The Immediate Effects of Transcranial Direct Current Stimulation on Quadriceps Muscle Function in Individuals With a History of Anterior Cruciate Ligament Reconstruction: A Preliminary Investigation

in Journal of Sport Rehabilitation

Context: Altered quadriceps activation is common following anterior cruciate ligament reconstruction (ACLR), and can persist for years after surgery. These neural deficits are due, in part, to chronic central nervous system alterations. Transcranial direct current stimulation (tDCS) is a noninvasive modality, that is, believed to immediately increase motor neuron activity by stimulating the primary motor cortex, making it a promising modality to use improve outcomes in the ACLR population. Objective: To determine if a single treatment of tDCS would result in increased quadriceps activity and decreased levels of self-reported pain and dysfunction during exercise. Design: Randomized crossover design. Setting: Controlled laboratory. Patients: Ten participants with a history of ACLR (5 males/5 females, 22.9 [4.23] y, 176.57 [12.01] cm, 80.87 [16.86] kg, 68.1 [39.37] mo since ACLR). Interventions: Active tDCS and Sham tDCS. Main Outcome Measures: Percentage of maximum electromyographic data of vastus medialis and lateralis, voluntary isometric strength, percentage of voluntary activation, and self-reported pain and symptom scores were measured. The 2 × 2 repeated-measures analysis of variance by limb were performed to explain the differences between time points (pre and post) and condition (tDCS and sham). Results: There was a significant time main effect for quadriceps percentage of maximum electromyographic of vastus medialis (F9,1 = 11.931, P = .01) and vastus lateralis (F9,1 = 9.132, P = .01), isometric strength (F9,1 = 5.343, P = .046), and subjective scores for pain (F9,1 = 15.499, P = .04) and symptoms (F9,1 = 15.499, P = .04). Quadriceps percentage of maximum electromyographic, isometric strength, and voluntary activation showed an immediate decline from pre to post regardless of tDCS condition. Subjective scores improved slightly after each condition. Conclusions: One session of active tDCS did not have an immediate effect on quadriceps activity and subjective scores of pain and symptoms. To determine if tDCS is a valid modality for this patient population, a larger scale investigation with multiple treatments of active tDCS is warranted.

Approximately 80,000 to 250,000 anterior cruciate ligament (ACL) injuries occur annually in the United States.1 Unfortunately, a portion of these patients can experience poor long-term outcomes following ACL reconstruction (ACLR) which is evident by reinjury rates that exceed 20%,2 and posttraumatic osteoarthritis development that occurs in an estimated 50% of patients within 15 years following surgery.36 Although many factors influence long-term sequalae, quadriceps muscle weakness, which is ubiquitous following injury, has been attributed as a major limiting factor restoration of clinical function.79 Specifically, quadriceps weakness has been linked to greater deficits in self-reported and biomechanical function, as well as higher risk of reinjury and osteoarthritis development.3,1012 Although ACLR rehabilitation programs already largely focus on restoring quadriceps strength,7,9 recent reviews have demonstrated that strength deficits can exceed 20% of the contralateral limb even after formalized rehabilitation has finished.7 Identifying innovative and evidence-based techniques to restore quadriceps muscle function is imperative to improving long-term outcomes in these patients.

Alterations in the excitability of peripheral and central nervous system pathways are hypothesized to contribute to quadriceps dysfunction following ACLR.13 Pain, swelling, and loss of mechanoreception from the joint can lead to altered afferent signals and poor somatosensation, which can negatively impair motor control.8,10,1420 Evidence supporting this hypothesis stems from alterations that have been discovered in corticospinal excitability and brain activation following ACLR highlighted by an inefficiency to generate and transmit action potentials from the motor cortex to the quadriceps muscle.8 Importantly, the excitability of the motor cortex is not only affected early in the injury process, but also can persist for years following ACLR, likely contributing to prolonged deficits in muscle strength and neuromuscular function in these patients.8,21 The reorganization of the corticospinal pathway can have implications on the downstream recruitment of alpha-motor neurons from the motor cortex, resulting in decreased voluntary muscle activation and strength.13,20,21

During traditional ACLR rehabilitation, underlying corticospinal alterations that influence muscle strength is left unaddressed, which limits the effectiveness of the exercises performed.15,22 Transcranial direct current stimulation (tDCS) is a noninvasive method of electrically stimulating segments of the brain to help increase cortical activity and excitability.23 Although tDCS has historically been used in the rehabilitation field to treat neurologically impaired patients (eg, stroke, Parkinson disease, etc), it has recently shown promise in improving muscle strength and decreasing pain and opioid use in individuals with musculoskeletal conditions such as osteoarthritis and total knee arthroplasty.24,25 Theoretically, excitability of the areas directly below the electrodes can be manipulated, which may potentially increase neural activity to the peripheral muscle being used. As mentioned above, patients with ACLR exhibit deficits in excitability of the motor cortex, therefore, the patients with ACLR may benefit from an increase in corticospinal activation during exercise via tDCS, as well as potential reductions in pain, allowing for greater levels of peripheral muscle activation to be used and thus optimizing the benefits from the exercises being performed.25,26

Therefore, the purpose of this study was to determine if a single treatment of tDCS would improve quadriceps muscle activity and reduce self-reported levels of pain and dysfunction during exercise in participants with a history of ACLR. We hypothesized that tDCS would improve quadriceps muscle activity and reduce pain in participants with a history of ACLR.

