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Erschienen in: European Journal of Applied Physiology 9/2013

01.09.2013 | Original Article

Near-infrared assessments of skeletal muscle oxidative capacity in persons with spinal cord injury

verfasst von: Melissa Lynn Erickson, Terence E. Ryan, Hui-Ju Young, Kevin K. McCully

Erschienen in: European Journal of Applied Physiology | Ausgabe 9/2013

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Abstract

After spinal cord injury (SCI) skeletal muscle decreases in size, increases in intramuscular fat, and has potential declines in mitochondrial function. Reduced mitochondrial function has been linked to the development of metabolic disease. The aim of this study was to measure mitochondrial function in persons with SCI using near-infrared spectroscopy (NIRS). Oxygen consumption of the vastus lateralis muscle was measured with NIRS during repeated short-duration arterial occlusions in nine able-bodied (AB) and nine persons with motor complete SCI. Skeletal muscle oxidative capacity (V max) was evaluated with two approaches: (1) rate constant of the recovery of oxygen consumption after exercise and (2) extrapolated maximum oxygen consumption from a progressive work test. V max as indicated by the rate constant (k) from the recovery kinetics test was lower in SCI compared with AB participants (k: SCI 0.7 ± 0.3 vs. AB 1.9 ± 0.4 min−1; p < 0.001). Time constants were SCI 91.9 ± 37.8 vs. AB 33.6 ± 8.3 s. V max from the progressive work test approached a significant difference between groups (SCI 5.1 ± 2.9 vs. AB 9.8 ± 5.5 % Hb-Mb/s; p = 0.06). NIRS measurements of V max suggest a deficit of 50–60 % in participants with SCI compared with AB controls, consistent with previous studies using 31P-MRS and muscle biopsies. NIRS measurements can assess mitochondrial capacity in people with SCI and potentially other injured/diseased populations.
Literatur
Zurück zum Zitat Anderson EJ, Lustig ME, Boyle KE, Woodlief TL, Kane DA, Lin CT, Price JW, Kang L, Rabinovitch PS, Szeto HH, Houmard JA, Cortright RN, Wasserman DH, Neufer PD (2009) Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Investig 119(3):573–581. doi:10.1172/jci37048 PubMedCrossRef Anderson EJ, Lustig ME, Boyle KE, Woodlief TL, Kane DA, Lin CT, Price JW, Kang L, Rabinovitch PS, Szeto HH, Houmard JA, Cortright RN, Wasserman DH, Neufer PD (2009) Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Investig 119(3):573–581. doi:10.​1172/​jci37048 PubMedCrossRef
Zurück zum Zitat Argov Z, Bank W, Maris J, Chance B (1987) Bioenergetic heterogeneity of human mitochondrial myopathies: phosphorus magnetic resonance spectroscopy study. Neurology 37:257–262PubMedCrossRef Argov Z, Bank W, Maris J, Chance B (1987) Bioenergetic heterogeneity of human mitochondrial myopathies: phosphorus magnetic resonance spectroscopy study. Neurology 37:257–262PubMedCrossRef
Zurück zum Zitat Befroy DE, Petersen KF, Dufour S, Mason GF, de Graaf RA, Rothman DL, Shulman GI (2007) Impaired mitochondrial substrate oxidation in muscle of insulin-resistant offspring of type 2 diabetic patients. Diabetes 56(5):1376–1381. doi:10.2337/db06-0783 PubMedCrossRef Befroy DE, Petersen KF, Dufour S, Mason GF, de Graaf RA, Rothman DL, Shulman GI (2007) Impaired mitochondrial substrate oxidation in muscle of insulin-resistant offspring of type 2 diabetic patients. Diabetes 56(5):1376–1381. doi:10.​2337/​db06-0783 PubMedCrossRef
