Assessment of in vivo skeletal muscle mitochondrial respiratory capacity in humans by near-infrared spectroscopy: A comparison with in situ measurements

Journal of Physiology

Volumn 592, Issue 15, 2014, Pages 3231-3241

  Ryan, Terence E ^a,b   Brophy, Patricia ^a,b   Lin, Chien Te ^a,b   Hickner, Robert C ^a,b,c   Neufer, P Darrell ^a,b  

^a EAST CAROLINA UNIVERSITY   (United States)

^b EAST CAROLINA UNIVERSITY   (United States)

^c UNIVERSITY OF KWAZULU NATAL   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); OXYGEN;

ADULT; ARTICLE; FEMALE; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; IN VIVO STUDY; MALE; MITOCHONDRIAL RESPIRATION; MUSCLE BIOPSY; MUSCLE ISOMETRIC CONTRACTION; NEAR INFRARED SPECTROSCOPY; NORMAL HUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RESPIROMETRY; SKELETAL MUSCLE; VASTUS LATERALIS MUSCLE; ADOLESCENT; CELL RESPIRATION; COMPARATIVE STUDY; METABOLISM; MUSCLE MITOCHONDRION; PROCEDURES;

ADOLESCENT; ADULT; CELL RESPIRATION; FEMALE; HUMANS; MALE; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; OXYGEN; OXYGEN CONSUMPTION; SPECTROSCOPY, NEAR-INFRARED;

EID: 84905217954     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.274456     Document Type: Article

References (62)

