Neuromuscular Function of the Knee Joint Following Knee Injuries: Does It Ever Get Back to Normal? A Systematic Review with Meta-Analyses

Beyza Tayfur, Chedsada Charuphongsa, Dylan Morrissey, Stuart Charles Miller, Beyza Tayfur, Chedsada Charuphongsa, Dylan Morrissey, Stuart Charles Miller

Abstract

Background: Neuromuscular deficits are common following knee injuries and may contribute to early-onset post-traumatic osteoarthritis, likely mediated through quadriceps dysfunction.

Objective: To identify how peri-articular neuromuscular function changes over time after knee injury and surgery.

Design: Systematic review with meta-analyses.

Data sources: PubMed, Web of Science, Embase, Scopus, CENTRAL (Trials).

Eligibility criteria for selecting studies: Moderate and high-quality studies comparing neuromuscular function of muscles crossing the knee joint between a knee-injured population (ligamentous, meniscal, osteochondral lesions) and healthy controls. Outcomes included normalized isokinetic strength, muscle size, voluntary activation, cortical and spinal-reflex excitability, and other torque related outcomes.

Results: A total of 46 studies of anterior cruciate ligament (ACL) and five of meniscal injury were included. For ACL injury, strength and voluntary activation deficits were evident (moderate to strong evidence). Cortical excitability was not affected at < 6 months (moderate evidence) but decreased at 24+ months (moderate evidence). Spinal-reflex excitability did not change at < 6 months (moderate evidence) but increased at 24+ months (strong evidence). We also found deficits in torque variability, rate of torque development, and electromechanical delay (very limited to moderate evidence). For meniscus injury, strength deficits were evident only in the short-term. No studies reported gastrocnemius, soleus or popliteus muscle outcomes for either injury. No studies were found for other ligamentous or chondral injuries.

Conclusions: Neuromuscular deficits persist for years post-injury/surgery, though the majority of evidence is from ACL injured populations. Muscle strength deficits are accompanied by neural alterations and changes in control and timing of muscle force, but more studies are needed to fill the evidence gaps we have identified. Better characterisation and therapeutic strategies addressing these deficits could improve rehabilitation outcomes, and potentially prevent PTOA.

Trial registration number: PROSPERO CRD42019141850.

Conflict of interest statement

Beyza Tayfur, Chedsada Charuphongsa, Dylan Morrissey and Stuart Miller declare that they have no conflicts of interest relevant to the content of this review.

Figures

Fig. 1
Fig. 1
Flow diagram of the study selection process
Fig. 2
Fig. 2
Findings and literature gap map for anterior cruciate ligament studies. Colours represent the evidence level as by van Tulder et al. [40] and directions represent injured group data when compared to control, with the effect size. SMD standardised mean difference, ST semitendinosus, BF biceps femoris, Ham:Quad hamstring:quadriceps
Fig. 3
Fig. 3
Findings and literature gap map for meniscus studies. Colours represent the evidence level as by van Tulder et al. [40] and directions represent injured group data when compared to control, with the effect size. SMD standardised mean difference, ST semitendinosus, BF biceps femoris, Ham:Quad hamstring:quadriceps
Fig. 4
Fig. 4
Forest plot of quadriceps active motor threshold from anterior cruciate ligament studies (increased active motor threshold meaning decreased cortical excitability)
Fig. 5
Fig. 5
Forest plot of quadriceps Hoffman reflex (spinal excitability) from anterior cruciate ligament studies
Fig. 6
Fig. 6
Forest plot of quadriceps voluntary activation from anterior cruciate ligament studies
Fig. 7
Fig. 7
Forest plot of quadriceps slow concentric strength from anterior cruciate ligament studies
Fig. 8
Fig. 8
Forest plot of hamstring slow concentric strength from anterior cruciate ligament studies