Zurück zum Zitat Brizendine JT, Ryan TE, Larson RD, McCully KK (2013) Skeletal muscle metabolism in endurance athletes with near-infrared spectroscopy. Med Sci Sports Exerc 45(5):869–875 Brizendine JT, Ryan TE, Larson RD, McCully KK (2013) Skeletal muscle metabolism in endurance athletes with near-infrared spectroscopy. Med Sci Sports Exerc 45(5):869–875
Zurück zum Zitat Castro MJ, Apple DF Jr, Melton-Rogers S, Dudley GA (2000) Muscle fiber type-specific myofibrillar Ca(2+) ATPase activity after spinal cord injury. Muscle Nerve 23(1):119–121PubMedCrossRef Castro MJ, Apple DF Jr, Melton-Rogers S, Dudley GA (2000) Muscle fiber type-specific myofibrillar Ca(2+) ATPase activity after spinal cord injury. Muscle Nerve 23(1):119–121PubMedCrossRef
Zurück zum Zitat 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 Nat Acad Sci 82:8384–8388PubMedCrossRef 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 Nat Acad Sci 82:8384–8388PubMedCrossRef
Zurück zum Zitat Chance B, Dait M, Zhang C, Hamaoka T, Hagerman F (1992) Recovery from exercise induced desaturation in the quadriceps muscles of elite competitive rowers. Am J Physiol 262:C766–C775PubMed Chance B, Dait M, Zhang C, Hamaoka T, Hagerman F (1992) Recovery from exercise induced desaturation in the quadriceps muscles of elite competitive rowers. Am J Physiol 262:C766–C775PubMed
Zurück zum Zitat Chance B, Im J, Nioka Shoko, Kushmerick M (2006) Skeletal muscle energetics with PNMR: personal views and historic perspectives. NMR Biomed 19(7):904–926PubMedCrossRef Chance B, Im J, Nioka Shoko, Kushmerick M (2006) Skeletal muscle energetics with PNMR: personal views and historic perspectives. NMR Biomed 19(7):904–926PubMedCrossRef
Zurück zum Zitat Chilibeck PD, Jeon J, Weiss C, Bell G, Burnham R (1999) Histochemical changes in muscle of individuals with spinal cord injury following functional electrical stimulated exercise training. Spinal Cord 37(4):264–268PubMedCrossRef Chilibeck PD, Jeon J, Weiss C, Bell G, Burnham R (1999) Histochemical changes in muscle of individuals with spinal cord injury following functional electrical stimulated exercise training. Spinal Cord 37(4):264–268PubMedCrossRef
Zurück zum Zitat DeBlasi R, 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 DeBlasi R, 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
Zurück zum Zitat Ferrari M, Binzoni T, Quaresima V (1997) Oxidative metabolism in muscle. Phil Trans R Soc Lond B 352:677–683CrossRef Ferrari M, Binzoni T, Quaresima V (1997) Oxidative metabolism in muscle. Phil Trans R Soc Lond B 352:677–683CrossRef
Zurück zum Zitat Hagströmer M, Oja P, Sjöström M (2006) The international physical activity questionnaire (IPAQ): a study of concurrent and construct validity. Public Health Nutr 9(6):755–762. doi:10.1079/PHN2005898 PubMedCrossRef Hagströmer M, Oja P, Sjöström M (2006) The international physical activity questionnaire (IPAQ): a study of concurrent and construct validity. Public Health Nutr 9(6):755–762. doi:10.​1079/​PHN2005898 PubMedCrossRef
Zurück zum Zitat Hamaoka T, McCully KK, Quaresima V, Yamamoto K, Chance B (2007) Near-infrared spectroscopy/imaging for monitoring muscle oxygenation and oxidative metabolism in healthy and diseased humans. J Biol Opt 12(6):062105CrossRef Hamaoka T, McCully KK, Quaresima V, Yamamoto K, Chance B (2007) Near-infrared spectroscopy/imaging for monitoring muscle oxygenation and oxidative metabolism in healthy and diseased humans. J Biol Opt 12(6):062105CrossRef
Zurück zum Zitat Larsen RG, Callahan DM, Foulis SA, Kent-Braun JA (2012) Age-related changes in oxidative capacity differ between locomotory muscles and are associated with physical activity behavior. Appl Physiol Nutr Metab 37(1):88–99. doi:10.1139/h11-135 PubMedCrossRef Larsen RG, Callahan DM, Foulis SA, Kent-Braun JA (2012) Age-related changes in oxidative capacity differ between locomotory muscles and are associated with physical activity behavior. Appl Physiol Nutr Metab 37(1):88–99. doi:10.​1139/​h11-135 PubMedCrossRef
