Top

Published in:

01-10-2017 | Original Article

Fatigability, oxygen uptake kinetics and muscle deoxygenation in incomplete spinal cord injury during treadmill walking

Authors: Jared M. Gollie, Jeffrey E. Herrick, Randall E. Keyser, Lisa M. K. Chin, John P. Collins, Richard K. Shields, Gino S. Panza, Andrew A. Guccione

Published in: European Journal of Applied Physiology | Issue 10/2017

Abstract

Purpose

The purpose of the present study was to characterize hypothesized relationships among fatigability and cardiorespiratory fitness in individuals with chronic motor-incomplete SCI (iSCI) during treadmill walking. The theoretical framework was that exacerbated fatigability would occur concomitantly with diminished cardiorespiratory fitness in people with iSCI.

Methods

Subjects with iSCI (n = 8) and an able-bodied reference group (REF) (n = 8) completed a 6-min walking bout followed by a walking bout of 30-min or until volitional exhaustion, both at a self-selected walking speed. Fatigability was assessed using both perceived fatigability and performance fatigability measures. Pulmonary oxygen uptake kinetics (VO₂ on-kinetics) was measured breath-by-breath and changes in deoxygenated hemoglobin/myoglobin concentration (∆[HHb]) of the lateral gastrocnemius was measured by near-infrared spectroscopy. Adjustment of VO₂ and ∆[HHb] on-kinetics were modeled using a mono-exponential equation.

Results

Perceived fatigability and performance fatigability were 52% and 44% greater in the iSCI group compared to the REF group (p = 0.003 and p = 0.004). Phase II time constant (τp) of VO₂ on-kinetics and ∆[HHb] ½ time during resting arterial occlusion were 55.4% and 16.3% slower in iSCI vs REF (p < 0.01 and p = 0.047, respectively).

Conclusions

The results of the present study may suggest that compromised O₂ delivery and/or utilization may have contributed to the severity of fatigability in these individuals with iSCI. The understanding of the extent to which fatigability and VO₂ and Δ[HHb] on-kinetics impacts locomotion after iSCI will assist in the future development of targeted interventions to enhance function.

Arena R, Humphrey R, Peberdy MA (2001) Measurement of oxygen consumption on-kinetics during exercise: implications for patients with heart failure. J Card Fail 7:302–310. doi:10.1054/jcaf.2001.27666 CrossRefPubMed

Barstow TJ, Scremin AM, Mutton DL et al (1995) Gas exchange kinetics during functional electrical stimulation in subjects with spinal cord injury. Med Sci Sports Exerc 27:1284–1291CrossRefPubMed

Biering-Sørensen B, Kristensen IB, Kjaer M, Biering-Sørensen F (2009) Muscle after spinal cord injury. Muscle Nerve 40:499–519. doi:10.1002/mus.21391 CrossRefPubMed

Brittain CJ, Rossiter HB, Kowalchuk JM, Whipp BJ (2001) Effect of prior metabolic rate on the kinetics of oxygen uptake during moderate-intensity exercise. Eur J Appl Physiol 86:125–134. doi:10.1007/s004210100514 CrossRefPubMed

Burns SP, Golding DG, Rolle WA et al (1997) Recovery of ambulation in motor-incomplete tetraplegia. Arch Phys Med Rehabil 78:1169–1172CrossRefPubMed

Cavagna GA, Heglund NC, Taylor CR (1977) Mechanical work in terrestrial locomotion: two basic mechanisms for minimizing energy expenditure. Am J Physiol 233:R243–R261PubMed

Chaudhuri A, Behan PO (2004) Fatigue in neurological disorders. Lancet Lond Engl 363:978–988. doi:10.1016/S0140-6736(04)15794-2 CrossRef

Chin LMK, Heigenhauser GJF, Paterson DH, Kowalchuk JM (2010) Effect of hyperventilation and prior heavy exercise on O₂ uptake and muscle deoxygenation kinetics during transitions to moderate exercise. Eur J Appl Physiol 108:913–925. doi:10.1007/s00421-009-1293-1 CrossRefPubMed

Chin LMK, Kowalchuk JM, Barstow TJ et al (2011) The relationship between muscle deoxygenation and activation in different muscles of the quadriceps during cycle ramp exercise. J Appl Physiol Bethesda Md 1985(111):1259–1265. doi:10.1152/japplphysiol.01216.2010