References

    1. Muthuri SG, McWilliams DF, Doherty M, Zhang W. History of knee injuries and knee osteoarthritis: a meta-analysis of observational studies. Osteoarthr Cartil. 2011;19:1286–1293.
    1. Poulsen E, Goncalves GH, Bricca A, Roos EM, Thorlund JB, Juhl CB. Knee osteoarthritis risk is increased 4–6 fold after knee injury - a systematic review and meta-analysis. Br J Sports Med. 2019;53:1454–1463.
    1. Snoeker B, Turkiewicz A, Magnusson K, Frobell R, Yu D, Peat G, et al. Risk of knee osteoarthritis after different types of knee injuries in young adults: a population-based cohort study. Br J Sport Med. 2020;54:725–730.
    1. Lie MM, Risberg MA, Storheim K, Engebretsen L, Øiestad BE. What’s the rate of knee osteoarthritis 10 years after anterior cruciate ligament injury? An updated systematic review. Br J Sports Med. 2019;53:1162–1167.
    1. Carbone A, Rodeo S. Review of current understanding of post-traumatic osteoarthritis resulting from sports injuries. J Orthop Res. 2017;35:397–405.
    1. Brophy RH, Gray BL, Nunley RM, Barrack RL, Clohisy JC. Total knee arthroplasty after previous knee surgery. J Bone Jt Surg Am. 2014;96:801–805.
    1. Little CB, Hunter DJ. Post-traumatic osteoarthritis: from mouse models to clinical trials. Nat Rev Rheumatol. 2013;9:485–497.
    1. Øiestad BE, Juhl CB, Eitzen I, Thorlund JB. Knee extensor muscle weakness is a risk factor for development of knee osteoarthritis. A systematic review and meta-analysis. Osteoarthr Cartil. 2015;23:171–177.
    1. Lepley AS, Gribble PA, Thomas AC, Tevald MA, Sohn DH, Pietrosimone BG. Quadriceps neural alterations in anterior cruciate ligament reconstructed patients: a 6-month longitudinal investigation. Scand J Med Sci Sports. 2015;25:828–839.
    1. Harkey MS, Luc-Harkey BA, Lepley AS, Grindstaff TL, Gribble P, Blackburn JT, et al. Persistent muscle inhibition after anterior cruciate ligament reconstruction. Med Sci Sport Exerc. 2016;48:2370–2377.
    1. Larsen JB, Farup J, Lind M, Dalgas U. Muscle strength and functional performance is markedly impaired at the recommended time point for sport return after anterior cruciate ligament reconstruction in recreational athletes. Hum Mov Sci. 2015;39:73–87.
    1. Tengman E, Olofsson LB, Stensdotter AK, Nilsson KG, Häger CK, Tengman E. Anterior cruciate ligament injury after more than 20 years. II. Concentric and eccentric knee muscle strength. Scand J Med Sci Sports. 2014;24:e501–509.
    1. Lewek M, Rudolph K, Axe M, Snyder-Mackler L. The effect of insufficient quadriceps strength on gait after anterior cruciate ligament reconstruction. Clin Biomech. 2002;17:56–63.
    1. Hart HF, Culvenor AG, Collins NJ, Ackland DC, Cowan SM, Machotka Z, et al. Knee kinematics and joint moments during gait following anterior cruciate ligament econstruction: a systematic review and meta-analysis. Br J Sports Med. 2016;50:597–612.
    1. Andriacchi TP, Koo S, Scanlan SF. Gait mechanics influence healthy cartilage morphology and osteoarthritis of the knee. J Bone Jt Surg Am. 2009;91:95–101.
    1. Whittaker JL, Roos EM. A pragmatic approach to prevent post-traumatic osteoarthritis after sport or exercise-related joint injury. Best Pract Res Clin Rheumatol. 2019;33:158–171.
    1. Allen KD, Choong PF, Davis AM, Dowsey MM, Dziedzic KS, Emery C, et al. Osteoarthritis: Models for appropriate care across the disease continuum. Best Pract Res Clin Rheumatol. 2016;30:503–535.
    1. Karanikas K, Arampatzis A, Brüggemann GP. Motor task and muscle strength followed different adaptation patterns after anterior cruciate ligament reconstruction. Eur J Phys Rehabil Med. 2009;45:37–45.