Methods

Design

A randomized crossover design was used to assess quadriceps muscle activity (electromyographic [EMG] activity, isometric strength, and voluntary activation) and self-reported levels of pain and function (Knee Injury and Osteoarthritis Outcome Scores for Pain and Symptoms) before and after 1 treatment of tDCS or a sham condition. We evaluated the participants’ reconstructed limb during each testing session.

Patients and Participants

This study consisted of 10 participants (5 males/5 females, 22.9 [4.23] y, 176.57 [12.01] cm, 80.87 [16.86] kg, 68.1 [39.37] mo since ACLR; Table 1). To be included, participants reported history of a unilateral ACLR and were a minimum of 6-month postreconstruction with full clearance for return to activity/sport by their physician. Participants were excluded from the study if the participant had experienced any of the following: a knee surgery prior to the ACLR; lower-extremity injury within the last 6 months other than the current ACLR; concomitant meniscal damage; heart condition; history of stroke, cranial neurosurgery, migraines, cancer in the brain, or a psychiatric or neurological disorder; taking medications that alter neural activity; intracranial metal clips; cochlear implants or other electronic devices implanted; a current pregnancy; known balance disorder or vertigo; any active skin infections; or an allergy to adhesive tape. All participants provided written, informed consent prior to enrollment. The Institutional Review Board at the University of Connecticut, Storrs approved all procedures.

Table 1

Demographics

ParticipantAge, yHeight, cmMass, kgMonths post-opSexGraft (PT and HS)
Participant 126180.3477.1164FemalePT
Participant 219172.7277.1179FemalePT
Participant 321170.6859.8728MalePT
Participant 419177.883.9111MalePT
Participant 519182.8898.8838MaleHS
Participant 626175.2579.3766MalePT
Participant 720203.20106.5961MalePT
Participant 823180.3398.8877MaleHS
Participant 924160.0254.43111FemaleHS
Participant 103272.5772.57146FemaleHS
Averages22.980.8780.8768.15 males/5 females6 PT/4 HS
SD4.2316.8616.8639.37

Abbreviations: HS, Hamstring; PT, patellar tendon.

Procedures

This crossover study consisted of a familiarization session and 2 separate test sessions. During the familiarization session, participants were positioned on an isokinetic dynamometer (Biodex System 4; Biodex Medical Systems, Shirley, NY) in the same position as they would be during the testing session, as explained below. Participants were also able to wear and become familiar with tDCS stimulation unit (Halo Sport; Halo Neuroscience, San Francisco, CA).

The 2 subsequent test sessions randomly consisted of an active tDCS stimulation session and a sham session with no stimulation during the walking period. The order of testing was as follows: a baseline assessment, the treatment condition (active tDCS or sham), and an immediate posttest assessment.

Quadriceps Strength Testing and Volitional Activation

Isometric strength was assessed using an isokinetic dynamometer by collecting the participant’s maximal voluntary force of the quadriceps muscles. Participants were instructed to sit on the dynamometer and were positioned in 90° of trunk flexion and 90° of knee flexion (Figure 1A). Restrictive straps were secured at the lap and over the shoulder of each participant to control accessory movement during the knee extension task. The tibia, just proximal to the ankle joint, was secured to a pad on the arm of the dynamometer with Velcro straps. Participants were instructed to cross their arms over the chest during all contractions to avoid unwanted upper-extremity involvement in the task. Once correctly positioned on the dynamometer, the participants were asked to perform a series of submaximal warm-up isometric quadriceps contractions in which they were attempting to extend their knee at 25%, 50%, and 75% of their perceived maximal effort. In addition, participants received submaximal electrical stimulation at 25%, 50%, and 75% of the maximal 150 volts (100 ms train of 10 stimuli, at 100 pps, with a pulse duration of 0.6 ms, and a 0.01 ms pulse delay via the Grass S48 dual channel electrical stimulation unit with an SIU8T isolation unit attached [Grass Products; Natus Neurology, Warwick, RI]). Participants then practiced maximal contractions (without electrical stimulation) until the investigator and participant were confident that a maximal effort was being put forth. Participants then performed 3 maximal voluntary isometric contractions (MVICs) with visual feedback and verbal encouragement with at least 60 seconds between trials, in which the average of the 3 MVIC trials were normalized to body mass (N·m/kg) and used to quantify muscle strength. When each participant reached a plateau in torque output, the supramaximal electrical stimulation was triggered, which contracted any muscle not voluntarily contracted by the participant.