Zurück zum Zitat Lehninger A (1976) Biochemistry, 2nd edn. Worth Publishers, Inc., New York Lehninger A (1976) Biochemistry, 2nd edn. Worth Publishers, Inc., New York
Zurück zum Zitat Levy M, Kushnir T, Mizrahi J, Itzchak Y (1993) In vivo 31P NMR studies of paraplegics’ muscles activated by functional electrical stimulation. Magn Reson Med 29(1):53–58PubMedCrossRef Levy M, Kushnir T, Mizrahi J, Itzchak Y (1993) In vivo 31P NMR studies of paraplegics’ muscles activated by functional electrical stimulation. Magn Reson Med 29(1):53–58PubMedCrossRef
Zurück zum Zitat Mahoney E, Puetz TW, Dudley GA, McCully KK (2007) Low-frequency fatigue in individuals with spinal cord injury. J Spinal Cord Med 30(5):458–466PubMed Mahoney E, Puetz TW, Dudley GA, McCully KK (2007) Low-frequency fatigue in individuals with spinal cord injury. J Spinal Cord Med 30(5):458–466PubMed
Zurück zum Zitat 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(6):530–536. doi:10.1177/0003319710362975 PubMedCrossRef 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(6):530–536. doi:10.​1177/​0003319710362975​ PubMedCrossRef
Zurück zum Zitat Martin TP, Stein RB, Hoeppner PH, Reid DC (1992) Influence of electrical stimulation on the morphological and metabolic properties of paralyzed muscle. J Appl Physiol 72(4):1401–1406PubMed Martin TP, Stein RB, Hoeppner PH, Reid DC (1992) Influence of electrical stimulation on the morphological and metabolic properties of paralyzed muscle. J Appl Physiol 72(4):1401–1406PubMed
Zurück zum Zitat 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(3):926–932PubMed 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(3):926–932PubMed
Zurück zum Zitat 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(2):813–819PubMed 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(2):813–819PubMed
Zurück zum Zitat Motobe M, Murase N, Osada T, Homma T, Uedo C, Nagasawa T, Kitahara A, Ichimura S, Kurosawa Y, Katsumura T, Hoskika A, Hamaoka T (2004) Noninvasive monitoring of deterioration in skeletal muscle function with forearm cast immobilization and the prevention of deterioration. Dyn Med 3(1):2PubMedCrossRef Motobe M, Murase N, Osada T, Homma T, Uedo C, Nagasawa T, Kitahara A, Ichimura S, Kurosawa Y, Katsumura T, Hoskika A, Hamaoka T (2004) Noninvasive monitoring of deterioration in skeletal muscle function with forearm cast immobilization and the prevention of deterioration. Dyn Med 3(1):2PubMedCrossRef
Zurück zum Zitat Nioka S, Kime R, Sunar U, Im J, Izzetoglu M, Zhang J, Alacam B, Chance B (2006) A novel method to measure regional muscle blood flow continuously using NIRS kinetics information. Dyn Med 5:5. doi:10.1186/1476-5918-5-5 PubMedCrossRef Nioka S, Kime R, Sunar U, Im J, Izzetoglu M, Zhang J, Alacam B, Chance B (2006) A novel method to measure regional muscle blood flow continuously using NIRS kinetics information. Dyn Med 5:5. doi:10.​1186/​1476-5918-5-5 PubMedCrossRef
Zurück zum Zitat Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI (2004) Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350(7):664–671. doi:10.1056/NEJMoa031314 PubMedCrossRef Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI (2004) Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350(7):664–671. doi:10.​1056/​NEJMoa031314 PubMedCrossRef