    1. Hart JM, Pietrosimone B, Hertel J, Ingersoll CD. Quadriceps activation following knee injuries: a systematic review. J Athl Train. 2010;45:87–97.
    1. Kuenze CM, Hertel J, Weltman A, Diduch D, Saliba SA, Hart JM. Persistent neuromuscular and corticomotor quadriceps asymmetry after anterior cruciate ligament reconstruction. J Athl Train. 2015;50:303–312.
    1. Wieschhoff GG, Mandell JC, Czuczman GJ, Nikac V, Shah N, Smith SE. Acute non-contact anterior cruciate ligament tears are associated with relatively increased vastus medialis to semimembranosus cross-sectional area ratio: a case-control retrospective MR study. Skeletal Radiol. 2017;46:1469–1475.
    1. Pamukoff DN, Pietrosimone BG, Ryan ED, Lee DR, Blackburn JT. Quadriceps function and hamstrings co-activation after anterior cruciate ligament reconstruction. J Athl Train. 2017;52:422–428.
    1. Vairo GL, Myers JB, Sell TC, Fu FH, Harner CD, Lephart SM. Neuromuscular and biomechanical landing performance subsequent to ipsilateral semitendinosus and gracilis autograft anterior cruciate ligament reconstruction. Knee Surg Sport Traumatol Arthrosc. 2008;16:2–14.
    1. Sasaki K, Neptune RR. Individual muscle contributions to the axial knee joint contact force during normal walking. J Biomech. 2010;43:2780–2784.
    1. Petersen W, Taheri P, Forkel P, Zantop T. Return to play following ACL reconstruction: a systematic review about strength deficits. Arch Orthop Trauma Surg. 2014;134:1417–1428.
    1. Lisee C, Lepley AS, Birchmeier T, O’Hagan K, Kuenze C. Quadriceps strength and volitional activation after anterior cruciate ligament reconstruction: a systematic review and meta-analysis. Sport Health. 2019;11:163–179.
    1. Hall M, Juhl CB, Lund H, Thorlund JB. Knee extensor muscle strength in middle-aged and older individuals undergoing arthroscopic partial meniscectomy: a systematic review and meta-analysis. Arthritis Care Res. 2015;67:1289–1296.
    1. Xergia SA, Mcclelland JA, Kvist J, Vasiliadis HS, Georgoulis AD. The influence of graft choice on isokinetic muscle strength 4–24 months after anterior cruciate ligament reconstruction. Knee Surg Sport Traumatol Arthrosc. 2011;5:768–780.
    1. Van Meer BL, Oei EHG, Meuffels DE, Van Arkel ERA, Verhaar JAN, Bierma-Zeinstra SMA, et al. Degenerative changes in the knee 2 years after anterior cruciate ligament rupture and related risk factors: a prospective observational follow-up study. Am J Sports Med. 2016;44:1524–1533.
    1. Mirkov DM, Knezevic OM, Maffiuletti NA, Kadija M, Nedeljkovic A, Jaric S. Contralateral limb deficit after ACL-reconstruction: an analysis of early and late phase of rate of force development. J Sports Sci. 2017;35:435–440.
    1. Hiemstra LA, Webber S, MacDonald PB, Kriellaars DJ. Contralateral limb strength deficits after anterior cruciate ligament reconstruction using a hamstring tendon graft. Clin Biomech. 2007;22:543–550.
    1. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151:264.
    1. Downs SH, Black N. The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J Epidemiol Community Health. 1998;52:377–384.
    1. Deasy M, Leahy E, Semciw AI. Hip strength deficits in people with symptomatic knee osteoarthritis: a systematic review with meta-analysis. J Orthop Sport Phys Ther. 2016;46:629–639.
    1. Munn J, Sullivan SJ, Schneiders AG. Evidence of sensorimotor deficits in functional ankle instability: a systematic review with meta-analysis. J Sci Med Sport. 2010;13:2–12.