1. Belardinelli R, Barstow TJ, Nguyen P & Wasserman K (1997). Skeletal muscle oxygenation and oxygen uptake kinetics following constant work rate exercise in chronic congestive heart failure. Am J Cardiol 80, 1319-1324.
2. 31P-NMR at the onset of constant-load exercise in humans. J Appl Physiol (1985) 73, 1644-1649.
3. Boone J, Koppo K, Barstow TJ & Bouckaert J (2009). Pattern of deoxy[Hb+Mb] during ramp cycle exercise: influence of aerobic fitness status. Eur J Appl Physiol 105, 851-859.
4. Boushel R, Langberg H, Green S, Skovgaard D, Bulow J & Kjaer M (2000). Blood flow and oxygenation in peritendinous tissue and calf muscle during dynamic exercise in humans. J Physiol 524, 305-313.
5. Brand MD & Nicholls DG (2011). Assessing mitochondrial dysfunction in cells. Biochem J 435, 297-312.
6. Breuer ME, Koopman WJ, Koene S, Nooteboom M, Rodenburg RJ, Willems PH & Smeitink JA (2013). The role of mitochondrial OXPHOS dysfunction in the development of neurologic diseases. Neurobiol Dis 51, 27-34.
7. Brizendine JT, Ryan TE, Larson RD & McCully KK (2013). Skeletal muscle metabolism in endurance athletes with near-infrared spectroscopy. Med Sci Sports Exerc 45, 869-875.
8. Chance B, Im J, Nioka S & Kushmerick M (2006). Skeletal muscle energetics with PNMR: personal views and historic perspectives. NMR Biomed 19, 904-926.
9. Chance B, Leigh JS, Clark BJ, Maris J, Kent J, Nioka S & Smith D (1985). Control of oxidative-metabolism and oxygen delivery in human skeletal-muscle - a steady-state analysis of the work energy-cost transfer-function. Proc Natl Acad Sci U S A 82, 8384-8388.
10. Chance B & Williams GR (1955). Respiratory enzymes in oxidative phosphorylation. III. The steady state. J Biol Chem 217, 409-427.
11. Coen PM, Jubrias SA, Distefano G, Amati F, Mackey DC, Glynn NW, Manini TM, Wohlgemuth SE, Leeuwenburgh C, Cummings SR, Newman AB, Ferrucci L, Toledo FG, Shankland E, Conley KE & Goodpaster BH (2013). Skeletal muscle mitochondrial energetics are associated with maximal aerobic capacity and walking speed in older adults. J Gerontol A Biol Sci Med Sci 68, 447-455.
12. Conley KE, Jubrias SA & Esselman PC (2000a). Mitochondrial oxidative capacity in vivo declines with age in human muscle. Faseb J 14, A49.
13. Conley KE, Jubrias SA & Esselman PC (2000b). Oxidative capacity and ageing in human muscle. J Physiol 526, 203-210.
14. Crow MT & Kushmerick MJ (1982). Chemical energetics of slow- and fast-twitch muscles of the mouse. J Gen Physiol 79, 147-166.
15. Deblasi RA, Ferrari M, Natali A, Conti G, Mega A & Gasparetto A (1994). Noninvasive measurement of forearm blood-flow and oxygen-consumption by near-infrared spectroscopy. J Appl Physiol 76, 1388-1393.
16. Erickson ML, Ryan TE, Young HJ & McCully KK (2013). Near-infrared assessments of skeletal muscle oxidative capacity in persons with spinal cord injury. Eur J Appl Physiol 113, 2275-2283.
17. Ferrari M, Mathalib M & Quaresima V (2011). The use of near-infrared spectroscopy in understanding skeletal muscle physiology: recent developments. Philos Trans A Math Phys Eng Sci 369, 4577-4590.
18. Figueiredo PA, Ferreira RM, Appell HJ & Duarte JA (2008). Age-induced morphological, biochemical, and functional alterations in isolated mitochondria from murine skeletal muscle. J Gerontol A Biol Sci Med Sci 63, 350-359.
19. Forbes SC, Paganini AT, Slade JM, Towse TF & Meyer RA (2009). Phosphocreatine recovery kinetics following low- and high-intensity exercise in human triceps surae and rat posterior hindlimb muscles. Am J Physiol Regul Integr Comp Physiol 296, R161-R170.
20. Gnaiger E (2009). Capacity of oxidative phosphorylation in human skeletal muscle: new perspectives of mitochondrial physiology. Int J Biochem Cell Biol 41, 1837-1845.
21. Gollnick PD, Armstrong RB, Saltin B, Saubert CWt, Sembrowich WL & Shepherd RE (1973). Effect of training on enzyme activity and fibre composition of human skeletal muscle. J Appl Physiol 34, 107-111.
22. Gollnick PD, Armstrong RB, Saubert CW, Piehl K & Saltin B (1972). Enzyme activity and fibre composition in skeletal muscle of untrained and trained men. J Appl Physiol 33, 312-319.
23. Grassi B, Pogliaghi S, Rampichini S, Quaresima V, Ferrari M, Marconi C & Cerretelli P (2003). Muscle oxygenation and pulmonary gas exchange kinetics during cycling exercise on-transitions in humans. J Appl Physiol 95, 149-158.
24. Hamaoka T, Iwane H, Shimomitsu T, Katsumura T, Murase N, Nishio S, Osada T, Kurosawa Y & Chance B (1996). Noninvasive measures of oxidative metabolism on working human muscles by near-infrared spectroscopy. J Appl Physiol 81, 1410-1417.
25. Hampson NB & Piantadosi CA (1988). Near infrared monitoring of human skeletal muscle oxygenation during forearm ischemia. J Appl Physiol 64, 2449-2457.
26. Hill DK (1940). The time course of the oxygen consumption of stimulated frog's muscle. J Physiol 98, 207-227.
27. Holloszy JO (1967). Biochemical adaptations in muscle. Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle. J Biol Chem 242, 2278-2282.
28. Jackman MR & Willis WT (1996). Characteristics of mitochondria isolated from type I and type IIb skeletal muscle. Am J Physiol 270, C673-678.
29. Jobsis FF (1977). Noninvasive, infrared monitoring of cerebral and myocardial oxygen sufficiency and circulatory parameters. Science 198, 1264-1267.
30. Johri A & Beal MF (2012). Mitochondrial dysfunction in neurodegenerative diseases. J Pharmacol Exp Ther 342, 619-630.