Figure 1
Figure 1

(A) Positioning for MVIC testing. (B) CAR testing. Visual representation of the SIB technique to determine the voluntary activation of the quadriceps, including the equation to find the percentage of quadriceps activation. The MVIC was divided by the torque produced with the SIB. CAR indicates central activation ratio; MVIC, maximal voluntary isometric contraction; SIB, superimposed burst.

Citation: Journal of Sport Rehabilitation 2020; 10.1123/jsr.2019-0179

The central activation ratio (CAR) was used to quantify the amount of quadriceps activation failure. To determine the CAR, the participant’s peak torque generated immediately prior to the delivery of the electrical stimulus was divided by the peak torque generated as a result of the electrical stimulus (superimposed burst torque; Figure 1B). The average of the 3 trials was used for analysis.

Electromyographic Testing

During all muscle strength testing, EMG signals were also collected. The bellies of the distal vastus medialis (VM) and lateralis (VL) were shaved and cleaned with isopropyl alcohol prior to attaching the electrodes (dual EMG electrodes [4 cm × 2.2 cm] and desktop DTS; Noraxon Inc, Scottsdale, AZ; Figure 2). EMG signals were band-passed filtered 10 to 1000 Hz and subsequently processed using a root-mean-square algorithm with a 50-ms moving window. Dynamic EMG collected during the contractions was normalized to the peak muscle activity that occurred during the testing session (%EMGmax).

Figure 2
Figure 2

Electromyography sensor and stimulation pad placement.

Citation: Journal of Sport Rehabilitation 2020; 10.1123/jsr.2019-0179

Self-Reported Questionnaires

At both the baseline and posttesting time points for each session, the participants were asked to complete questionnaires pertaining to their knee pain, knee function, and overall activity. The Knee Injury Osteoarthritis Outcome Score (KOOS) was used to assess self-reported knee function. The KOOS allows for investigation into 5 subscales of self-reported function: pain, disease-specific symptoms, activities of daily living, sport and recreation function, and knee-related quality of life. For this investigation, we focused on pain (KOOS Pn) and disease-specific symptom scores (KOOS Sx).

Transcranial Direct Current Stimulation

The device tested was designed as a headset similar to noise canceling headphones with primer attachments to fit along the headset (Halo Sport tDCS; Halo Neuroscience; Figure 3). The participants were familiarized with the tDCS unit prior to their first testing session. In accordance with manufacture instructions, prior to the application of tDCS, the investigator thoroughly wet the primers prior to connecting them to the headset. The participants were instructed to place the headset directly over the motor cortex area as directed by the investigator, which was estimated using anatomical landmarks of straight lines vertically in the sagittal (using nose and occiput) and frontal (using tragus to tragus) planes. The investigator controlled the headset with the software application, which specifically showed where the primers needed more contact with the head and then was adjusted so that the headset correctly covered all necessary portions of the treatment area. The application did not allow for tDCS stimulation unless there was appropriate contact with the participant’s head per manufacturer’s design.

Figure 3
Figure 3

Transcranial direct current stimulation placement.

Citation: Journal of Sport Rehabilitation 2020; 10.1123/jsr.2019-0179

Once the primers were in complete contact with the participant’s head, the stimulation session began. Based on manufacturer specifications, the intensity of the signals could reach a maximum of 2.2 mA. However, the application simplified intensity on a scale from 1 (0 mA) to 10 (2.2 mA). At the start of the treatment, the intensity was preset to 5 and could be manually adjusted by the investigator to the participant’s comfort. The stimulation intensity was documented for each testing session.

The tDCS device also allowed for a sham condition, in which the device was used but no electrical stimulation was delivered through the primers. It was explained to the participant that they may or may not feel a sensation from the device during the sham condition. The order in which the sham or stimulation condition was received was randomized. During both the stimulation and sham condition, the participant completed a 20-minute exercise of walking on the treadmill at 2.0 mph at a 1% incline.

Statistical Analyses

All statistical analyses were performed using SPSS statistics software (version 24; IBM, Armonk, NY). Separate 2 × 2 repeated-measures analysis of variance (time × condition) were used to determine significant differences between time and condition for all outcome measures (VM and VL %EMGmax, MVIC, CAR, KOOS Sx, and KOOS Pn). In addition, percentage change scores (change score=[post–prepre]×100) and Cohen d effect sizes with 95% confidence intervals (CIs) were calculated for all variables. Paired samples t tests were conducted on change scores between the tDCS and sham conditions. Alpha level was set a priori at P ≤ .05.