    1. Zhang Z, Xu X, Ni H. Small studies may overestimate the effect sizes in critical care meta-analyses: a meta-epidemiological study. Crit Care. 2013;17:R2.
    1. Sterne JA, Egger M, Smith GD. Systematic reviews in health care: Investigating and dealing with publication and other biases in meta-analysis. BMJ. 2001;323:101–105.
    1. Higgins JPT, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–560.
    1. Cohen J. Statistical power analysis for the behavioral sciences. 2. Cambridge: Academic press; 2013.
    1. van Tulder M, Furlan A, Bombardier C, Bouter L, Editorial Board of the Cochrane Collaboration Back Review Group Updated method guidelines for systematic reviews in the Cochrane collaboration back review group. Spine. 2003;28:1290–1299.
    1. de Almeida AM, Santos Silva PR, Pedrinelli A, Hernandez AJ. Aerobic fitness in professional soccer players after anterior cruciate ligament reconstruction. PLoS ONE. 2018;13:e0194432.
    1. Chung KS, Ha JK, Yeom CH, Ra HJ, Lim JW, Kwon MS, et al. Are muscle strength and function of the uninjured lower limb weakened after anterior cruciate ligament injury? Am J Sports Med. 2015;43:3013–3021.
    1. Clagg S, Paterno MV, Hewett TE, Schmitt LC. Performance on the modified star excursion balance test at the time of return to sport following anterior cruciate ligament reconstruction. J Orthop Sports Phys Ther. 2015;45:444–452.
    1. Engelen-van Melick N, van Cingel REH, van Tienen TG, Nijhuis-van der Sanden MWG. Functional performance 2–9 years after ACL reconstruction: cross-sectional comparison between athletes with bone–patellar tendon–bone, semitendinosus/gracilis and healthy controls. Knee Surg Sport Traumatol Arthrosc. 2017;25:1412–1423.
    1. Freddolini M, Battaglioli A, Chiechi F, Placella G, Georgoulis A, Cerulli G, et al. Electromechanical delay of the knee flexor muscles after anterior cruciate ligament reconstruction using semitendinosus tendon. Sport Biomech. 2015;14:384–393.
    1. Garrison JC, Hannon J, Goto S, Giesler L, Bush C, Bothwell JM. Participants at three months post-operative anterior cruciate ligament reconstruction (ACL-R) demonstrate differences in lower extremity energy absorption contribution and quadriceps strength compared to healthy controls. Knee. 2018;25:782–789.
    1. Goetschius J, Hart JM. Knee-extension torque variability and subjective knee function in patients with a history of anterior cruciate ligament reconstruction. J Athl Train. 2016;51:22–27.
    1. Goetschius J, Hertel J, Saliba S, Brockmeier SF, Hart JM. The effects of patellar tendon vibration on quadriceps strength in anterior cruciate ligament reconstructed knees. Phys Ther Sport. 2019;40:71–77.
    1. Hall M, Wrigley TV, Metcalf BR, Hinman RS, Dempsey AR, Mills PM, et al. A longitudinal study of strength and gait after arthroscopic partial meniscectomy. Med Sci Sport Exerc. 2013;45:2036–2043.
    1. Holsgaard-Larsen A, Jensen C, Mortensen NHM, Aagaard P. Concurrent assessments of lower limb loading patterns, mechanical muscle strength and functional performance in ACL-patients — a cross-sectional study. Knee. 2014;21:66–73.
    1. Hsiao S-F, Chou P-H, Hsu H-C, Lue Y-J. Changes of muscle mechanics associated with anterior cruciate ligament deficiency and reconstruction. J Strength Cond Res. 2014;28:390–400.
    1. Hsieh C-J, Indelicato PA, Moser MW, Vandenborne K, Chmielewski TL. Speed, not magnitude, of knee extensor torque production is associated with self-reported knee function early after anterior cruciate ligament reconstruction. Knee Surg Sport Traumatol Arthrosc. 2015;23:3214–3220.