Craig A, Tran Y, Wijesuriya N, Middleton J (2012) Fatigue and tiredness in people with spinal cord injury. J Psychosom Res 73:205–210. doi:10.1016/j.jpsychores.2012.07.005 CrossRefPubMed

de Smirmaul B de PC (2012) Sense of effort and other unpleasant sensations during exercise: clarifying concepts and mechanisms. Br J Sports Med 46:308–311. doi:10.1136/bjsm.2010.071407 CrossRef

Edgerton VR, Courtine G, Gerasimenko YP et al (2008) Training locomotor networks. Brain Res Rev 57:241–254. doi:10.1016/j.brainresrev.2007.09.002 CrossRefPubMed

Enoka RM, Duchateau J (2016) Translating fatigue to human performance. Med Sci Sports Exerc 48:2228–2238. doi:10.1249/MSS.0000000000000929 CrossRefPubMed

Erickson ML, Ryan TE, Young H-J, McCully KK (2013) Near-infrared assessments of skeletal muscle oxidative capacity in persons with spinal cord injury. Eur J Appl Physiol 113:2275–2283. doi:10.1007/s00421-013-2657-0 CrossRefPubMedPubMedCentral

Fawkes-Kirby TM, Wheeler MA, Anton HA et al (2008) Clinical correlates of fatigue in spinal cord injury. Spinal Cord 46:21–25. doi:10.1038/sj.sc.3102053 CrossRefPubMed

Gollie JM, Guccione AA, Panza GS et al (2017) Effects of overground locomotor training on walking performance in chronic cervical motor incomplete spinal cord injury: a pilot study. Arch Phys Med Rehabil 98:1119–1125. doi:10.1016/j.apmr.2016.10.022 CrossRefPubMed

Grassi B, Quaresima V (2016) Near-infrared spectroscopy and skeletal muscle oxidative function in vivo in health and disease: a review from an exercise physiology perspective. J Biomed Opt 21:091313. doi:10.1117/1.JBO.21.9.091313 CrossRefPubMed

Grassi B, Poole DC, Richardson RS et al (1996) Muscle O₂ uptake kinetics in humans: implications for metabolic control. J Appl Physiol Bethesda Md 1985(80):988–998

Grassi B, Porcelli S, Salvadego D, Zoladz JA (2011) Slow VO₂ kinetics during moderate-intensity exercise as markers of lower metabolic stability and lower exercise tolerance. Eur J Appl Physiol 111:345–355. doi:10.1007/s00421-010-1609-1 CrossRefPubMed

Gurd BJ, Peters SJ, Heigenhauser GJF et al (2009) Prior heavy exercise elevates pyruvate dehydrogenase activity and muscle oxygenation and speeds O₂ uptake kinetics during moderate exercise in older adults. Am J Physiol Regul Integr Comp Physiol 297:R877–R884. doi:10.1152/ajpregu.90848.2008 CrossRefPubMed

Haas F, Axen K, Pineda H (1986) Aerobic capacity in spinal cord injured people. Cent Nerv Syst Trauma J Am Paralys Assoc 3:77–91

Hamaoka T, McCully KK, Quaresima V et al (2007) Near-infrared spectroscopy/imaging for monitoring muscle oxygenation and oxidative metabolism in healthy and diseased humans. J Biomed Opt 12:062105. doi:10.1117/1.2805437 CrossRefPubMed

Hammell KW, Miller WC, Forwell SJ et al (2009) Fatigue and spinal cord injury: a qualitative analysis. Spinal Cord 47:44–49. doi:10.1038/sc.2008.68 CrossRefPubMed

Inman VT (1967) Conservation of energy in ambulation. Arch Phys Med Rehabil 48:484–488PubMed

Jensen MP, Kuehn CM, Amtmann D, Cardenas DD (2007) Symptom burden in persons with spinal cord injury. Arch Phys Med Rehabil 88:638–645. doi:10.1016/j.apmr.2007.02.002 CrossRefPubMedPubMedCentral

Jones AM, Poole DC (eds) (2005) Oxygen uptake kinetics in sport, exercise and medicine. Routledge, London

