Dudley GA. Influence of complete spinal cord injury on skeletal muscle cross-sectional area within the first 6 months of injury. Eur J Appl Physiol Occup Physiol. Sep 1999;80(4):373-8.
5. Ragnarsson KT. Physiologic effects of functional electrical stimulation-induced exercises in spinal cord-injured individuals. Clinical orthopaedics and related research. Aug 1988;(233):53-63.
6. Bergstrom J. Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Review. Scand J Clin Lab Invest. Nov 1975;35(7):609-16.
7. McCully KK, Kent JA, Chance B. Application of 31-P magnetic resonance spectrocopy to the study of athletic performance. Sports Med. 1988;5:312-321.
8. Blomstrand E, Ekblom B, Newsholme EA. Maximum activities of key glycolytic and oxidative enzymes in human muscle from differently trained individuals. J Physiol. Dec 1986;381:111-8.
9. Gollnick PD, Armstrong RB, Saubert CWt, Piehl K, Saltin B. Enzyme activity and fiber composition in skeletal muscle of untrained and trained men. J Appl Physiol. Sep 1972;33(3):312-9.
10. McCully K, Boden B, Tuchler M, Fountain M, Chance B. Wrist flexor muscles of elite rowers measured with magnetic resonance spectroscopy. Journal of Applied Physiology. 1989;67(3):926-932.
11. McCully KK, Vandenborne K, DeMeirleir K, Posner JD, Leigh Jr JS. Muscle metabolism in track athletes, using 31P magnetic resonance spectroscopy. Canadian Journal of Physiology and Pharmacology. 1992;70(10):1353.
12. Sako T, Hamaoka T, Higuchi H, Kurosawa Y, Katsumura T. Validity of NIR spectroscopy for quantitatively measuring muscle oxidative metabolic rate in exercise. Journal of Applied Physiology. January 1, 2001 2001;90(1):338-344.
13. Nagasawa T, Hamaoka T, Sako T, et al. A practical indicator of muscle oxidative capacity determined by recovery of muscle O 2 consumption using NIR spectroscopy. European Journal of Sport Science. 2003/04/01 2003;3(2):1-10. doi:10.1080/17461390300073207
14. 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 (1985). Jul 2012;113(2):175-83. doi:10.1152/japplphysiol.00319.2012
15. Ryan TE, Brophy P, Lin CT, Hickner RC, Neufer PD. Assessment of in vivo skeletal muscle mitochondrial respiratory capacity in humans by near-infrared spectroscopy: a comparison with in situ measurements. J Physiol. Aug 1 2014;592(Pt 15):3231-41. doi:10.1113/jphysiol.2014.274456
16. 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). Dec 2013;115(12):1757-66. doi:10.1152/japplphysiol.00835.2013
17. Ryan TE, Southern WM, Brizendine JT, McCully KK. Activity-induced changes in skeletal muscle metabolism measured with optical spectroscopy. Med Sci Sports Exerc. Dec 2013;45(12):2346-52. doi:10.1249/MSS.0b013e31829a726a
18. Southern WM, Ryan TE, Kepple K, Murrow JR, Nilsson KR, McCully KK. Reduced skeletal muscle oxidative capacity and impaired training adaptations in heart failure. Physiol Rep. Apr 2015;3(4)doi:10.14814/phy2.12353
19. Brizendine JT, Ryan TE, Larson RD, McCully KK. Skeletal muscle metabolism in endurance athletes with near-infrared spectroscopy. Med Sci Sports Exerc. May 2013;45(5):869-75. doi:10.1249/MSS.0b013e31827e0eb6
20. Forbes SC, Slade JM, Francis RM, Meyer RA. Comparison of oxidative capacity among leg muscles in humans using gated 31P 2-D chemical shift imaging. NMR Biomed. Dec 2009;22(10):1063-71. doi:10.1002/nbm.1413
21. Richardson RS, Noyszewski EA, Haseler LJ, Bluml S, Frank LR. Evolving techniques for the investigation of muscle bioenergetics and oxygenation. Biochem Soc Trans. Apr 2002;30(2):232-7.