Results

A significant main effect of time was discovered for VM (F9,1 = 11.931, P = .01) and VL %EMGmax (F9,1 = 9.132, P = .01), indicating that regardless of condition, EMG activity decreased from pre to post for each session. During the tDCS session, VM %EMGmax activity decreased by 12.1% (d = −0.88; CI, −1.80 to 0.04), whereas VM %EMGmax activity decreased by 18.9% (d = −1.75, CI, −2.77 to −0.72) during the sham condition. No significant difference was detected for the change in VM %EMGmax between the tDCS and sham conditions (t = 1.07, P = .31; Figure 4). VL %EMGmax activity decreased by 14.8% in the active tDCS trial (d = −0.65; CI, −1.55 to 0.25), whereas in the sham condition, there was a decrease in activity by 25.9% (d = −1.82; CI, −2.86 to −0.78). No significant difference was detected for the change in VL %EMGmax between the tDCS and sham conditions (t = 1.232, P = .25; Figure 5).

Figure 4
Figure 4

The group averages of VM EMG activity at pretesting and posttesting for each condition. EMG indicates electromyography; tDCS, transcranial direct current stimulation; VM, vastus medialis; VMO, vastus medialis oblique; VLO, vastus lateralis oblique. *A significant (P < .05) time main effect inferring that there is a change in VM EMG activity regardless of the condition present during the trial. The percentages represent the change score from pretesting to posttesting. d = 0.41; −0.47 to 1.30; Δ score tDCS = −12.1%; Δ score sham = −18.9% (t = 1.03, P = .31).

Citation: Journal of Sport Rehabilitation 2020; 10.1123/jsr.2019-0179

Figure 5
Figure 5

The group averages of VL EMG activity at pretesting and posttesting for each condition. EMG indicates electromyography; tDCS, transcranial direct current stimulation; VL, vastus lateralis. *A significant (P < .05) time main effect inferring that there is a change in VL EMG activity regardless of the condition present during the trial. The percentages represent the change score from pretesting to posttesting. d = 0.47; −0.41 to 1.36; Δ score tDCS = −14.8%; Δ score sham = −25.9% (t = 1.323, P = .25).

Citation: Journal of Sport Rehabilitation 2020; 10.1123/jsr.2019-0179

A significant main effect for time (F9,1 = 5.343, P = .046) and condition (F9,1 = 12.268, P = .01) was discovered for isometric strength, indicating that regardless of the condition or the time point, there was a change in torque production. During active tDCS, strength decreased by 8.9% (d = −0.41; CI, −1.29 to 0.48), whereas torque decreased by 10.1% (d = −0.42; CI, −1.31 to 0.47) during the sham condition. No significant difference was detected for the change in isometric strength between the tDCS and sham conditions (t = .336, P = .75; Figure 6). There were no significant interactions or main effects discovered for CAR. CAR decreased by 5.03% during the active tDCS trials (d = −0.50; CI, −1.39 to 0.39) and by 5.5% during the sham condition (d = −0.49; CI, −1.38 to 0.40). No significant difference was detected for the change in voluntary activation between the tDCS and sham conditions (t = −.278, P = .79; Figure 7).

Figure 6
Figure 6

The group averages of isometric strength at pretesting and posttesting for each condition. MVIC indicates maximal voluntary isometric contraction; tDCS, transcranial direct current stimulation. *A significant (P < .05) time main effect inferring that there is a change in isometric strength regardless of the condition present during the trial. The percentages represent the change score from pretesting to posttesting. d = 0.12; −0.76 to 1.00; Δ score tDCS = −8.9%; Δ score sham = −10.1% (t = .336, P = .75). MVIC indicates maximal voluntary isometric contraction; tDCS, transcranial direct current stimulation.

Citation: Journal of Sport Rehabilitation 2020; 10.1123/jsr.2019-0179

Figure 7
Figure 7

The group averages of percentage voluntary activation at pretesting and posttesting for each condition. The percentages represent the change score from pretesting to posttesting. CAR indicates central activation ratio; tDCS, transcranial direct current stimulation.

Citation: Journal of Sport Rehabilitation 2020; 10.1123/jsr.2019-0179

A significant time main effect (F9,1 = 15.499, P = .04) revealed that KOOS Sx increased regardless of condition (indicating a reduction in symptoms). There was an increase in KOOS Sx outcome scores after both the tDCS condition, 4.7% (d = 0.21; CI, −0.67 to 1.09), and the sham condition, 3.1% (d = 0.15; CI, −0.72 to 1.03). No significant difference was detected for the change in KOOS Sx between the tDCS and sham conditions (t = 1.929, P = .09; Figure 8). KOOS Pn displayed significant time and condition main effects (time: F9,1 = 15.499, P = .04; condition: F9,1 = 6.106, P = .04), with KOOS Pn scores increasing regardless of condition (indicating a reduction in reported pain). After the tDCS condition, there was a 2.8% increase (d = 0.36; CI, −0.52 to 1.25) and a 0.6% increase after the sham condition (d = 0.07; CI, −0.81 to 0.94). No significant difference was detected for the change in KOOS Pn outcome score between the tDCS and sham conditions (t = .756, P = .47; Figure 9).

