Training Modifies Corticomotor Function in Walking Activity in Athletes with Anterior Cruciate Ligament Rupture

Document Type : Original article

Authors

1 Department of Motor Behavior, Central Tehran Branch, Islamic Azad University, Tehran, Iran.

2 Department of Motor Control, Faculty of Rehabilitation, Tehran University of Medical Sciences, Tehran, Iran.

3 Department of Knowledge and Cognitive Intelligence, Imam Hossein University, Tehran, Iran.

4 Department of Sport Management, Faculty of Physical Education and Sport Sciences, Central Branch of Islamic Azad University, Tehran, Iran.

10.32598/SJRM.13.5.1

Abstract

Background and Aims Due to the lack of mechanoreceptors in people with anterior cruciate ligament rupture (ACLR), sensory and motor neuroplasticity occurs, which causes abnormal and asymmetric motor control patterns in the lower limbs. Perturbation-based training can improve motor asymmetry and functional deficits in people with ACLR. In this study, we used a mechanical perturbation training to assess its effect on the cortico-muscular performance during walking in athletes with ACLR.
Methods Thirty athletes with unilateral ACLR were randomly assigned to two groups of perturbation-based and standard training. The training program of the two groups was done in three sessions every other day per week for one month. The surface electromyography and relative power analysis of alpha and beta waves in quantitative electroencephalography were performed during a walking task.
Results The perturbation-based training group showed a significantly higher muscle activity in both healthy and affected knees after increase in the similarity index (P=0.08, Cohen’s d=0.81), while there was no significant difference in the standard training group (P=0.39, Cohen’s d= 0.39). In cortical activity tests, the perturbation-based training group showed excellent symmetry in the relative power of alpha wave compared to the standard training group (P=0.94, Cohen’s d =0.02) and a good symmetry in the relative power of beta wave (P=0.24, Cohen’s d=0.26).
Conclusion The perturbation-based training is a more appropriate training for athletes with ACLR, probably due to having real-world challenges. 