22. Parasoglou P, Xia D, Chang G, Regatte RR. Dynamic three-dimensional imaging of phosphocreatine recovery kinetics in the human lower leg muscles at 3T and 7T: a preliminary study. NMR Biomed. Mar 2013;26(3):348-56. doi:10.1002/nbm.2866
23. Ortenblad N, Nielsen J, Boushel R, Soderlund K, Saltin B, Holmberg HC. The Muscle Fiber Profiles, Mitochondrial Content, and Enzyme Activities of the Exceptionally Well-Trained Arm and Leg Muscles of Elite Cross-Country Skiers. Front Physiol. 2018;9:1031. doi:10.3389/fphys.2018.01031
24. Stewart AD, Hannan J. Total and regional bone density in male runners, cyclists, and controls. Med Sci Sports Exerc. Aug 2000;32(8):1373-7. doi:10.1097/00005768-200008000-00003
25. 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. Sep 2013;113(9):2275-83. doi:10.1007/s00421-013-2657-0
26. Bigelman KA, Fan EH, Chapman DP, Freese EC, Trilk JL, Cureton KJ. Effects of six weeks of quercetin supplementation on physical performance in ROTC cadets. Mil Med. Oct 2010;175(10):791-8.
27. Borg G, Dahlstrom H. A pilot study of perceived exertion and physical working capacity. Acta Societatis Medicorum Upsaliensis. 1962;67:21-7.
28. Hanna R, Gosalia J, Demalis A, et al. Bilateral NIRS measurements of muscle mitochondrial capacity: Feasibility and repeatability. Physiol Rep. Apr 2021;9(8):e14826. doi:10.14814/phy2.14826
29. Lagerwaard B, Janssen JJE, Cuijpers I, Keijer J, de Boer VCJ, Nieuwenhuizen AG. Muscle mitochondrial capacity in high- and low-fitness females using near-infrared spectroscopy. Physiol Rep. May 2021;9(9):e14838. doi:10.14814/phy2.14838
30. 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. May 2014;39(5):521-9. doi:10.1139/apnm-2013-0347
31. Green HJ, Daub B, Houston ME, Thomson JA, Fraser I, Ranney D. Human vastus lateralis and gastrocnemius muscles. A comparative histochemical and biochemical analysis. J Neurol Sci. Nov-Dec 1981;52(2-3):201-10.
32. Larsen RG, Callahan DM, Foulis SA, Kent-Braun JA. In vivo oxidative capacity varies with muscle and training status in young adults. J Appl Physiol (1985). Sep 2009;107(3):873-9. doi:10.1152/japplphysiol.00260.2009
33. Gregory CM, Vandenborne K, Dudley GA. Metabolic enzymes and phenotypic expression among human locomotor muscles. Muscle Nerve. Mar 2001;24(3):387-93.
34. Bori Z, Zhao Z, Koltai E, et al. The effects of aging, physical training, and a single bout of exercise on mitochondrial protein expression in human skeletal muscle. Experimental gerontology. Jun 2012;47(6):417-24. doi:10.1016/j.exger.2012.03.004
35. Coen PM, Jubrias SA, Distefano G, et al. Skeletal muscle mitochondrial energetics are associated with maximal aerobic capacity and walking speed in older adults. J Gerontol A Biol Sci Med Sci. Apr 2013;68(4):447-55. doi:10.1093/gerona/gls196
36. Tonkonogi M, Sahlin K. Rate of oxidative phosphorylation in isolated mitochondria from human skeletal muscle: effect of training status. Acta Physiol Scand. Nov 1997;161(3):345-53. doi:10.1046/j.1365-201X.1997.00222.x
37. Costill DL, Fink WJ, Pollock ML. Muscle fiber composition and enzyme activities of elite distance runners. Med Sci Sports. Summer 1976;8(2):96-100.
38. Willingham TB, Backus D, McCully KK. Muscle Dysfunction and Walking Impairment in Women with Multiple Sclerosis. Int J MS Care. Nov-Dec 2019;21(6):249-256. doi:10.7224/1537-2073.2018-020
39. Picard M, Jung B, Liang F, et al. Mitochondrial dysfunction and lipid accumulation in the human diaphragm during mechanical ventilation. Am J Respir Crit Care Med. Dec 1 2012;186(11):1140-9. doi:10.1164/rccm.201206-0982OC
40. Schmalbruch H, Kamieniecka Z. Fiber types in the human brachial biceps muscle. Exp Neurol. Aug 1974;44(2):313-28. doi:10.1016/0014-4886(74)90069-7
41. van Beekvelt M, Borghuis M, van Engelen B, Wevers R, Colier W. Adipose tissue thickness affects in vivo quantitative near-IR spectroscopy in human skeletal muscle. Clin Sci (Lond). 2001;101:21-28.
42. Sumner MD, Beard S, Pryor EK, Das I, McCully KK. Near Infrared Spectroscopy Measurements of Mitochondrial Capacity Using Partial Recovery Curves. Frontiers in physiology. 2020;11:111.
2. Holloszy JO, Coyle EF. Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. Journal of applied physiology: respiratory, environmental and exercise physiology. Apr 1984;56(4):831-8.