    1. Ilich SS, Dempsey AR, Mills PM, Sturnieks DL, Stachowiak GW, Maguire KF, et al. Physical activity patterns and function 3 months after arthroscopic partial meniscectomy. J Sci Med Sport. 2013;16:195–199.
    1. Johnson AK, Palmieri-Smith RM, Lepley LK. Contribution of neuromuscular factors to quadriceps asymmetry after anterior cruciate ligament reconstruction. J Athl Train. 2018;53:347–354.
    1. Kaminska E, Piontek T, Wiernicka M, Cywinska-Wasilewska G, Lewandowski J, Lochynski D. Differences in isokinetic strength of the knee extensors and flexors in men with isolated and combined cruciate-ligament knee injury. J Sport Rehabil. 2015;24:268–277.
    1. Kellis E, Galanis N, Kofotolis N. Hamstring-to-quadriceps ratio in female athletes with a previous hamstring injury, anterior cruciate ligament reconstruction, and controls. Sports. 2019;7:214.
    1. Kline PW, Burnham J, Yonz M, Johnson D, Ireland ML, Noehren B. Hip external rotation strength predicts hop performance after anterior cruciate ligament reconstruction. Knee Surg Sport Traumatol Arthrosc. 2018;26:1137–1144.
    1. Krishnan C, Williams GN. Factors explaining chronic knee extensor strength deficits after ACL reconstruction. J Orthop Res. 2011;29:633–640.
    1. Kuenze CM, Kelly AR, Jun H-P, Eltoukhy M. Unilateral quadriceps strengthening with disinhibitory cryotherapy and quadriceps symmetry after anterior cruciate ligament reconstruction. J Athl Train. 2017;52:1010–1018.
    1. Kvist J, Karlberg C, Gerdle B, Gillquist J. Anterior tibial translation during different isokinetic quadriceps torque in anterior cruciate ligament deficient and nonimpaired individuals. J Orthop Sport Phys Ther. 2001;31:4–15.
    1. Lepley AS, Ericksen HM, Sohn DH, Pietrosimone BG. Contributions of neural excitability and voluntary activation to quadriceps muscle strength following anterior cruciate ligament reconstruction. Knee. 2014;21:736–742.
    1. Lepley AS, Grooms DR, Burland JP, Davi SM, Kinsella-Shaw JM, Lepley LK. Quadriceps muscle function following anterior cruciate ligament reconstruction: systemic differences in neural and morphological characteristics. Exp Brain Res. 2019;237:1267–1278.
    1. Maeda N, Urabe Y, Tsutsumi S, Fujishita H, Numano S, Takeuchi T, et al. Symmetry tensiomyographic neuromuscular response after chronic anterior cruciate ligament (ACL) reconstruction. Knee Surg Sport Traumatol Arthrosc. 2018;26:411–417.
    1. Norte GE, Hertel J, Saliba SA, Diduch DR, Hart JM. Quadriceps neuromuscular function in patients with anterior cruciate ligament reconstruction with or without knee osteoarthritis: a cross-sectional study. J Athl Train. 2018;53:475–485.
    1. Oeffinger DJ, Shapiro R, Nyland J, Pienkowski D, Caborn DNM. Delayed gastrocnemius muscle response to sudden perturbation in rehabilitated patients with anterior cruciate ligament reconstruction. Knee Surg Sport Traumatol Arthrosc. 2001;9:19–27.
    1. O’Malley E, Richter C, King E, Strike S, Moran K, Franklyn-Miller A, et al. Countermovement jump and isokinetic dynamometry as measures of rehabilitation status after anterior cruciate ligament reconstruction. J Athl Train. 2018;53:687–695.
    1. Pamukoff DN, Montgomery MM, Choe KH, Moffit TJ, Garcia SA, Vakula MN. Bilateral alterations in running mechanics and quadriceps function following unilateral anterior cruciate ligament reconstruction. J Orthop Sports Phys Ther. 2018;48:960–967.
    1. Reed-Jones RJ, Vallis LA. Kinematics and muscular responses to a ramp descent in the ACL deficient knee. Knee. 2008;15:117–124.