Keywords

Main Subjects

References

  1. Grooms D, Appelbaum G, Onate J. Neuroplasticity following anterior cruciate ligament injury: A framework for visual-motor training approaches in rehabilitation. The Journal of Orthopaedic and Sports Physical Therapy. 2015; 45(5):381-93. [DOI:10.2519/jospt.2015.5549][PMID]
  2. Diermeier T, Rothrauff BB, Engebretsen L, Lynch AD, Ayeni OR, Paterno MV, et al. Treatment after anterior cruciate ligament injury: Panther Symposium ACL Treatment Consensus Group. Knee Surgery, Sports Traumatology, Arthroscopy: Official Journal of the ESSKA. 2020; 28(8):2390–402. [DOI:10.1007/s00167-020-06012-6][PMID]
  3. Nawasreh Z, Logerstedt D, Failla M, Snyder-Mackler L. No difference between mechanical perturbation training with compliant surface and manual perturbation training on knee functional performance after ACL rupture. Journal of Orthopaedic Research: Official Publication of the Orthopaedic Research Society. 2018; 36(5):1391-7. [DOI:10.1002/jor.23784][PMID]
  4. Hartigan E, Axe MJ, Snyder-Mackler L. Perturbation training prior to ACL reconstruction improves gait asymmetries in non-copers. Journal of Orthopaedic Research: Official Publication of the Orthopaedic Research Society. 2009; 27(6):724-9. [DOI:10.1002/jor.20754][PMID]
  5. Nawasreh ZH, Marmon AR, Logerstedt D, Snyder-Mackler L. The effect of training on a compliant surface on muscle activation and co-contraction after anterior cruciate ligament injury. International Journal of Sports Physical Therapy. 2019; 14(4):3554-63. [DOI:10.26603/ijspt20190554][PMID]
  6. Nawasreh Z, Failla M, Marmon A, Logerstedt D, Snyder-Mackler L. Comparing the effects of mechanical perturbation training with a compliant surface and manual perturbation training on joints kinematics after ACL-rupture. Gait & Posture. 2018; 64:43-9. [DOI:10.1016/j.gaitpost.2018.05.027][PMID]
  7. Miao X, Huang H, Hu X, Li D, Yu Y, Ao Y. The characteristics of EEG power spectra changes after ACL rupture. PLoS One. 2017; 12(2):e0170455. [DOI:10.1371/journal.pone.0170455][PMID]
  8. Neto T, Sayer T, Theisen D, Mierau A. Functional brain plasticity associated with ACL injury: A scoping review of current evidence. Neural Plasticity. 2019; 2019:3480512. [DOI:10.1155/2019/3480512][PMID]
  9. Needle AR, Lepley AS, Grooms DR. Central nervous system adaptation after ligamentous injury: A summary of theories, evidence, and clinical interpretation. Sports Medicine (Auckland, N.Z.). 2017; 47(7):1271-88. [DOI:10.1007/s40279-016-0666-y][PMID]
  10. Daneshmandi H, Payandeh M, Mohammad Ashour Z. Brain neuroplasticity effects on the occurrence of anterior cruciate ligament injury and the effect of this injury on brain function and structure: A systematic review. Archives of Rehabilitation (Previously title "Journal of Rehabilitation"). 2022; 23(2):162-85. [DOI:10.32598/RJ.23.2.3377.1]
  11. Grooms DR, Page S, Onate JA. Brain activation for knee movement measured days before second anterior cruciate ligament injury: Neuroimaging in musculoskeletal medicine. Journal of Athletic Training. 2015; 50(10):1005–10. [DOI:10.4085/1062-6050-50-10-02] [PMID]
  12. Okuda K, Abe N, Katayama Y, Senda M, Kuroda T, Inoue H. Effect of vision on postural sway in anterior cruciate ligament injured knees. Journal of Orthopaedic Science: Official Journal of the Japanese Orthopaedic As 2005; 10(3):277-83. [DOI:10.1007/s00776-005-0893-9][PMID]
  13. Héroux ME, Tremblay F. Corticomotor excitability associated with unilateral knee dysfunction secondary to anterior cruciate ligament injury. Knee Surgery, Sports Traumatology, Arthroscopy: Official Journal of the ESSKA. 2006; 14(9):823-33. [DOI:10.1007/s00167-006-0063-4][PMID]
  14. Criss CR, Melton MS, Ulloa SA, Simon JE, Clark BC, France CR, et al. Rupture, reconstruction, and rehabilitation: A multi-disciplinary review of mechanisms for central nervous system adaptations following anterior cruciate ligament injury. The Knee. 2021; 30:78-89. [DOI:10.1016/j.knee.2021.03.009][PMID]