3. Bickel CS, Slade JM, Haddad F, Adams GR, Dudley GA. Acute molecular responses of skeletal muscle to resistance exercise in able-bodied and spinal cord-injured subjects. J Appl Physiol. Jun 2003;94(6):2255-62. doi:10.1152/japplphysiol.00014.2003
00014.2003 [pii]
4. Castro MJ, Apple DF, Jr., Hillegass EA, Dudley GA. Influence of complete spinal cord injury on skeletal muscle cross-sectional area within the first 6 months of injury. Eur J Appl Physiol Occup Physiol. Sep 1999;80(4):373-8.
5. Ragnarsson KT. Physiologic effects of functional electrical stimulation-induced exercises in spinal cord-injured individuals. Clinical orthopaedics and related research. Aug 1988;(233):53-63.
6. Bergstrom J. Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Review. Scand J Clin Lab Invest. Nov 1975;35(7):609-16.
7. McCully KK, Kent JA, Chance B. Application of 31-P magnetic resonance spectrocopy to the study of athletic performance. Sports Med. 1988;5:312-321.
8. Blomstrand E, Ekblom B, Newsholme EA. Maximum activities of key glycolytic and oxidative enzymes in human muscle from differently trained individuals. J Physiol. Dec 1986;381:111-8.
9. Gollnick PD, Armstrong RB, Saubert CWt, Piehl K, Saltin B. Enzyme activity and fiber composition in skeletal muscle of untrained and trained men. J Appl Physiol. Sep 1972;33(3):312-9.
10. McCully K, Boden B, Tuchler M, Fountain M, Chance B. Wrist flexor muscles of elite rowers measured with magnetic resonance spectroscopy. Journal of Applied Physiology. 1989;67(3):926-932.
11. McCully KK, Vandenborne K, DeMeirleir K, Posner JD, Leigh Jr JS. Muscle metabolism in track athletes, using 31P magnetic resonance spectroscopy. Canadian Journal of Physiology and Pharmacology. 1992;70(10):1353.
12. Sako T, Hamaoka T, Higuchi H, Kurosawa Y, Katsumura T. Validity of NIR spectroscopy for quantitatively measuring muscle oxidative metabolic rate in exercise. Journal of Applied Physiology. January 1, 2001 2001;90(1):338-344.
13. Nagasawa T, Hamaoka T, Sako T, et al. A practical indicator of muscle oxidative capacity determined by recovery of muscle O 2 consumption using NIR spectroscopy. European Journal of Sport Science. 2003/04/01 2003;3(2):1-10. doi:10.1080/17461390300073207
14. 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 (1985). Jul 2012;113(2):175-83. doi:10.1152/japplphysiol.00319.2012
15. Ryan TE, Brophy P, Lin CT, Hickner RC, Neufer PD. Assessment of in vivo skeletal muscle mitochondrial respiratory capacity in humans by near-infrared spectroscopy: a comparison with in situ measurements. J Physiol. Aug 1 2014;592(Pt 15):3231-41. doi:10.1113/jphysiol.2014.274456
16. 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). Dec 2013;115(12):1757-66. doi:10.1152/japplphysiol.00835.2013
17. Ryan TE, Southern WM, Brizendine JT, McCully KK. Activity-induced changes in skeletal muscle metabolism measured with optical spectroscopy. Med Sci Sports Exerc. Dec 2013;45(12):2346-52. doi:10.1249/MSS.0b013e31829a726a
18. Southern WM, Ryan TE, Kepple K, Murrow JR, Nilsson KR, McCully KK. Reduced skeletal muscle oxidative capacity and impaired training adaptations in heart failure. Physiol Rep. Apr 2015;3(4)doi:10.14814/phy2.12353
19. Brizendine JT, Ryan TE, Larson RD, McCully KK. Skeletal muscle metabolism in endurance athletes with near-infrared spectroscopy. Med Sci Sports Exerc. May 2013;45(5):869-75. doi:10.1249/MSS.0b013e31827e0eb6
20. Forbes SC, Slade JM, Francis RM, Meyer RA. Comparison of oxidative capacity among leg muscles in humans using gated 31P 2-D chemical shift imaging. NMR Biomed. Dec 2009;22(10):1063-71. doi:10.1002/nbm.1413
21. Richardson RS, Noyszewski EA, Haseler LJ, Bluml S, Frank LR. Evolving techniques for the investigation of muscle bioenergetics and oxygenation. Biochem Soc Trans. Apr 2002;30(2):232-7.