    1. Ristanis S, Tsepis E, Giotis D, Stergiou N, Cerulli G, Georgoulis AD. Electromechanical delay of the knee flexor muscles is impaired after harvesting hamstring tendons for anterior cruciate ligament reconstruction. Am J Sports Med. 2009;37:2179–2186.
    1. Roos PE, Button K, van Deursen RWM. Motor control strategies during double leg squat following anterior cruciate ligament rupture and reconstruction: an observational study. J Neuroeng Rehabil. 2014;11:19.
    1. Scheurer SA, Sherman DA, Glaviano NR, Ingersoll CD, Norte GE. Corticomotor function is associated with quadriceps rate of torque development in individuals with ACL surgery. Exp Brain Res. 2020;238:283–294.
    1. Sturnieks DL, Besier TF, Hamer PW, Ackland TR, Mills PM, Stachowiak GW, et al. Knee strength and knee adduction moments following arthroscopic partial meniscectomy. Med Sci Sport Exerc. 2008;40:991–997.
    1. Thomas AC, Lepley LK, Wojtys EM, McLean SG, Palmieri-Smith RM. Effects of neuromuscular fatigue on quadriceps strength and activation and knee biomechanics in individuals post–anterior cruciate ligament reconstruction and healthy adults. J Orthop Sport Phys Ther. 2015;45:1042–1050.
    1. Thorlund JB, Aagaard P, Roos EM. Thigh muscle strength, functional capacity, and self-reported function in patients at high risk of knee osteoarthritis compared with controls. Arthritis Care Res. 2010;62:1244–1251.
    1. Thorlund JB, Aagaard P, Roos EM. Muscle strength and functional performance in patients at high risk of knee osteoarthritis: a follow-up study. Knee Surg Sport Traumatol Arthrosc. 2012;20:1110–1117.
    1. Tourville TW, Jarrell KM, Naud S, Slauterbeck JR, Johnson RJ, Beynnon BD. Relationship between isokinetic strength and tibiofemoral joint space width changes after anterior cruciate ligament reconstruction. Am J Sports Med. 2014;42:302–311.
    1. Tsarouhas A, Giakas G, Malizos KN, Spiropoulos G, Sideris V, Koutedakis Y, et al. Dynamic effect of quadriceps muscle activation on anterior tibial translation after single-bundle and double-bundle anterior cruciate ligament reconstruction. Arthrosc J Arthrosc Relat Surg. 2015;31:1303–1309.
    1. Vairo GL. Knee flexor strength and endurance profiles after ipsilateral hamstring tendons anterior cruciate ligament reconstruction. Arch Phys Med Rehabil. 2014;95:552–561.
    1. Vairo GL, Miller SJ, Sherbondy PS, Sebastianelli WJ, Buckley WE. Standing flexion deficits predict self-reported outcomes in women after ipsilateral hamstring anterior cruciate ligament reconstruction. Arthroscopy. 2013;29:1796–1803.
    1. Ward SH, Perraton L, Bennell K, Pietrosimone B, Bryant AL. Deficits in quadriceps force control after anterior cruciate ligament injury: potential central mechanisms. J Athl Train. 2019;54:505–512.
    1. Welling W, Benjaminse A, Lemmink K, Dingenen B, Gokeler A. Progressive strength training restores quadriceps and hamstring muscle strength within 7 months after ACL reconstruction in amateur male soccer players. Phys Ther Sport. 2019;40:10–18.
    1. Xergia SA, Pappas E, Zampeli F, Georgiou S, Georgoulis AD. Asymmetries in functional hop tests, lower extremity kinematics, and isokinetic strength persist 6 to 9 months following anterior cruciate ligament reconstruction. J Orthop Sports Phys Ther. 2013;43:154–162.
    1. Zarzycki R, Morton SM, Charalambous CC, Marmon A, Snyder-Mackler L. Corticospinal and intracortical excitability differ between athletes early after ACLR and matched controls. J Orthop Res. 2018;36:2941–2948.