  15. Kapreli E, Athanasopoulos S. The anterior cruciate ligament deficiency as a model of brain plasticity. Medical 2006; 67(3):645-50. [DOI:10.1016/j.mehy.2006.01.063][PMID]
  16. Moksnes H, Snyder-Mackler L, Risberg MA. Individuals with an anterior cruciate ligament-deficient knee classified as noncopers may be candidates for nonsurgical rehabilitation. The Journal of Orthopaedic and Sports Physical Therapy. 2008; 38(10):586-95. [DOI:10.2519/jospt.2008.2750][PMID]
  17. Gokeler A, Bisschop M, Myer GD, Benjaminse A, Dijkstra PU, van Keeken HG, et al. Immersive virtual reality improves movement patterns in patients after ACL reconstruction: Implications for enhanced criteria-based return-to-sport rehabilitation. Knee Surgery, Sports Traumatology, Arthroscopy: Official Journal of the ESSKA. 2016; 24(7):2280-6. [DOI:10.1007/s00167-014-3374-x][PMID]
  18. Jomhouri S, Talebian S, Vaez Mousavi M, Hatef B, Sadjadi-Hazaveh SH. Corticomuscular adaptations in the single-leg jump task in response to progressive mechanical perturbation training in individuals with anterior cruciate ligament deficiency. Journal of Modern Rehabilitation. 2022; 16(1):85-100. [DOI:10.18502/jmr.v16i1.8572]
  19. Jomhouri S, Talebian S, Vaez Mousavi M, Hatef B, Sadjadi-Hazaveh SH. Changes in the trend of walking motor control in athletes with anterior cruciate ligament deficiency in response to progressive perturbation trainings. Austin Sports Medicine. 2021; 6(1):1045-53. [DOI:10.26420/austinsportsmed.2021.1045]
  20. Kim HJ, Lee JH, Lee DH. Proprioception in patients with anterior cruciate ligament tears: A meta-analysis comparing injured and uninjured limbs. The American Journal of Sports Medicine. 2017; 45(12):2916-22. [DOI:10.1177/0363546516682231][PMID]
  21. Dominic D, Saravanan P, Kishore S. A quantitative assessment of proprioceptive function improvement after Arthroscopic ACL Reconstruction surgery. Journal of Evolution of Medical and Dental Sciences. 2015; 4(38):6565-71. [DOI:10.14260/jemds/2015/952]
  22. Han J, Waddington G, Adams R, Anson J, Liu Y. Assessing proprioception: A critical review of methods. Journal of Sport and Health Science. 2016; 5(1):80-90. [DOI:10.1016/j.jshs.2014.10.004][PMID]
  23. Gokeler A, Neuhaus D, Benjaminse A, Grooms DR, Baumeister J. Principles of motor learning to support neuroplasticity after ACL injury: Implications for optimizing performance and reducing risk of second ACL injury. Sports Medicine (Auckland, N.Z.). 2019; 49(6):853-65. [DOI:10.1007/s40279-019-01058-0][PMID]
  24. Gokeler A, Seil R, Kerkhoffs G, Verhagen E. A novel approach to enhance ACL injury prevention programs. Journal of Experimental Orthopaedics. 2018; 5(1):22. [DOI:10.1186/s40634-018-0137-5][PMID]
  25. McLean SG, Lipfert SW, van den Bogert AJ. Effect of gender and defensive opponent on the biomechanics of sidestep cutting. Medicine and Science in Sports and Exercise. 2004; 36(6):1008-16. [DOI:10.1249/01.MSS.0000128180.51443.83][PMID]
  26. Negahban H, Mazaheri M, Kingma I, van Dieën JH. A systematic review of postural control during single-leg stance in patients with untreated anterior cruciate ligament injury. Knee Surgery, Sports Traumatology, Arthroscopy: Official Journal of the ESSKA. 2014; 22(7):1491-504. [DOI:10.1007/s00167-013-2501-4][PMID]
  27. Borotikar BS, Newcomer R, Koppes R, McLean SG. Combined effects of fatigue and decision making on female lower limb landing postures: Central and peripheral contributions to ACL injury risk. Clinical Biomechanics (Bristol, Avon). 2008; 23(1):81-92. [DOI:10.1016/j.clinbiomech.2007.08.008][PMID]