Kent-Braun JA, Fitts RH, Christie A (2012) Skeletal muscle fatigue. In: Terjung R (ed) Comprehensive physiology. Wiley, Hoboken

Keyser RE, Rus V, Mikdashi JA, Handwerger BS (2010) Exploratory study on oxygen consumption on-kinetics during treadmill walking in women with systemic lupus erythematosus. Arch Phys Med Rehabil 91:1402–1409. doi:10.1016/j.apmr.2010.06.003 CrossRefPubMedPubMedCentral

Kirshblum S, Waring W (2014) Updates for the international standards for neurological classification of spinal cord injury. Phys Med Rehabil Clin N Am 25:505–517. doi:10.1016/j.pmr.2014.04.001 CrossRefPubMed

Kuo AD, Donelan JM (2010) Dynamic principles of gait and their clinical implications. Phys Ther 90:157–174. doi:10.2522/ptj.20090125 CrossRefPubMedPubMedCentral

Lamarra N, Whipp BJ, Ward SA, Wasserman K (1987) Effect of interbreath fluctuations on characterizing exercise gas exchange kinetics. J Appl Physiol Bethesda Md 1985(62):2003–2012

Lewis JE, Nash MS, Hamm LF et al (2007) The relationship between perceived exertion and physiologic indicators of stress during graded arm exercise in persons with spinal cord injuries. Arch Phys Med Rehabil 88:1205–1211. doi:10.1016/j.apmr.2007.05.016 CrossRefPubMed

McCully KK, Hamaoka T (2000) Near-infrared spectroscopy: what can it tell us about oxygen saturation in skeletal muscle? Exerc Sport Sci Rev 28:123–127PubMed

McCully KK, Mulcahy TK, Ryan TE, Zhao Q (2011) Skeletal muscle metabolism in individuals with spinal cord injury. J Appl Physiol 111:143–148. doi:10.1152/japplphysiol.00094.2011 CrossRefPubMedPubMedCentral

Mehrholz J, Kugler J, Pohl M (2012) Locomotor training for walking after spinal cord injury. In: The Cochrane Collaboration (ed) Cochrane database of systematic reviews. Wiley, Chichester

Mehrholz J, Harvey LA, Thomas S, Elsner B (2017) Is body-weight-supported treadmill training or robotic-assisted gait training superior to overground gait training and other forms of physiotherapy in people with spinal cord injury? A systematic review. Spinal Cord. doi:10.1038/sc.2017.31 PubMed

Morawietz C, Moffat F (2013) Effects of locomotor training after incomplete spinal cord injury: a systematic review. Arch Phys Med Rehabil 94:2297–2308. doi:10.1016/j.apmr.2013.06.023 CrossRefPubMed

Nooijen CFJ, Vogels S, Bongers-Janssen HMH et al (2015) Fatigue in persons with subacute spinal cord injury who are dependent on a manual wheelchair. Spinal Cord 53:758–762. doi:10.1038/sc.2015.66 CrossRefPubMed

Ozyener F, Rossiter HB, Ward SA, Whipp BJ (2001) Influence of exercise intensity on the on- and off-transient kinetics of pulmonary oxygen uptake in humans. J Physiol 533:891–902CrossRefPubMedPubMedCentral

Papaiordanidou M, Varray A, Fattal C, Guiraud D (2014) Neural and muscular mechanisms of electrically induced fatigue in patients with spinal cord injury. Spinal Cord 52:246–250. doi:10.1038/sc.2013.172 CrossRefPubMed

Pelletier CA, Hicks AL (2011) Muscle fatigue characteristics in paralyzed muscle after spinal cord injury. Spinal Cord 49:125–130. doi:10.1038/sc.2010.62 CrossRefPubMed

Petrie MA, Suneja M, Faidley E, Shields RK (2014) Low force contractions induce fatigue consistent with muscle mRNA expression in people with spinal cord injury. Physiol Rep. doi:10.1002/phy2.248 PubMedPubMedCentral

Petrie M, Suneja M, Shields RK (2015) Low-frequency stimulation regulates metabolic gene expression in paralyzed muscle. J Appl Physiol 118:723–731. doi:10.1152/japplphysiol.00628.2014 CrossRefPubMedPubMedCentral

