Skip to main content
Top
Published in: Knee Surgery, Sports Traumatology, Arthroscopy 2/2019

01-02-2019 | KNEE

Muscle hypotrophy, not inhibition, is responsible for quadriceps weakness during rehabilitation after anterior cruciate ligament reconstruction

Authors: Takumi Fukunaga, Christopher D. Johnson, Stephen J. Nicholas, Malachy P. McHugh

Published in: Knee Surgery, Sports Traumatology, Arthroscopy | Issue 2/2019

Login to get access

Abstract

Purpose

Quadriceps weakness is common after anterior cruciate ligament reconstruction (ACLR). Limited neuromuscular activation may have a role in the weakness. The purpose of this study was to use peripheral magnetic stimulation to measure changes in quadriceps inhibition in patients during rehabilitation from ACLR.

Methods

Ten patients (7M/3F; age 35 ± 8 years; BMI 26.0 ± 4.8 kg/m2) who had ACLR with patellar tendon autograft were recruited. At 3 and 6 months postoperatively, patients’ knee extension peak torque was measured during maximum voluntary isometric contraction (MVIC), magnetic stimulation-evoked contraction, and MVIC augmented with superimposed burst magnetic stimulation to the femoral nerve. All tests were done bilaterally at 30° and 65° of knee flexion on a dynamometer. Central activation ratio was calculated by dividing the peak torque before stimulation by peak torque after stimulation.

Results

Patients had marked deficits in MVIC, with improvement from 3 to 6 months that was more apparent at 65° versus 30° (P < 0.05). There was significant deficit in stimulation-evoked torque on the involved side that diminished over time, and this change occurred differently between the two angles (P < 0.05). Central activation ratio was lower on the involved side versus the noninvolved side and this effect was more prominent at 3 versus 6 months: combining the angles, mean central activation ratio on the involved and noninvolved sides, respectively, was 91.4 ± 7.6% and 97.5 ± 5.3% at 3 months, and 93.0 ± 7.8% and 95.8 ± 6.8% at 6 months.

Conclusions

At 3 and 6 months after ACLR, there were significant deficits in quadriceps strength and activation. Quadriceps activation levels were high (> 90%) for both sides at both time points. The substantial strength deficits at this postoperative period may be largely due to muscle atrophy with limited contribution from central inhibition. Rehabilitation interventions to normalize quadriceps strength should emphasize hypertrophic stimuli as opposed to neuromuscular activation strategies.

