Abstract
Hemiparesis after stroke decreases ability to dorsiflex the more-affected ankle during walking. Increased strength would be beneficial, but the more-affected limb is often too weak to be trained. In neurologically intact participants, training one limb induces strength gains in the contralateral, untrained limb. This approach remains unexplored post-stroke. The aim of this study was to test the hypothesis that unilateral dorsiflexor high-intensity resistance training on the less-affected side increases strength and motor output bilaterally following stroke. 19 participants (84.1 ± 77.6 months post-infarct) performed 6 weeks of maximal isometric dorsiflexion training using the less-affected leg. Voluntary isometric strength (dorsiflexion torque, muscle activation), reciprocal inhibition (RI), walking ability (gait speed, kinematics, EMG patterns), and clinical function were measured within 1 week before and 4 days following training. Post-intervention, dorsiflexion torque increased by ~31 % (p < 0.05) in the more-affected (untrained) and by ~34 % (p < 0.05) in the less-affected (trained) legs. Muscle activation significantly increased bilaterally, by ~59 and ~20 % in the trained and untrained legs, respectively. Notably, 4 participants who were unable to generate functional dorsiflexion on the more-affected side before training could do so post-intervention. Significant correlations between muscle activation and size of RI were noted across muscle groups before and after training, and the relation between size of RI and level of muscle activation in the more-affected tibialis anterior muscle was significantly altered by training. Thus, significant gains in voluntary strength and muscle activation on the untrained, more-affected side after stroke can be invoked through training the opposite limb. We demonstrate residual plasticity existing many years post-stroke and suggest clinical application of the cross-education effect where training the more-affected limb is not initially possible.
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References
Abe T, DeHoyos DV, Pollock ML, Garzarella L (2000) Time course for strength and muscle thickness changes following upper and lower body resistance training in men and women. Eur J Appl Physiol 81:174–180
Adams RW, Gandevia SC, Skuse NF (1990) The distribution of muscle weakness in upper motoneuron lesions affecting the lower limb. Brain 113(Pt 5):1459–1476
Barzi Y, Zehr EP (2008) Rhythmic arm cycling suppresses hyperactive soleus H-reflex amplitude after stroke. Clin Neurophysiol 119:1443–1452. doi:10.1016/j.clinph.2008.02.016
Beckerman H, Roebroeck ME, Lankhorst GJ, Becher JG, Bezemer PD, Verbeek AL (2001) Smallest real difference, a link between reproducibility and responsiveness. Qual Life Res 10:571–578
Berg KO, Wood-Dauphinee SL, Williams JI, Maki B (1992) Measuring balance in the elderly: validation of an instrument. Can J Public Health 83(Suppl 2):S7–S11
Bird SP, Tarpenning KM, Marino FE (2005) Designing resistance training programmes to enhance muscular fitness: a review of the acute programme variables. Sports Med 35:841–851
Butefisch C (1995) Repetitive training of isolated movements improves the outcome of motor rehabilitation of the centrally paretic hand. J Neurol Sci 130:59–68
Capaday C, Cody FW, Stein RB (1990) Reciprocal inhibition of soleus motor output in humans during walking and voluntary tonic activity. J Neurophysiol 64:607–616
Carroll TJ, Herbert RD, Munn J, Lee M, Gandevia SC (2006) Contralateral effects of unilateral strength training: evidence and possible mechanisms. J Appl Physiol 101:1514–1522. doi:10.1152/japplphysiol.00531.2006
Carroll TJ, Lee M, Hsu M, Sayde J (2008) Unilateral practice of a ballistic movement causes bilateral increases in performance and corticospinal excitability. J Appl Physiol 104:1656–1664. doi:10.1152/japplphysiol.01351.2007