Poole DC, Jones AM (2012) Oxygen uptake kinetics. In: Terjung R (ed) Comprehensive physiology. Wiley, Hoboken

Rossiter HB, Howe FA, Ward SA et al (2000) Intersample fluctuations in phosphocreatine concentration determined by ³¹P-magnetic resonance spectroscopy and parameter estimation of metabolic responses to exercise in humans. J Physiol 528:359–369. doi:10.1111/j.1469-7793.2000.t01-1-00359.x CrossRefPubMedPubMedCentral

Schalcher C, Rickli H, Brehm M et al (2003) Prolonged oxygen uptake kinetics during low-intensity exercise are related to poor prognosis in patients with mild-to-moderate congestive heart failure. Chest 124:580–586CrossRefPubMed

Schnelle JF, Buchowski MS, Ikizler TA et al (2012) Evaluation of two fatigability severity measures in elderly adults. J Am Geriatr Soc 60:1527–1533. doi:10.1111/j.1532-5415.2012.04062.x CrossRefPubMedPubMedCentral

Shah PK, Stevens JE, Gregory CM et al (2006) Lower-extremity muscle cross-sectional area after incomplete spinal cord injury. Arch Phys Med Rehabil 87:772–778. doi:10.1016/j.apmr.2006.02.028 CrossRefPubMed

Sheriff DD (2003) Muscle pump function during locomotion: mechanical coupling of stride frequency and muscle blood flow. Am J Physiol Heart Circ Physiol 284:H2185–H2191. doi:10.1152/ajpheart.01133.2002 CrossRefPubMed

Shields RK (1995) Fatigability, relaxation properties, and electromyographic responses of the human paralyzed soleus muscle. J Neurophysiol 73:2195–2206PubMed

Spinal Cord Injury (SCI) (2016) Facts and figures at a glance. J Spinal Cord Med 39:493–494. doi:10.1080/10790268.2016.1210925 CrossRef

Waters RL, Lunsford BR (1985) Energy cost of paraplegic locomotion. J Bone Jt Surg Am 67:1245–1250CrossRef

Waters RL, Mulroy S (1999) The energy expenditure of normal and pathologic gait. Gait Posture 9:207–231CrossRefPubMed

Waters RL, Lunsford BR, Perry J, Byrd R (1988) Energy-speed relationship of walking: standard tables. J Orthop Res 6:215–222. doi:10.1002/jor.1100060208 CrossRefPubMed

West CR, Bellantoni A, Krassioukov AV (2013) Cardiovascular function in individuals with incomplete spinal cord injury: a systematic review. Top Spinal Cord Inj Rehabil 19:267–278. doi:10.1310/sci1904-267 CrossRefPubMedPubMedCentral

Wilson JR, Mancini DM, McCully K et al (1989) Noninvasive detection of skeletal muscle underperfusion with near-infrared spectroscopy in patients with heart failure. Circulation 80:1668–1674CrossRefPubMed

Zarrugh MY, Todd FN, Ralston HJ (1974) Optimization of energy expenditure during level walking. Eur J Appl Physiol 33:293–306CrossRef

Title: Fatigability, oxygen uptake kinetics and muscle deoxygenation in incomplete spinal cord injury during treadmill walking
Authors: Jared M. Gollie
Jeffrey E. Herrick
Randall E. Keyser
Lisa M. K. Chin
John P. Collins
Richard K. Shields
Gino S. Panza
Andrew A. Guccione
Publication date: 01-10-2017
Publisher: Springer Berlin Heidelberg
Published in: European Journal of Applied Physiology / Issue 10/2017
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI: https://doi.org/10.1007/s00421-017-3685-y

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Fatigability, oxygen uptake kinetics and muscle deoxygenation in incomplete spinal cord injury during treadmill walking

Abstract

Purpose

Methods

Results

Conclusions

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 10/2017

Increase in echo intensity and extracellular-to-intracellular water ratio is independently associated with muscle weakness in elderly women

The effects of supramaximal versus submaximal intensity eccentric training when performed until volitional fatigue

Classical experiments in whole-body metabolism: closed-circuit respirometry

Early detection of exercise-induced muscle damage using elastography

Aerobic interval training reduces vascular resistances during submaximal exercise in obese metabolic syndrome individuals

Erratum to: Sitting position affects performance in cross-country sit-skiing