Level of evidence

II, prospective cohort study.
Literature
1.
go back to reference Ardern CL, Taylor NF, Feller JA, Whitehead TS, Webster KE (2015) Sports participation 2 years after anterior cruciate ligament reconstruction in athletes who had not returned to sport at 1 year: a prospective follow-up of physical function and psychological factors in 122 athletes. Am J Sports Med 43:848–856CrossRefPubMed Ardern CL, Taylor NF, Feller JA, Whitehead TS, Webster KE (2015) Sports participation 2 years after anterior cruciate ligament reconstruction in athletes who had not returned to sport at 1 year: a prospective follow-up of physical function and psychological factors in 122 athletes. Am J Sports Med 43:848–856CrossRefPubMed
2.
go back to reference Czuppon S, Racette BA, Klein SE, Harris-Hayes M (2014) Variables associated with return to sport following anterior cruciate ligament reconstruction: a systematic review. Br J Sports Med 48:356–364CrossRefPubMed Czuppon S, Racette BA, Klein SE, Harris-Hayes M (2014) Variables associated with return to sport following anterior cruciate ligament reconstruction: a systematic review. Br J Sports Med 48:356–364CrossRefPubMed
3.
go back to reference Gerber JP, Marcus RL, Dibble LE, Greis PE, Burks RT, LaStayo PC (2009) Effects of early progressive eccentric exercise on muscle size and function after anterior cruciate ligament reconstruction: a 1-year follow-up study of a randomized clinical trial. Phys Ther 89:51–59CrossRefPubMed Gerber JP, Marcus RL, Dibble LE, Greis PE, Burks RT, LaStayo PC (2009) Effects of early progressive eccentric exercise on muscle size and function after anterior cruciate ligament reconstruction: a 1-year follow-up study of a randomized clinical trial. Phys Ther 89:51–59CrossRefPubMed
4.
go back to reference Gerber JP, Marcus RL, Dibble LE, Greis PE, Burks RT, LaStayo PC (2007) Effects of early progressive eccentric exercise on muscle structure after anterior cruciate ligament reconstruction. J Bone Jt Surg Am 89:559–570CrossRef Gerber JP, Marcus RL, Dibble LE, Greis PE, Burks RT, LaStayo PC (2007) Effects of early progressive eccentric exercise on muscle structure after anterior cruciate ligament reconstruction. J Bone Jt Surg Am 89:559–570CrossRef
5.
go back to reference Glace BW, Kremenic IJ, McHugh MP (2013) Sex differences in central and peripheral mechanisms of fatigue in cyclists. Eur J Appl Physiol 113:1091–1098CrossRefPubMed Glace BW, Kremenic IJ, McHugh MP (2013) Sex differences in central and peripheral mechanisms of fatigue in cyclists. Eur J Appl Physiol 113:1091–1098CrossRefPubMed
6.
7.
go back to reference Keays SL, Bullock-Saxton JE, Keays AC, Newcombe PA, Bullock MI (2007) A 6-year follow-up of the effect of graft site on strength, stability, range of motion, function, and joint degeneration after anterior cruciate ligament reconstruction: patellar tendon versus semitendinosus and gracilis tendon graft. Am J Sports Med 35:729–739CrossRefPubMed Keays SL, Bullock-Saxton JE, Keays AC, Newcombe PA, Bullock MI (2007) A 6-year follow-up of the effect of graft site on strength, stability, range of motion, function, and joint degeneration after anterior cruciate ligament reconstruction: patellar tendon versus semitendinosus and gracilis tendon graft. Am J Sports Med 35:729–739CrossRefPubMed
8.
go back to reference Konishi Y, Ikeda K, Nishino A, Sunaga M, Aihara Y, Fukubayashi T (2007) Relationship between quadriceps femoris muscle volume and muscle torque after anterior cruciate ligament repair. Scand J Med Sci Sports 17:656–661CrossRefPubMed Konishi Y, Ikeda K, Nishino A, Sunaga M, Aihara Y, Fukubayashi T (2007) Relationship between quadriceps femoris muscle volume and muscle torque after anterior cruciate ligament repair. Scand J Med Sci Sports 17:656–661CrossRefPubMed
9.
go back to reference Kremenic IJ, Ben-Avi SS, Leonhardt D, McHugh MP (2004) Transcutaneous magnetic stimulation of the quadriceps via the femoral nerve. Muscle Nerve 30:379–381CrossRefPubMed Kremenic IJ, Ben-Avi SS, Leonhardt D, McHugh MP (2004) Transcutaneous magnetic stimulation of the quadriceps via the femoral nerve. Muscle Nerve 30:379–381CrossRefPubMed
10.
go back to reference Kremenic IJ, Glace BW, Ben-Avi SS, Nicholas SJ, McHugh MP (2009) Central fatigue after cycling evaluated using peripheral magnetic stimulation. Med Sci Sports Exerc 41:1461–1466CrossRefPubMed Kremenic IJ, Glace BW, Ben-Avi SS, Nicholas SJ, McHugh MP (2009) Central fatigue after cycling evaluated using peripheral magnetic stimulation. Med Sci Sports Exerc 41:1461–1466CrossRefPubMed