Cohen J (1992) A power primer. Psychol Bull 112:155–159
Crone C, Nielsen J, Petersen N, Ballegaard M, Hultborn H (1994) Disynaptic reciprocal inhibition of ankle extensors in spastic patients. Brain 117(Pt 5):1161–1168
Crone C, Johnsen LL, Biering-Sorensen F, Nielsen JB (2003) Appearance of reciprocal facilitation of ankle extensors from ankle flexors in patients with stroke or spinal cord injury. Brain 126:495–507
Delwaide PJ, Pepin JL (1991) The influence of contralateral primary afferents on Ia inhibitory interneurones in humans. J Physiol 439:161–179
Delwaide PJ, Sabatino M, Pepin JL, La Grutta V (1988) Reinforcement of reciprocal inhibition by contralateral movements in man. Exp Neurol 99:10–16
Dobkin B (2003) The clinical science of neurologic rehabilitation. Oxford University Press, Oxford
Dragert K, Zehr EP (2011) Bilateral neuromuscular plasticity from unilateral training of the ankle dorsiflexors. Exp Brain Res 208:217–227. doi:10.1007/s00221-010-2472-3
Duncan PW, Zorowitz R, Bates B, Choi JY, Glasberg JJ, Graham GD, Katz RC, Lamberty K, Reker D (2005) Management of adult stroke rehabilitation care: a clinical practice guideline. Stroke 36:e100–e143. doi:10.1161/01.STR.0000180861.54180.FF
Eng JJ (2004) Strength training in individuals with stroke. Physiother Can 56:189–201
Engardt M, Knutsson E, Jonsson M, Sternhag M (1995) Dynamic muscle strength training in stroke patients: effects on knee extension torque, electromyographic activity, and motor function. Arch Phys Med Rehabil 76:419–425
Farthing JP, Krentz JR, Magnus CRA (2009) Strength training the free limb attenuates strength loss during unilateral immobilization. J Appl Physiol 106:830–836
Fimland MS, Helgerud J, Solstad GM, Iversen VM, Leivseth G, Hoff J (2009) Neural adaptations underlying cross-education after unilateral strength training. Eur J Appl Physiol 107:723–730. doi:10.1007/s00421-009-1190-7
Flansbjer UB, Holmback AM, Downham D, Patten C, Lexell J (2005) Reliability of gait performance tests in men and women with hemiparesis after stroke. J Rehabil Med 37:75–82. doi:10.1080/16501970410017215
Fugl-Meyer AR, Jaasko L, Leyman I, Olsson S, Steglind S (1975) Post-stroke hemiplegic patient: 1. A Method for evaluation of physical performance. Scand J Rehabil Med 7:13–31
Geertsen SS, Lundbye-Jensen J, Nielsen JB (2008) Increased central facilitation of antagonist reciprocal inhibition at the onset of dorsiflexion following explosive strength training. J Appl Physiol 105:915–922. doi:10.1152/japplphysiol.01155.2007
Gracies JM (2005) Pathophysiology of spastic paresis. II: emergence of muscle overactivity. Muscle Nerve 31:552–571. doi:10.1002/mus.20285
Haridas C, Zehr EP (2003) Coordinated interlimb compensatory responses to electrical stimulation of cutaneous nerves in the hand and foot during walking. J Neurophysiol 90:2850–2861. doi:10.1152/jn.00531.2003
Holden MK, Gill KM, Magliozzi MR, Nathan J, Piehl-Baker L (1984) Clinical gait assessment in the neurologically impaired. Reliability and meaningfulness. Phys Ther 64:35–40
Hubal MJ, Gordish-Dressman H, Thompson PD, Price TB, Hoffman EP, Angelopoulos TJ, Gordon PM, Moyna NM, Pescatello LS, Visich PS, Zoeller RF, Seip RL, Clarkson PM (2005) Variability in muscle size and strength gain after unilateral resistance training. Med Sci Sports Exerc 37:964–972
Huston R (2009) Principles of biomechanics. CRC Press, Boca Raton
Kido A, Tanaka N, Stein RB (2004) Spinal reciprocal inhibition in human locomotion. J Appl Physiol 96:1969–1977. doi:10.1152/japplphysiol.01060.2003
Krakauer J (2005) Arm function after stroke: from physiology to recovery. Semin Neurol 25:384–395
Lagerquist O, Zehr EP, Baldwin ERL, Klakowicz PM, Collins DF (2006a) Diurnal changes in the amplitude of the Hoffmann reflex in the human soleus but not in the flexor carpi radialis muscle. Exp Brain Res 170:1–6. doi:10.1007/s00221-005-0172-1