Figure 8
Figure 8

The group averages of KOOS Pn score at pretesting and posttesting for each condition. KOOS Pn indicates Knee Injury Osteoarthritis Outcome Score on Pain. *A significant (P < .05) time main effect inferring that there is a change in KOOS Pn score activity regardless of the condition present during the trial. The percentages represent the change score from pretesting to posttesting.

Citation: Journal of Sport Rehabilitation 2020; 10.1123/jsr.2019-0179

Figure 9
Figure 9

The group averages of KOOS Sx score at pretesting and posttesting for each condition. KOOS Sx indicates Knee Injury Osteoarthritis Outcome Score on disease-specific symptom scores.*A significant (P < .05) time main effect inferring that there is a change in KOOS Sx score regardless of the condition present during the trial. The percentages represent the change score from pretesting to posttesting.

Citation: Journal of Sport Rehabilitation 2020; 10.1123/jsr.2019-0179

Discussion

The purpose of this study was to use a randomized crossover design to determine if a single treatment of tDCS would improve quadriceps muscle activity and reduce levels of pain and symptoms during exercise in participants with a history of ACLR. The investigation discovered that there were no differences in quadriceps muscle activity or any self-reported outcomes when comparing active tDCS and sham treatments. The %EMGmax activity in both the VM and VL muscles was lower posttreatment (active or sham) with no differences between conditions. Decreased quadriceps strength and voluntary activation were also present in both the active tDCS and sham conditions when observing the pre and post time points. There were no differences in subjective scoring for the KOOS Pn and KOOS Sx.

Both VL and VM %EMGmax activity significantly declined following the 20-minute treadmill walking exercise for both the tDCS and sham conditions, however no interaction effect was discovered, indicating that tDCS had no effect on EMG activity. The decrease in EMG activity was surprising to the investigators, as we did not expect 20 minutes of walking to result in a decline of muscle activity. This may speak to the increased fatigability of the quadriceps muscle following ACLR, even during low demand task such as walking.27,28 Even with a decline in EMG activity from the walking session, we still believed that tDCS would at least be protective to the EMG decline comparative to the sham session. Thus, our results are contrary to our hypothesis, as we had believed that tDCS would increase muscle activity from pretreatment to posttreatment (or preserve muscle activity), allowing for more muscle activation to be available during exercise. Although not statistically significant, it should be noted that when observing change scores and effect sizes from premeasurement and postmeasurement, there is less of an average decline in percentage of maximum EMG activity in the tDCS compared with the sham treatment for both the VM (tDCS = 12.1% decrease; sham = 18.9% decrease; d = 0.41; CI, −0.47 to 1.30) and VL (tDCS = 14.8% decrease; sham = 25.9% decrease; d = 0.47, CI, −0.41 to 1.36). This potentially indicates that the tDCS group may be becoming more neurally efficient or is fatiguing less quickly in comparison with the sham group, however with no statistically significant findings and weak to moderate effect sizes, these differences remain inconclusive. Larger sample sizes are warranted to further investigate the effect tDCS has on overall muscle activation. Although there is limited evidence on tDCS in musculoskeletal populations, a study by Cogiamanian et al,29 used EMG as a measurement in a fatiguing trial using maximal isometric contractions for the elbow flexors in a healthy population. It was shown that EMG activation was significantly higher immediately after the tDCS treatment; however, this finding was also demonstrated in the control/placebo group as well. Combined with the results of the current investigation, these findings indicate that the immediate application of tDCS has no effect on the change in EMG activation during exercise.

Similar to our EMG outcomes, tDCS did not have a significant effect on isometric muscle strength, voluntary activation, or patient reported outcomes of pain and symptoms. We hypothesized tDCS may have been beneficial in the ACLR population because of the direct stimulation over the primary motor cortex. The motor cortex stores pyramidal cells that are responsible for activating alpha motor neurons, which directly simulates muscle during voluntary contractions.15 Theoretically, by increasing the motor cortex excitability with direct electrical stimulation, there should have been an increase in muscular activation or strength immediately after the tDCS was delivered due to the increased activity of the alpha motor neurons. Similar to Cogiamanian et al,29 Angius et al30 also investigated the effects of different tDCS electrode locations on lower limb isometric exercise and endurance time. Muscle strength decreased significantly after the endurance trials, but the rate of perceived exhaustion and time to exhaustion was significantly longer with an electrode placement that included left motor cortex and above the right shoulder. It is possible that the electrode placement by Angius et al,30 in contrast to the stimulation location (and portable device) used in our study, is more beneficial for observing gains in peripheral muscle function. However, more investigations are needed to understand the electrode placement on patient outcomes.