11.
go back to reference Krishnan C, Theuerkauf P (2015) Effect of knee angle on quadriceps strength and activation after anterior cruciate ligament reconstruction. J Appl Physiol 119:223–231CrossRefPubMedPubMedCentral Krishnan C, Theuerkauf P (2015) Effect of knee angle on quadriceps strength and activation after anterior cruciate ligament reconstruction. J Appl Physiol 119:223–231CrossRefPubMedPubMedCentral
12.
13.
go back to reference Kuenze C, Hertel J, Saliba S, Diduch DR, Weltman A, Hart JM (2015) Clinical thresholds for quadriceps assessment after anterior cruciate ligament reconstruction. J Sport Rehabil 24:36–46CrossRefPubMed Kuenze C, Hertel J, Saliba S, Diduch DR, Weltman A, Hart JM (2015) Clinical thresholds for quadriceps assessment after anterior cruciate ligament reconstruction. J Sport Rehabil 24:36–46CrossRefPubMed
14.
go back to reference Kuenze CM, Blemker SS, Hart JM (2016) Quadriceps function relates to muscle size following ACL reconstruction. J Orthop Res 34:1656–1662CrossRefPubMed Kuenze CM, Blemker SS, Hart JM (2016) Quadriceps function relates to muscle size following ACL reconstruction. J Orthop Res 34:1656–1662CrossRefPubMed
15.
go back to reference Kuenze CM, Hertel J, Weltman A, Diduch D, Saliba SA, Hart JM (2015) Persistent neuromuscular and corticomotor quadriceps asymmetry after anterior cruciate ligament reconstruction. J Athl Train 50:303–312CrossRefPubMedPubMedCentral Kuenze CM, Hertel J, Weltman A, Diduch D, Saliba SA, Hart JM (2015) Persistent neuromuscular and corticomotor quadriceps asymmetry after anterior cruciate ligament reconstruction. J Athl Train 50:303–312CrossRefPubMedPubMedCentral
16.
go back to reference Lautamies R, Harilainen A, Kettunen J, Sandelin J, Kujala UM (2008) Isokinetic quadriceps and hamstring muscle strength and knee function 5 years after anterior cruciate ligament reconstruction: comparison between bone-patellar tendon-bone and hamstring tendon autografts. Knee Surg Sports Traumatol Arthrosc 16:1009–1016CrossRefPubMed Lautamies R, Harilainen A, Kettunen J, Sandelin J, Kujala UM (2008) Isokinetic quadriceps and hamstring muscle strength and knee function 5 years after anterior cruciate ligament reconstruction: comparison between bone-patellar tendon-bone and hamstring tendon autografts. Knee Surg Sports Traumatol Arthrosc 16:1009–1016CrossRefPubMed
17.
go back to reference Lepley AS, Gribble PA, Thomas AC, Tevald MA, Sohn DH, Pietrosimone BG (2015) Quadriceps neural alterations in anterior cruciate ligament reconstructed patients: a 6-month longitudinal investigation. Scand J Med Sci Sports 25:828–839CrossRefPubMed Lepley AS, Gribble PA, Thomas AC, Tevald MA, Sohn DH, Pietrosimone BG (2015) Quadriceps neural alterations in anterior cruciate ligament reconstructed patients: a 6-month longitudinal investigation. Scand J Med Sci Sports 25:828–839CrossRefPubMed
18.
go back to reference Man WD, Moxham J, Polkey MI (2004) Magnetic stimulation for the measurement of respiratory and skeletal muscle function. Eur Respir J 24:846–860CrossRefPubMed Man WD, Moxham J, Polkey MI (2004) Magnetic stimulation for the measurement of respiratory and skeletal muscle function. Eur Respir J 24:846–860CrossRefPubMed
19.
go back to reference McHugh MP, Tyler TF, Browne MG, Gleim GW, Nicholas SJ (2002) Electromyographic predictors of residual quadriceps muscle weakness after anterior cruciate ligament reconstruction. Am J Sports Med 30:334–339CrossRefPubMed McHugh MP, Tyler TF, Browne MG, Gleim GW, Nicholas SJ (2002) Electromyographic predictors of residual quadriceps muscle weakness after anterior cruciate ligament reconstruction. Am J Sports Med 30:334–339CrossRefPubMed
20.
go back to reference Palmieri-Smith RM, Thomas AC, Wojtys EM (2008) Maximizing quadriceps strength after ACL reconstruction. Clin Sports Med 27:405–424CrossRefPubMed Palmieri-Smith RM, Thomas AC, Wojtys EM (2008) Maximizing quadriceps strength after ACL reconstruction. Clin Sports Med 27:405–424CrossRefPubMed
21.
go back to reference Paterno MV, Schmitt LC, Ford KR, Rauh MJ, Myer GD, Huang B et al (2010) Biomechanical measures during landing and postural stability predict second anterior cruciate ligament injury after anterior cruciate ligament reconstruction and return to sport. Am J Sports Med 38:1968–1978CrossRefPubMedPubMedCentral Paterno MV, Schmitt LC, Ford KR, Rauh MJ, Myer GD, Huang B et al (2010) Biomechanical measures during landing and postural stability predict second anterior cruciate ligament injury after anterior cruciate ligament reconstruction and return to sport. Am J Sports Med 38:1968–1978CrossRefPubMedPubMedCentral