31. Kemp GJ, Ahmad RE, Nicolay K & Prompers JJ (2014). Quantification of skeletal muscle mitochondrial function by P magnetic resonance spectroscopy techniques: a quantitative review. Acta Physiol (Oxf) doi: 10.1111/alpha.12307.
32. 31P-MR spectroscopy: a cross-validation with in vitro measurements. J Magn Reson Imaging 34, 1143-1150.
33. Lanza IR & Nair KS (2009). Functional assessment of isolated mitochondria in vitro. Methods Enzymol 457, 349-372.
34. Larsen RG, Callahan DM, Foulis SA & Kent-Braun JA (2012a). Age-related changes in oxidative capacity differ between locomotory muscles and are associated with physical activity behaviour. Appl Physiol Nutr Metab 37, 88-99.
35. Larsen S, Hey-Mogensen M, Rabol R, Stride N, Helge JW & Dela F (2012b). The influence of age and aerobic fitness: effects on mitochondrial respiration in skeletal muscle. Acta Physiol (Oxf) 205, 423-432.
36. Larson-Meyer DE, Newcomer BR, Hunter GR, Joanisse DR, Weinsier RL & Bamman MM (2001). Relation between in vivo and in vitro measurements of skeletal muscle oxidative metabolism. Muscle Nerve 24, 1665-1676.
37. 31P MRS quantitative methods in sedentary and trained subjects. NMR Biomed 24, 425-438.
38. 2 availability in elderly people. Age (Dordr) 35, 1183-1192.
39. O2 and phosphorylcreatine level. Implications for the control of respiration. J Gen Physiol 86, 135-165.
40. Malagoni AM, Felisatti M, Mandini S, Mascoli F, Manfredini R, Basaglia N, Zamboni P & Manfredini F (2010). Resting muscle oxygen consumption by near-infrared spectroscopy in peripheral arterial disease: a parameter to be considered in a clinical setting? Angiology 61, 530-536.
41. McCully KK, Boden BP, Tuchler M, Fountain MR & Chance B (1989). Wrist flexor muscles of elite rowers measured with magnetic resonance spectroscopy. J Appl Physiol 67, 926-932.
42. McCully KK, Fielding RA, Evans WJ, Leigh JS, Jr & Posner JD (1993). Relationships between in vivo and in vitro measurements of metabolism in young and old human calf muscles. J Appl Physiol 75, 813-819.
43. Meyer RA (1988). A linear-model of muscle respiration explains monoexponential phosphocreatine changes. Am J Physiol 254, C548-553.
44. Motobe M, Murase N, Osada T, Homma T, Ueda C, Nagasawa T, Kitahara A, Ichimura S, Kurosawa Y, Katsumura T, Hoshika A & Hamaoka T (2004). Noninvasive monitoring of deterioration in skeletal muscle function with forearm cast immobilization and the prevention of deterioration. Dyn Med 3, 2.
45. 2 consumption using NIR spectroscopy. Eur J Sport Sci 3, 1-10.
46. Paganini AT, Foley JM & Meyer RA (1997). Linear dependence of muscle phosphocreatine kinetics on oxidative capacity. Am J Physiol 272, C501-C510.
47. Perry CG, Kane DA, Lanza IR & Neufer PD (2013). Methods for assessing mitochondrial function in diabetes. Diabetes 62, 1041-1053.
48. Perry CG, Kane DA, Lin CT, Kozy R, Cathey BL, Lark DS, Kane CL, Brophy PM, Gavin TP, Anderson EJ & Neufer PD (2011). Inhibiting myosin-ATPase reveals a dynamic range of mitochondrial respiratory control in skeletal muscle. Biochem J 437, 215-222.
49. 31P magnetic resonance spectroscopy. Int J Biochem Cell Biol 50, 67-72.
50. Quistorff B, Johansen L & Sahlin K (1993). Absence of phosphocreatine resynthesis in human calf muscle during ischaemic recovery. Biochem J 291, 681-686.
51. Ryan TE, Brizendine JT & McCully KK (2013a). A comparison of exercise type and intensity on the noninvasive assessment of skeletal muscle mitochondrial function using near-infrared spectroscopy. J Appl Physiol 114, 230-237.
52. Ryan TE, Erickson ML, Brizendine JT, Young HJ & McCully KK (2012). Noninvasive evaluation of skeletal muscle mitochondrial capacity with near-infrared spectroscopy: correcting for blood volume changes. J Appl Physiol 113, 175-183.
53. Ryan TE, Southern WM, Brizendine JT & McCully KK (2013b). Activity-induced changes in skeletal muscle metabolism measured with optical spectroscopy. Med Sci Sports Exerc 45, 2346-2352.
54. Ryan TE, Southern WM, Reynolds MA & McCully KK (2013c). A cross-validation of near-infrared spectroscopy measurements of skeletal muscle oxidative capacity with phosphorus magnetic resonance spectroscopy. J Appl Physiol 115, 1757-1766.
55. Salvadego D, Domenis R, Lazzer S, Porcelli S, Rittweger J, Rizzo G, Mavelli I, Simunic B, Pisot R & Grassi B (2013). Skeletal muscle oxidative function in vivo and ex vivo in athletes with marked hypertrophy from resistance training. J Appl Physiol 114, 1527-1535.
56. 2 emission capacities without major shifts in myosin heavy chain isoform. J Appl Physiol 113, 1624-1634.
57. Seiyama A, Hazeki O & Tamura M (1988). Noninvasive quantitative analysis of blood oxygenation in rat skeletal muscle. J Biochem 103, 419-424.
58. 2 consumption and blood flow in skeletal muscle. J Appl Physiol 90, 511-519.
59. Van Beekvelt MCP, Borghuis MS, Engelen BGM, Wevers RA & Colier WN (2001b). Adipose tissue thickness affects in vivo quantitative near-IR spectroscopy in human skeletal muscle. Clin Sci 101, 21-28.
60. Vorgerd M, Schols L, Hardt C, Ristow M, Epplen JT & Zange J (2000). Mitochondrial impairment of human muscle in Friedreich ataxia in vivo. Neuromuscul Disord 10, 430-435.
61. Wallace DC (2013). A mitochondrial bioenergetic etiology of disease. J Clin Invest 123, 1405-1412.
62. Walter G, Vandenborne K, McCully KK & Leigh JS (1997). Noninvasive measurement of phosphocreatine recovery kinetics in single human muscles. Am J Physiol 41, C525-C534.