Vargas et al31 examined the effects of tDCS on MVICs of the quadriceps in a healthy group of soccer players, which included an active and a sham session while measuring 5 different MVICs at different time points post-tDCS/sham condition. When compared with the sham tDCS, the active tDCS improved MVIC during, 30 minutes post, and 60 minutes post treatment by 5.2%, 6.3%, and 9.4% in the dominant limb.31 Unlike Vargas et al31 who utilized healthy individuals, isometric strength values in our study decreased for the tDCS (8.9% decrease) and sham (10.1% decrease) conditions after 20 minutes of walking (d = 0.12; CI, −0.76 to 1.00). This decrease in torque may be the result from the active recovery following the pretesting. A study conducted by Zarrouk et al,32 compared recovery strategies after peak torque trials during isokinetic contractions of the quadriceps muscles. Peak torque and EMG data were both collected to see the effects of passive recovery, active recovery, and electromyostimulation recovery after the fatiguing task.32 The investigators provided evidence that the active recovery sessions resulted in a greater deficit in peak torque for isokinetic contractions at 60, 120, and 180°/s.32 Also, following the active recovery, there were deficits in EMG activity levels when compared with the passive rest and electromyostimulation rest.32 Based on these results, we may have had a similar experience with our trials. Future experiments would benefit from investigating the effect of active and passive recovery in between the sham and active tDCS conditions.

We also expected to see an improvement in subjective scores after the tDCS condition based on the improvement in pain and symptom scores in patients with osteoarthritis and total knee arthroplasty.24,25 When observing the change scores and effect sizes for KOOS Pn (d = 0.41; CI, −0.48 to 1.30; tDCS = 2.8% increase, sham = 0.6% increase) and KOOS Sx (d = 0.52; CI, −0.37 to 1.41; tDCS = 4.7% increase, sham = 3.1% increase), there was a statistically significant increase from the premeasurement and postmeasurement regardless of the condition. The slight improvement of these scores may be a result of the 20 minutes of treadmill walking. Exercise as a symptom management provides evidence-based treatment while also providing similar, if not better, effects in comparison with other medical treatments.33 Therefore, it would make sense to see a slight improvement in scores even with this short bout of exercise. However, the subjective scores improvement did not meet the minimal detectable change for either condition. For the KOOS scores, the pain subsection needs at least a raw change score of 6 points and whereas the symptom subsection needs to present a 5 to 8.5 point change in the raw scores.34 To conclusively say that exercise had an effect on the subjective scores, we would need to see a higher change in the raw scores. With more participants, we may see more of a meaningful change.

It is important to note that we were investigating the immediate effects of tDCS during exercise, and therefore only 1 trial of tDCS was performed. Previous literature has suggested that after ACLR, the central nervous system undergoes neuroplasticity and alters excitability of the motor cortex as participants’ progress through the injury process.8 Due to this reorganization, there is a lack of communication between the central nervous system and the muscles surrounding the reconstructed joint. The increased neuroplasticity results in higher activation in other parts of the brain outside of the motor cortex (anterior cingulate gyrus, inferior frontal gyrus, etc) to complete specific functional tasks.35 These changes in the neural pathways have been shown to exist up to 6-year post-ACLR.35 We specifically chose participants with a history of ACLR due to the progression of cortical changes that are greater at later stages of injury.8,13 Our participants were on ranged from 11-month to 12-year post-ACLR. Due to the persistent restructuring in the pathways, we believe that 1 session of tDCS was not enough to reverse the effects of the pathway alterations. Future research should investigate whether utilizing tDCS in acute stages of rehabilitation would be protective to the documented deficits in corticospinal excitability of ACLR patients. Previous tDCS studies in other populations have used multiple treatment sessions of active tDCS where they saw beneficial effects resulting from the treatment,24,25 and we believe that future research should investigate the effect of multiple tDCS sessions in the ACLR population. It is vital for researchers to understand the dose response of tDCS in ACLR patients to investigate how many tDCS sessions result in beneficial gains in neuromuscular function.

Limitations

Although we believe a strength of this study is the investigation of peripheral measures of muscle function following a centrally applied intervention, the collection of gross measurements of torque and EMG data may have limited our ability to detect significant changes. More sensitive outcome measures such as transcranial magnetic stimulation (TMS) would be beneficial to future investigations to help detect any immediate changes in corticospinal excitability at the cortex level. TMS has been used in studies noting neuromuscular changes in ACLR patients because of the corticospinal changes postsurgery.8,10,17,19,28,3538 Although the tDCS unit in the current study did not have shown any peripheral effects, there may have been an increase of activity within the motor cortex that we were not able to detect. TMS would have allowed for us to obtain premeasurement and postmeasurement of corticospinal excitability. Another limitation of this present study, and the stimulator used is that we did not know the exact intensity of the stimulation to the motor cortex. Although the product has its own scale of intensity (1–10), there is no algorithm provided to help determine the exact milliamps used to stimulate the brain. Our investigation team was also not able to determine the depth of stimulation of the motor cortex. The area of the motor cortex directly responsible for quadriceps muscle function is located slightly deeper than the rest of the active areas. In future studies, electroencephalography could be used to help determine the depth of penetration of the motor cortex after an active tDCS trial. We did not control for sport participation of our participants or surgical technique. Type of sport may influence individual’s motor programs and should be further investigated in future research. Finally, due to the cross-sectional nature of this study we were unable to control for surgical procedures/techniques used.