22.
go back to reference Pietrosimone B, Lepley AS, Harkey MS, Luc-Harkey BA, Blackburn JT, Gribble PA et al (2016) Quadriceps Strength Predicts Self-reported Function Post-ACL Reconstruction. Med Sci Sports Exerc 48:1671–1677CrossRefPubMed Pietrosimone B, Lepley AS, Harkey MS, Luc-Harkey BA, Blackburn JT, Gribble PA et al (2016) Quadriceps Strength Predicts Self-reported Function Post-ACL Reconstruction. Med Sci Sports Exerc 48:1671–1677CrossRefPubMed
23.
go back to reference Pincivero DM, Salfetnikov Y, Campy RM, Coelho AJ (2004) Angle- and gender-specific quadriceps femoris muscle recruitment and knee extensor torque. J Biomech 37:1689–1697CrossRefPubMed Pincivero DM, Salfetnikov Y, Campy RM, Coelho AJ (2004) Angle- and gender-specific quadriceps femoris muscle recruitment and knee extensor torque. J Biomech 37:1689–1697CrossRefPubMed
24.
go back to reference Polkey MI, Kyroussis D, Hamnegard CH, Mills GH, Green M, Moxham J (1996) Quadriceps strength and fatigue assessed by magnetic stimulation of the femoral nerve in man. Muscle Nerve 19:549–555CrossRefPubMed Polkey MI, Kyroussis D, Hamnegard CH, Mills GH, Green M, Moxham J (1996) Quadriceps strength and fatigue assessed by magnetic stimulation of the femoral nerve in man. Muscle Nerve 19:549–555CrossRefPubMed
25.
go back to reference Snyder-Mackler L, De Luca PF, Williams PR, Eastlack ME, Bartolozzi AR 3rd (1994) Reflex inhibition of the quadriceps femoris muscle after injury or reconstruction of the anterior cruciate ligament. J Bone Jt Surg Am 76:555–560CrossRef Snyder-Mackler L, De Luca PF, Williams PR, Eastlack ME, Bartolozzi AR 3rd (1994) Reflex inhibition of the quadriceps femoris muscle after injury or reconstruction of the anterior cruciate ligament. J Bone Jt Surg Am 76:555–560CrossRef
26.
go back to reference Snyder-Mackler L, Delitto A, Bailey SL, Stralka SW (1995) Strength of the quadriceps femoris muscle and functional recovery after reconstruction of the anterior cruciate ligament. A prospective, randomized clinical trial of electrical stimulation. J Bone Jt Surg Am 77:1166–1173CrossRef Snyder-Mackler L, Delitto A, Bailey SL, Stralka SW (1995) Strength of the quadriceps femoris muscle and functional recovery after reconstruction of the anterior cruciate ligament. A prospective, randomized clinical trial of electrical stimulation. J Bone Jt Surg Am 77:1166–1173CrossRef
27.
go back to reference Tourville TW, Jarrell KM, Naud S, Slauterbeck JR, Johnson RJ, Beynnon BD (2014) Relationship between isokinetic strength and tibiofemoral joint space width changes after anterior cruciate ligament reconstruction. Am J Sports Med 42:302–311CrossRefPubMed Tourville TW, Jarrell KM, Naud S, Slauterbeck JR, Johnson RJ, Beynnon BD (2014) Relationship between isokinetic strength and tibiofemoral joint space width changes after anterior cruciate ligament reconstruction. Am J Sports Med 42:302–311CrossRefPubMed
28.
go back to reference Urbach D, Nebelung W, Becker R, Awiszus F (2001) Effects of reconstruction of the anterior cruciate ligament on voluntary activation of quadriceps femoris a prospective twitch interpolation study. J Bone Jt Surg Br 83:1104–1110CrossRef Urbach D, Nebelung W, Becker R, Awiszus F (2001) Effects of reconstruction of the anterior cruciate ligament on voluntary activation of quadriceps femoris a prospective twitch interpolation study. J Bone Jt Surg Br 83:1104–1110CrossRef
29.
go back to reference Yasuda N, Glover EI, Phillips SM, Isfort RJ, Tarnopolsky MA (2005) Sex-based differences in skeletal muscle function and morphology with short-term limb immobilization. J Appl Physiol 99:1085–1092CrossRefPubMed Yasuda N, Glover EI, Phillips SM, Isfort RJ, Tarnopolsky MA (2005) Sex-based differences in skeletal muscle function and morphology with short-term limb immobilization. J Appl Physiol 99:1085–1092CrossRefPubMed
Metadata
Title
Muscle hypotrophy, not inhibition, is responsible for quadriceps weakness during rehabilitation after anterior cruciate ligament reconstruction
Authors
Takumi Fukunaga
Christopher D. Johnson
Stephen J. Nicholas
Malachy P. McHugh
Publication date
01-02-2019
Publisher
Springer Berlin Heidelberg
Published in
Knee Surgery, Sports Traumatology, Arthroscopy / Issue 2/2019
Print ISSN: 0942-2056
Electronic ISSN: 1433-7347
DOI
https://doi.org/10.1007/s00167-018-5166-1

Other articles of this Issue 2/2019

Knee Surgery, Sports Traumatology, Arthroscopy 2/2019 Go to the issue