22. Parasoglou P, Xia D, Chang G, Regatte RR. Dynamic three-dimensional imaging of phosphocreatine recovery kinetics in the human lower leg muscles at 3T and 7T: a preliminary study. NMR Biomed. Mar 2013;26(3):348-56. doi:10.1002/nbm.2866
23. Ortenblad N, Nielsen J, Boushel R, Soderlund K, Saltin B, Holmberg HC. The Muscle Fiber Profiles, Mitochondrial Content, and Enzyme Activities of the Exceptionally Well-Trained Arm and Leg Muscles of Elite Cross-Country Skiers. Front Physiol. 2018;9:1031. doi:10.3389/fphys.2018.01031
24. Stewart AD, Hannan J. Total and regional bone density in male runners, cyclists, and controls. Med Sci Sports Exerc. Aug 2000;32(8):1373-7. doi:10.1097/00005768-200008000-00003
25. 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. Sep 2013;113(9):2275-83. doi:10.1007/s00421-013-2657-0
26. Bigelman KA, Fan EH, Chapman DP, Freese EC, Trilk JL, Cureton KJ. Effects of six weeks of quercetin supplementation on physical performance in ROTC cadets. Mil Med. Oct 2010;175(10):791-8.
27. Borg G, Dahlstrom H. A pilot study of perceived exertion and physical working capacity. Acta Societatis Medicorum Upsaliensis. 1962;67:21-7.
28. Hanna R, Gosalia J, Demalis A, et al. Bilateral NIRS measurements of muscle mitochondrial capacity: Feasibility and repeatability. Physiol Rep. Apr 2021;9(8):e14826. doi:10.14814/phy2.14826
29. Lagerwaard B, Janssen JJE, Cuijpers I, Keijer J, de Boer VCJ, Nieuwenhuizen AG. Muscle mitochondrial capacity in high- and low-fitness females using near-infrared spectroscopy. Physiol Rep. May 2021;9(9):e14838. doi:10.14814/phy2.14838
30. 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. May 2014;39(5):521-9. doi:10.1139/apnm-2013-0347
31. Green HJ, Daub B, Houston ME, Thomson JA, Fraser I, Ranney D. Human vastus lateralis and gastrocnemius muscles. A comparative histochemical and biochemical analysis. J Neurol Sci. Nov-Dec 1981;52(2-3):201-10.
32. Larsen RG, Callahan DM, Foulis SA, Kent-Braun JA. In vivo oxidative capacity varies with muscle and training status in young adults. J Appl Physiol (1985). Sep 2009;107(3):873-9. doi:10.1152/japplphysiol.00260.2009
33. Gregory CM, Vandenborne K, Dudley GA. Metabolic enzymes and phenotypic expression among human locomotor muscles. Muscle Nerve. Mar 2001;24(3):387-93.
34. Bori Z, Zhao Z, Koltai E, et al. The effects of aging, physical training, and a single bout of exercise on mitochondrial protein expression in human skeletal muscle. Experimental gerontology. Jun 2012;47(6):417-24. doi:10.1016/j.exger.2012.03.004
35. Coen PM, Jubrias SA, Distefano G, et al. Skeletal muscle mitochondrial energetics are associated with maximal aerobic capacity and walking speed in older adults. J Gerontol A Biol Sci Med Sci. Apr 2013;68(4):447-55. doi:10.1093/gerona/gls196
36. Tonkonogi M, Sahlin K. Rate of oxidative phosphorylation in isolated mitochondria from human skeletal muscle: effect of training status. Acta Physiol Scand. Nov 1997;161(3):345-53. doi:10.1046/j.1365-201X.1997.00222.x
37. Costill DL, Fink WJ, Pollock ML. Muscle fiber composition and enzyme activities of elite distance runners. Med Sci Sports. Summer 1976;8(2):96-100.
38. Willingham TB, Backus D, McCully KK. Muscle Dysfunction and Walking Impairment in Women with Multiple Sclerosis. Int J MS Care. Nov-Dec 2019;21(6):249-256. doi:10.7224/1537-2073.2018-020
39. Picard M, Jung B, Liang F, et al. Mitochondrial dysfunction and lipid accumulation in the human diaphragm during mechanical ventilation. Am J Respir Crit Care Med. Dec 1 2012;186(11):1140-9. doi:10.1164/rccm.201206-0982OC
40. Schmalbruch H, Kamieniecka Z. Fiber types in the human brachial biceps muscle. Exp Neurol. Aug 1974;44(2):313-28. doi:10.1016/0014-4886(74)90069-7
41. van Beekvelt M, Borghuis M, van Engelen B, Wevers R, Colier W. Adipose tissue thickness affects in vivo quantitative near-IR spectroscopy in human skeletal muscle. Clin Sci (Lond). 2001;101:21-28.
42. Sumner MD, Beard S, Pryor EK, Das I, McCully KK. Near Infrared Spectroscopy Measurements of Mitochondrial Capacity Using Partial Recovery Curves. Frontiers in physiology. 2020;11:111.