Lagerquist O, Zehr EP, Docherty D (2006b) Increased spinal reflex excitability is not associated with neural plasticity underlying the cross-education effect. J Appl Physiol 100:83–90. doi 10.1152/japplphysiol.00533.2005
Lee M, Carroll TJ (2007) Cross education: possible mechanisms for the contralateral effects of unilateral resistance training. Sports Med 37:1–14
Lee KC, Carson L, Kinnin E, Patterson V (1989) The Ashworth Scale: a reliable and reproducible method of measuring spasticity. Neurorehabil Neural Repair 205–209. doi:10.1177/136140968900300406
Magnus CRA, Barss TS, Lanovaz JL, Farthing JP (2010) Effects of cross-education on the muscle after a period of unilateral limb immobilization using a shoulder sling and swathe. J Appl Physiol 109:1887–1894
Moritani T, deVries HA (1979) Neural factors versus hypertrophy in the time course of muscle strength gain. Am J Phys Med 58:115–130
Morris SL, Dodd KJ, Morris ME (2004) Outcomes of progressive resistance strength training following stroke: a systematic review. Clin Rehabil 18:27–39
Munn J (2005) Training with unilateral resistance exercise increases contralateral strength. J Appl Physiol 99:1880–1884
Munn J, Herbert RD, Gandevia SC (2004) Contralateral effects of unilateral resistance training: a meta-analysis. J Appl Physiol 96:1861–1866. doi:10.1152/japplphysiol.00541.2003
Olsen TS (1989) Improvement of function and motor impairment after stroke. Neurorehabil Neural Repair 3:187–192
Patten C, Lexell J, Brown HE (2004) Weakness and strength training in persons with poststroke hemiplegia: rationale, method, and efficacy. J Rehabil Res Dev 41:293–312
Podsiadlo D, Richardson S (1991) The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 39:142–148
Scripture EW, Smith TL, Brown EM (1894) On the education of muscular control and power. Studies Yale Psych Lab 2:114–119
Sharp SA, Brouwer BJ (1997) Isokinetic strength training of the hemiparetic knee: effects on function and spasticity. Arch Phys Med Rehabil 78:1231–1236
Sheskin DJ (2004) Handbook of parametric and non-parametric statistical procedures. Chapman & Hall/CRC, Boca Raton
Shima N (2002) Cross education of muscular strength during unilateral resistance training and detraining. Eur J Appl Physiol 86:287–294
Stein RB, Thompson AK (2006) Muscle reflexes in motion: how, what, and why. Exerc Sport Sci Rev 34:145–153. doi:10.1249/01.jes.0000240024.37996.e5
Taylor NF, Dodd KJ, Damiano DL (2005) Progressive resistance exercise in physical therapy: a summary of systematic reviews. Phys Ther 85:1208–1223
Thompson AK, Estabrooks KL, Chong S, Stein RB (2009) Spinal reflexes in ankle flexor and extensor muscles after chronic central nervous system lesions and functional electrical stimulation. Neurorehabil Neural Repair 23:133–142. doi:10.1177/1545968308321067
Zehr EP (2002) Considerations for use of the Hoffmann reflex in exercise studies. Eur J Appl Physiol 86:455–468. doi:10.1007/s00421-002-0577-5
Zehr EP (2011) Evidence-based risk assessment and recommendations for physical activity clearance: stroke and spinal cord injury. Appl Physiol Nutr Metab 36:S231
Zehr EP, Loadman PM (2012) Persistence of locomotor-related interlimb reflex networks during walking after stroke. Clin Neurophysiol 123:796–807. doi:10.1016/j.clinph.2011.07.049
Acknowledgments
The authors wish to acknowledge Holly Murray and Pamela Loadman for their contributions during data acquisition. This work was supported by the Heart and Stroke Foundation of Canada (BC & Yukon). Funding sources had no involvement in study design, nor in data collection, analyses, and/or interpretation.
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Dragert, K., Zehr, E.P. High-intensity unilateral dorsiflexor resistance training results in bilateral neuromuscular plasticity after stroke. Exp Brain Res 225, 93–104 (2013). https://doi.org/10.1007/s00221-012-3351-x
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DOI: https://doi.org/10.1007/s00221-012-3351-x