    1. Zult T, Gokeler A, van Raay JJAM, Brouwer RW, Zijdewind I, Hortobágyi T. An anterior cruciate ligament injury does not affect the neuromuscular function of the non-injured leg except for dynamic balance and voluntary quadriceps activation. Knee Surg Sport Traumatol Arthrosc. 2017;25:172–183.
    1. Zwolski C, Schmitt LC, Thomas S, Hewett TE, Paterno MV. The utility of limb symmetry indices in return-to-sport assessment in patients with bilateral anterior cruciate ligament reconstruction. Am J Sports Med. 2016;44:2030–2038.
    1. Myer GD, Paterno MV, Ford KR, Quatman CE, Hewett TE. Rehabilitation after anterior cruciate ligament reconstruction: criteria-based progression through the return-to-sport phase. J Orthop Sport Phys Ther. 2006;36:385–402.
    1. van Melick N, van Cingel REH, Brooijmans F, Neeter C, van Tienen T, Hullegie W, et al. Evidence-based clinical practice update: practice guidelines for anterior cruciate ligament rehabilitation based on a systematic review and multidisciplinary consensus. Br J Sports Med. 2016;50:1506–1515.
    1. Adams D, Logerstedt D, Hunter-Giordano A, Axe MJ, Snyder-Mackler L. Current concepts for anterior cruciate ligament reconstruction: a criterion-based rehabilitation progression. J Orthop Sport Phys Ther. 2012;42:601–614.
    1. Hopkins JT, Ingersoll CD. Arthrogenic muscle inhibition: a limiting factor in joint rehabilitation. J Sport Rehabil. 2000;9:135–159.
    1. Sonnery-Cottet B, Saithna A, Quelard B, Daggett M, Borade A, Ouanezar H, et al. Arthrogenic muscle inhibition after ACL reconstruction: a scoping review of the efficacy of interventions. Br J Sports Med. 2019;53:289–298.
    1. Hart JM, Kuenze CM, Diduch DR, Ingersoll CD. Quadriceps muscle function after rehabilitation with cryotherapy in patients with anterior cruciate ligament reconstruction. J Athl Train. 2014;49:733–739.
    1. Lynch AD, Logerstedt DS, Grindem H, Eitzen I, Hicks GE, Axe MJ, et al. Consensus criteria for defining “successful outcome” after ACL injury and reconstruction: a Delaware-Oslo ACL cohort investigation. Br J Sports Med. 2015;49:335–342.
    1. Filbay SR, Grindem H. Evidence-based recommendations for the management of anterior cruciate ligament (ACL) rupture. Best Pract Res Clin Rheumatol. 2019;33:33–47.
    1. Hopkins JT, Ingersoll CD, Andrew Krause B, Edwards JE, Cordova ML. Effect of knee joint effusion on quadriceps and soleus motoneuron pool excitability. Med Sci Sports Exerc. 2001;33:123–126.
    1. Park J, Hopkins JT. Induced anterior knee pain immediately reduces involuntary and voluntary quadriceps activation. Clin J Sport Med. 2013;23:19–24.
    1. Palmieri RM, Tom JA, Edwards JE, Weltman A, Saliba EN, Mistry DJ, et al. Arthrogenic muscle response induced by an experimental knee joint effusion is mediated by pre- and post-synaptic spinal mechanisms. J Electromyogr Kinesiol. 2004;14:631–640.
    1. Hopkins JT, Ingersoll CD, Edwards JE, Cordova ML. Changes in soleus motoneuron pool excitability after artificial knee joint effusion. Arch Phys Med Rehabil. 2000;81:1199–1203.
    1. Groppa S, Oliviero A, Eisen A, Quartarone A, Cohen LG, Mall V, et al. A practical guide to diagnostic transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol. 2012;123:858–882.
    1. Bodkin SG, Norte GE, Hart JM. Corticospinal excitability can discriminate quadriceps strength indicative of knee function after ACL-reconstruction. Scand J Med Sci Sport. 2019;29:716–724.
    1. Alkjaer T, Raffalt PC, Dalsgaard H, Simonsen EB, Petersen NC, Bliddal H, et al. Gait variability and motor control in people with knee osteoarthritis. Gait Posture. 2015;42:479–484.