  28. Fitzgerald GK, Axe MJ, Snyder-Mackler L. Proposed practice guidelines for nonoperative anterior cruciate ligament rehabilitation of physically active individuals. The Journal of Orthopaedic and Sports Physical Therapy. 2000; 30(4):194-203. [DOI:10.2519/jospt.2000.30.4.194][PMID]
  29. Letafatkar A, Rajabi R, Minoonejad H, Rabiei P. Efficacy of perturbation-enhanced neuromuscular training on hamstring and quadriceps onset time, activation and knee flexion during tuck-jump task. International Journal of Sports Physical Therapy. 2019; 14(2):214-27. [PMID]
  30. Mohapatra S, Krishnan V, Aruin AS. Postural control in response to an external perturbation: Effect of altered proprioceptive information. Experimental Brain Research. 2012; 217(2):197-208. [PMID]
  31. Baumeister J, von Detten S, van Niekerk SM, Schubert M, Ageberg E, Louw QA. Brain activity in predictive sensorimotor control for landings: An EEG pilot study. International Journal of Sports Medicine. 2013; 34(12):1106-11. [DOI:10.1055/s-0033-1341437][PMID]
  32. Bazanova OM, Vernon D. Interpreting EEG alpha activity. Neuroscience and Biobehavioral Reviews. 2014; 44:94-110. [DOI:10.1016/j.neubiorev.2013.05.007][PMID]
  33. Klimesch W. α-band oscillations, attention, and controlled access to stored information. Trends in Cognitive Sciences. 2012; 16(12):606-17. [DOI:10.1016/j.tics.2012.10.007][PMID]
  34. Wang H, Kwag JS, Jung MC. Review of EMG indexes for quantifying the total muscle activity. Korean Society of Engineering Conference. 2011; 514-7. [Link]
  35. Pollok B, Latz D, Krause V, Butz M, Schnitzler A. Changes of motor-cortical oscillations associated with motor learning. Neuroscience. 2014; 275:47-53. [DOI:10.1016/j.neuroscience.2014.06.008][PMID]
  36. Gola M, Magnuski M, Szumska I, Wróbel A. EEG beta band activity is related to attention and attentional deficits in the visual performance of elderly subjects. International Journal of Psychophysiology: Official Journal of the International Organization of Psychophysiology. 2013; 89(3):334-41. [DOI:10.1016/j.ijpsycho.2013.05.007][PMID]
  37. Del Percio C, Babiloni C, Marzano N, Iacoboni M, Infarinato F, Vecchio F, et al. "Neural efficiency" of athletes' brain for upright standing: A high-resolution EEG study. Brain Research Bulletin. 2009; 79(3-4):193-200. [DOI:10.1016/j.brainresbull.2009.02.001][PMID]
  38. Gutmann B, Hülsdünker T, Mierau J, Strüder HK, Mierau A. Exercise-induced changes in EEG alpha power depend on frequency band definition mode. Neuroscience Letters. 2018; 662:271-5. [DOI:10.1016/j.neulet.2017.10.033][PMID]
  39. Lee DC, Lim HK, McKay WB, Priebe MM, Holmes SA, Sherwood AM. Toward an objective interpretation of surface EMG patterns: A voluntary response index (VRI). Journal of Electromyography and Kinesiology: Official Journal of the International Society of Electrophysiological Kinesiology. 2004; 14(3):379-88. [DOI:10.1016/j.2003.10.006][PMID]
  40. Norouzi Fashkhami A, Rahimi A, Khademi Kalantari K. The voluntary response index in electromyographic study during landing test of the patients with ACL deficiency: A new study protocol. Iranian Red Crescent Medical Journal. 2014; 16(5):e14119. [DOI:10.5812/ircmj.14119][PMID]
  41. Lim HK, Lee DC, McKay WB, Protas EJ, Holmes SA, Priebe MM, et al. Analysis of sEMG during voluntary movement--Part II: Voluntary response index sensitivity. IEEE Transactions on Neural Systems and Rehabilitation Engineering: A Publication of the IEEE Engineering in Medicine and Biology Society. 2004; 12(4):416-21. [DOI:10.1109/TNSRE.2004.838445][PMID]
  42. McLeod S. What does effect size tell you? [Internet]. SimplyPsychology. 2023 [Updated 2023 July 31]. Available from: [Link]
  43. Rangaswamy M, Porjesz B, Chorlian DB, Wang K, Jones KA, Bauer LO, et al. Beta power in the EEG of alcoholics. Beta power in the EEG of alcoholics. Biological Psychiatry. 2002; 52(8):831-42. [DOI:10.1016/S0006-3223(02)01362-8][PMID]