Conclusions

The results of this investigation suggested that there was a decline in EMG activity as well as isometric strength whether participants received active tDCS or a sham condition. Also, isometric strength was shown to change no matter what time point the data was collected at. Subjective scores were shown to increase between precondition and postcondition and was not dependent on the condition. No significant interactions were detected between time and condition for individuals with ACLR following active tDCS. Future research needs to observe the effects of tDCS at different time points on multiple testing sessions. More sensitive measures, such as TMS, should be collected to determine if tDCS has any effect on corticospinal excitability.

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    • Export Citation
  • 3.

    Lohmander LS, Ostenberg A, Englund M, Roos H. High prevalence of knee osteoarthritis, pain, and functional limitations in female soccer players twelve years after anterior cruciate ligament injury. Arthritis Rheum. 2004;50(10):31453152. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    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(6):806819. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Li RT, Lorenz S, Xu Y, Harner CD, Fu FH, Irrgang JJ. Predictors of radiographic knee osteoarthritis after anterior cruciate ligament reconstruction. Am J Sports Med. 2011;39(12):25952603. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Oiestad BE, Holm I, Aune AK, et al. Knee function and prevalence of knee osteoarthritis after anterior cruciate ligament reconstruction: a prospective study with 10 to 15 years of follow-up. Am J Sports Med. 2010;38(11):22012210.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Palmieri-Smith RM, Thomas AC, Wojtys EM. Maximizing quadriceps strength after ACL reconstruction. Clin Sports Med. 2008;27(3):405424. doi:

  • 8.

    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(6):828839. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Thomas AC, Villwock M, Wojtys EM, Palmieri-Smith RM. Lower extremity muscle strength after anterior cruciate ligament injury and reconstruction. J Athl Train. 2013;48(5):610620. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Pietrosimone BG, Lepley AS, Ericksen HM, Gribble PA, Levine J. Quadriceps strength and corticospinal excitability as predictors of disability after anterior cruciate ligament reconstruction. J Sport Rehabil. 2013;22(1):16. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Paterno MV, Schmitt LC, Ford KR, et al. 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. 2010;38(10):19681978. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    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(2):302311. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Needle AR, Lepley AS, Grooms DR. Central nervous system adaptation after ligamentous injury: a summary of theories, evidence, and clinical interpretation. Sports Med. 2017;47(7):12711288. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Hart JM, Pietrosimone B, Hertel J, Ingersoll CD. Quadriceps activation following knee injuries: a systematic review. J Athl Train. 2010;45(1):8797. doi:

  • 15.

    Hopkins JT, Ingersoll CD. Arthogenic muscle inhibition: a limiting factor in joint rehabilitation. J Sport Rehabil. 2000;9(2):135159. doi:

  • 16.

    Ingelsrud LH, Terwee CB, Terluin B, et al. Meaningful change scores in the knee injury and osteoarthritis outcome score in patients undergoing anterior cruciate ligament reconstruction. Am J Sports Med. 2018;46(5):11201128. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    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(3):736742. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Pietrosimone B, Lepley AS, Harkey MS, et al. Quadriceps strength predicts self-reported function post-ACL reconstruction. Med Sci Sports Exerc. 2016;48(9):16711677. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Pietrosimone B, McLeod MM, Florea D, Gribble PA, Tevald MA. Immediate increases in quadriceps corticomotor excitability during an electromyography biofeedback intervention. J Electromyogr Kinesiol. 2015;25(2):316322. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Pietrosimone BG, McLeod MM, Lepley AS. A theoretical framework for understanding neuromuscular response to lower extremity joint injury. Sports Health. 2012;4(1):3135. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Ward S, Pearce AJ, Pietrosimone B, Bennell K, Clark R, Bryant AL. Neuromuscular deficits after peripheral joint injury: a neurophysiological hypothesis. Muscle Nerve. 2015;51(3):327332. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Rice DA, McNair PJ. Quadriceps arthrogenic muscle inhibition: neural mechanisms and treatment perspectives. Semin Arthritis Rheum. 2010;40(3):250266. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Ziemann U, Paulus W, Nitsche MA, et al. Consensus: motor cortex plasticity protocols. Brain Stimul. 2008;1(3):164182. doi:

  • 24.