Zurück zum Zitat Richardson RS, Noyszewski EA, Haseler LJ, Bluml S, Frank LR (2002) Evolving techniques for the investigation of muscle bioenergetics and oxygenation. Biochem Soc Trans 30(2):232–237PubMedCrossRef Richardson RS, Noyszewski EA, Haseler LJ, Bluml S, Frank LR (2002) Evolving techniques for the investigation of muscle bioenergetics and oxygenation. Biochem Soc Trans 30(2):232–237PubMedCrossRef
Zurück zum Zitat Ryan TE, Brizendine JT, McCully KK (2013) A comparison of exercise type and intensity on the noninvasive assessment of skeletal muscle mitochondrial function using near infrared spectroscopy. J Appl Physiol 114(2):230–237. doi:10.1152/japplphysiol.01043.2012 Ryan TE, Brizendine JT, McCully KK (2013) A comparison of exercise type and intensity on the noninvasive assessment of skeletal muscle mitochondrial function using near infrared spectroscopy. J Appl Physiol 114(2):230–237. doi:10.​1152/​japplphysiol.​01043.​2012
Zurück zum Zitat 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(2):175–183. doi:10.1152/japplphysiol.00319.2012 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(2):175–183. doi:10.​1152/​japplphysiol.​00319.​2012
Zurück zum Zitat Scott WB, Lee SC, Johnston TE, Binkley J, Binder-Macleod SA (2006) Contractile properties and the force-frequency relationship of the paralyzed human quadriceps femoris muscle. Phys Ther 86(6):788–799PubMed Scott WB, Lee SC, Johnston TE, Binkley J, Binder-Macleod SA (2006) Contractile properties and the force-frequency relationship of the paralyzed human quadriceps femoris muscle. Phys Ther 86(6):788–799PubMed
Zurück zum Zitat Soden RJ, Walsh J, MIddleton JW, Craven ML, Rutkowski SB, Yeo JD (2000) Causes of death after spinal cord injury. Spinal Cord 38:604–610PubMedCrossRef Soden RJ, Walsh J, MIddleton JW, Craven ML, Rutkowski SB, Yeo JD (2000) Causes of death after spinal cord injury. Spinal Cord 38:604–610PubMedCrossRef
Zurück zum Zitat van Beekvelt M, Borghuis M, van Engelen B, Wevers R, Colier W (2001a) Adipose tissue thickness affects in vivo quantitative near-IR spectroscopy in human skeletal muscle. Clin Sci (Lond) 101:21–28CrossRef van Beekvelt M, Borghuis M, van Engelen B, Wevers R, Colier W (2001a) Adipose tissue thickness affects in vivo quantitative near-IR spectroscopy in human skeletal muscle. Clin Sci (Lond) 101:21–28CrossRef
Zurück zum Zitat van Beekvelt MCP, Shoemaker JK, Tschakovsky ME, Hopman MTE, Hughson R (2001b) Blood flow and muscle oxygen uptake at the onset and end of moderate and heavy dynamic forearm exercise. Am J Physiol Regul Integr Comp Physiol 280:R1741–R1747PubMed van Beekvelt MCP, Shoemaker JK, Tschakovsky ME, Hopman MTE, Hughson R (2001b) Blood flow and muscle oxygen uptake at the onset and end of moderate and heavy dynamic forearm exercise. Am J Physiol Regul Integr Comp Physiol 280:R1741–R1747PubMed
Zurück zum Zitat Walter G, Vandenborne K, McCully KK, Leigh JS (1997) Noninvasive measurement of phosphocreatine recovery kinetics in single human muscles. Am J Physiol 272(2 Pt 1):C525–C534PubMed Walter G, Vandenborne K, McCully KK, Leigh JS (1997) Noninvasive measurement of phosphocreatine recovery kinetics in single human muscles. Am J Physiol 272(2 Pt 1):C525–C534PubMed
Metadaten
Titel
Near-infrared assessments of skeletal muscle oxidative capacity in persons with spinal cord injury
verfasst von
Melissa Lynn Erickson
Terence E. Ryan
Hui-Ju Young
Kevin K. McCully
Publikationsdatum
01.09.2013
Verlag
Springer Berlin Heidelberg
Erschienen in
European Journal of Applied Physiology / Ausgabe 9/2013
Print ISSN: 1439-6319
Elektronische ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-013-2657-0

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