    1. Pietrosimone BG, McLeod MM, Lepley AS. A theoretical framework for understanding neuromuscular response to lower extremity joint injury. Sport Health. 2012;4:31–35.
    1. Relph N, Herrington L, Tyson S. The effects of ACL injury on knee proprioception: a meta-analysis. Physiotherapy. 2014;100:187–195.
    1. Luc B, Gribble PA, Pietrosimone BG. Osteoarthritis prevalence following anterior cruciate ligament reconstruction: a systematic review and numbers-needed-to-treat analysis. J Athl Train. 2014;49:806–819.
    1. Risberg MA, Oiestad BE, Gunderson R, Aune AK, Engebretsen L, Culvenor A, et al. Changes in knee osteoarthritis, symptoms, and function after anterior cruciate ligament reconstruction. Am J Sports Med. 2015;44:1215–1224.
    1. Lepley LK, Wojtys EM, Palmieri-Smith RM. Does concomitant meniscectomy or meniscal repair affect the recovery of quadriceps function post-ACL reconstruction? Knee Surg Sport Traumatol Arthrosc. 2015;23:2756–2761.
    1. Aagaard P, Simonsen EB, Andersen JL, Magnusson P, Dyhre-Poulsen P. Increased rate of force development and neural drive of human skeletal muscle following resistance training. J Appl Physiol. 2002;93:1318–1326.
    1. Angelozzi M, Madama M, Corsica C, Calvisi V, Properzi G, McCaw ST, et al. Rate of force development as an adjunctive outcome measure for return-to-sport decisions after anterior cruciate ligament reconstruction. J Orthop Sport Phys Ther. 2012;42:772–780.
    1. Andersen LL, Aagaard P. Influence of maximal muscle strength and intrinsic muscle contractile properties on contractile rate of force development. Eur J Appl Physiol. 2006;96:46–52.
    1. Kaneko F, Onari K, Kawaguchi K, Tsukisaka K, Roy SH. Electromechanical delay after ACL reconstruction: an innovative method for investigating central and peripheral contributions. J Orthop Sport Phys Ther. 2002;32:158–165.
    1. Pääsuke M, Ereline J, Gapeyeva H. Knee extension strength and vertical jumping performance in nordic combined athletes. J Sports Med Phys Fit. 2001;41:354–361.
    1. Andriacchi TP, Favre J. The nature of in vivo mechanical signals that influence cartilage health and progression to knee osteoarthritis. Curr Rheumatol Rep. 2014;16:463.
    1. Hortobágyi T, Garry J, Holbert D, Devita P. Aberrations in the control of quadriceps muscle force in patients with knee osteoarthritis. Arthritis Care Res. 2004;51:562–569.
    1. Williams GN, Buchanan TS, Barrance PJ, Axe MJ, Snyder-Mackler L. Quadriceps weakness, atrophy, and activation failure in predicted noncopers after anterior cruciate ligament injury. Am J Sports Med. 2005;33:402–407.
    1. Thomas AC, Wojtys EM, Brandon C, Palmieri-Smith RM. Muscle atrophy contributes to quadriceps weakness after anterior cruciate ligament reconstruction. J Sci Med Sport. 2016;19:7–11.
    1. Kambhampati SBS, Vaishya R. Trends in publications on the anterior cruciate ligament over the past 40 years on PubMed. Orthop J Sport Med. 2019;7:2325967119856883.
    1. Smeets A, Malfait B, Dingenen B, Robinson MA, Vanrenterghem J, Peers K, et al. Is knee neuromuscular activity related to anterior cruciate ligament injury risk? A pilot study. Knee. 2019;26:40–51.
    1. Kobayashi H, Koyama Y, Enoka RM, Suzuki S. A unique form of light-load training improves steadiness and performance on some functional tasks in older adults. Scand J Med Sci Sports. 2014;24:98–110.
    1. Gruber M, Gollhofer A. Impact of sensorimotor training on the rate of force development and neural activation. Eur J Appl Physiol. 2004;92:98–105.

Source: PubMed

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