  44. Chmielewski TL, Hurd WJ, Rudolph KS, Axe MJ, Snyder-Mackler L. Perturbation training improves knee kinematics and reduces muscle co-contraction after complete unilateral anterior cruciate ligament rupture. Physical Therapy. 2005; 85(8):740-9; discussion 750-4. [DOI:10.1093/ptj/85.8.740][PMID]
  45. Fitzgerald GK, Axe MJ, Snyder-Mackler L. The efficacy of perturbation training in nonoperative anterior cruciate ligament rehabilitation programs for physical active individuals. Physical Therapy. 2000; 80(2):128-40. [DOI:10.1093/ptj/80.2.128][PMID]
  46. Gustavsson A, Neeter C, Thomeé P, Silbernagel KG, Augustsson J, Thomeé R, et al. A test battery for evaluating hop performance in patients with an ACL injury and patients who have undergone ACL reconstruction. Knee Surgery, Sports Traumatology, Arthroscopy: Official Journal of the ESSKA. 2006; 14(8):778-88. [DOI:10.1007/s00167-006-0045-6][PMID]
  47. Shabani B, Bytyqi D, Lustig S, Cheze L, Bytyqi C, Neyret P. Gait changes of the ACL-deficient knee 3D kinematic assessment. Knee Surgery, Sports Traumatology, Arthroscopy: Official Journal of the ESSKA. 2015; 23(11):3259-65. [DOI:10.1007/s00167-014-3169-0][PMID]
  48. Hart JM, Ko JW, Konold T, Pietrosimone B. Sagittal plane knee joint moments following anterior cruciate ligament injury and reconstruction: A systematic review. Clinical Biomechanics (Bristol, Avon). 2010; 25(4):277-83. [DOI:10.1016/j.clinbiomech.2010.04.008]
  49. Ward SH, Pearce A, Bennell KL, Pietrosimone B, Bryant AL. Corrigendum to "Quadriceps cortical adaptations in individuals with an anterior cruciate ligament injury" [Knee 23 (2016) 582-587]. The Knee. 2016; 23(6):1172. [DOI:10.1016/j.knee.2016.08.003][PMID]
  50. Schmied A, Forget R, Vedel JP. Motor unit firing pattern, synchrony and coherence in a deafferented patient. Frontiers in Human Neuroscience. 2014; 8:746. [DOI:10.3389/fnhum.2014.00746][PMID]
  51. Ward SH, Perraton L, Bennell K, Pietrosimone B, Bryant AL. Deficits in quadriceps force control after anterior cruciate ligament injury: Potential central mechanisms. Journal of Athletic Training. 2019; 54(5):505-12. [DOI:10.4085/1062-6050-414-17][PMID]
  52. Koga H, Nakamae A, Shima Y, Iwasa J, Myklebust G, Engebretsen L, et al. Mechanisms for noncontact anterior cruciate ligament injuries: Knee joint kinematics in 10 injury situations from female team handball and basketball. The American Journal of Sports Medicine. 2010; 38(11):2218-25. [DOI:10.1177/0363546510373570][PMID]
  53. Baumeister J, Reinecke K, Schubert M, Weiss M. Altered electrocortical brain activity after ACL reconstruction during force control. Journal of Orthopaedic Research: Official Publication of the Orthopaedic Research Society. 2011; 29(9):1383-9. [DOI:10.1002/jor.21380][PMID]
  54. Edwards AE, Guven O, Furman MD, Arshad Q, Bronstein AM. Electroencephalographic correlates of continuous postural tasks of increasing difficulty. Neuroscience. 2018; 395:35-48. [DOI:10.1016/j.neuroscience.2018.10.040][PMID]
  55. Gola M, Kamiński J, Brzezicka A, Wróbel A. β band oscillations as a correlate of alertness--changes in aging. International Journal of Psychophysiology: Official Journal of the International Organization of Psychophysiology. 2012; 85(1):62-7. [DOI:10.1016/j.ijpsycho.2011.09.001][PMID]
  56. Del Percio C, Brancucci A, Bergami F, Marzano N, Fiore A, Di Ciolo E, et al. Cortical alpha rhythms are correlated with body sway during quiet open-eyes standing in athletes: A high-resolution EEG study. NeuroImage. 2007; 36(3):822-9. [DOI:10.1016/j.neuroi2007.02.054][PMID]
The Scientific Journal of Rehabilitation Medicine
Volume 13, Issue 5
November and December 2024
Pages 1002-1021

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History

  • Receive Date: 10 July 2023
  • Revise Date: 18 July 2023
  • Accept Date: 19 July 2023
  • First Publish Date: 19 August 2023

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