    Borckardt JJ, Reeves ST, Robinson SM, et al. Transcranial direct current stimulation (tDCS) reduces postsurgical opioid consumption in total knee arthroplasty (TKA). Clin J Pain. 2013;29(11):925928. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Chang WJ, Bennell KL, Hodges PW, et al. Addition of transcranial direct current stimulation to quadriceps strengthening exercise in knee osteoarthritis: a pilot randomised controlled trial. PLoS One. 2017;12(6):e0180328. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Krishnan C, Washabaugh EP, Dutt-Mazumder A, Brown SR, Wojtys EM, Palmieri-Smith RM. Conditioning brain responses to improve quadriceps function in an individual with anterior cruciate ligament reconstruction. Sports Health. 2019;11(4):306315. doi:

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27.

    Kuenze CM, Hertel J, Hart JM. Quadriceps muscle function after exercise in men and women with a history of anterior cruciate ligament reconstruction. J Athl Train. 2014;49(6):740746. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    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(5):475485. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Cogiamanian F, Marceglia S, Ardolino G, Barbieri S, Priori A. Improved isometric force endurance after transcranial direct current stimulation over the human motor cortical areas. Eur J Neurosci. 2007;26(1):242249. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Angius L, Pageaux B, Hopker J, Marcora SM, Mauger AR. Transcranial direct current stimulation improves isometric time to exhaustion of the knee extensors. Neuroscience. 2016;339:363375. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Vargas VZ, Baptista AF, Pereira GOC, et al. Modulation of isometric quadriceps strength in soccer players with transcranial direct current stimulation: a crossover study. J Strength Cond Res. 2018;32(5):13361341. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Zarrouk N, Rebai H, Yahia A, Souissi N, Hug F, Dogui M. Comparison of recovery strategies on maximal force-generating capacity and electromyographic activity level of the knee extensor muscles. J Athl Train. 2011;46(4):386394. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Pedersen BK, Saltin B. Exercise as medicine—evidence for prescribing exercise as therapy in 26 different chronic diseases. Scand J Med Sci Sports. 2015;25(suppl 3):172. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Collins NJ, Misra D, Felson DT, Crossley KM, Roos EM. Measures of knee function: International Knee Documentation Committee (IKDC) subjective knee evaluation form, Knee Injury and Osteoarthritis Outcome Score (KOOS), Knee Injury and Osteoarthritis Outcome Score Physical Function Short form (KOOS-PS), Knee Outcome Survey Activities of Daily Living Scale (KOS-ADL), Lysholm Knee Scoring Scale, Oxford Knee Score (OKS), Western Ontario and McMaster Universities Osteoarthritis Index (WOMAC), Activity Rating Scale (ARS), and Tegner Activity Score (TAS). Arthritis Care Res. 2011;63(suppl 11):S208S228. doi:

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35.

    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(5):12671278. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Lepley AS, Bahhur NO, Murray AM, Pietrosimone BG. Quadriceps corticomotor excitability following an experimental knee joint effusion. Knee Surg Sports Traumatol Arthrosc. 2015;23(4):10101017. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Lepley AS, Gribble PA, Thomas AC, Tevald MA, Sohn DH, Pietrosimone BG. Longitudinal evaluation of stair walking biomechanics in patients with ACL injury. Med Sci Sports Exerc. 2016;48(1):715. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Pietrosimone BG, Lepley AS, Ericksen HM, Clements A, Sohn DH, Gribble PA. Neural excitability alterations after anterior cruciate ligament reconstruction. J Athl Train. 2015;50(6):665674. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

If the inline PDF is not rendering correctly, you can download the PDF file here.

Rush is with the School of Exercise and Rehabilitation Sciences, College of Health and Human Services, The University of Toledo, Toledo, OH, USA. L.K. Lepley and A.S. Lepley are with the School of Kinesiology, University of Michigan, Ann Arbor, MI, USA. Davi is with the Sports Optimization and Rehabilitation Laboratory, Department of Kinesiology, University of Connecticut, Storrs, CT, USA. A.S. Lepley is also with the Michigan Performance Research Laboratory, University of Michigan, Ann Arbor, MI, USA.

Rush (justin.rush@rockets.utoledo.edu) is corresponding author.
  • View in gallery

    (A) Positioning for MVIC testing. (B) CAR testing. Visual representation of the SIB technique to determine the voluntary activation of the quadriceps, including the equation to find the percentage of quadriceps activation. The MVIC was divided by the torque produced with the SIB. CAR indicates central activation ratio; MVIC, maximal voluntary isometric contraction; SIB, superimposed burst.

  • View in gallery

    Electromyography sensor and stimulation pad placement.

  • View in gallery

    Transcranial direct current stimulation placement.

  • View in gallery

    The group averages of VM EMG activity at pretesting and posttesting for each condition. EMG indicates electromyography; tDCS, transcranial direct current stimulation; VM, vastus medialis; VMO, vastus medialis oblique; VLO, vastus lateralis oblique. *A significant (P < .05) time main effect inferring that there is a change in VM EMG activity regardless of the condition present during the trial. The percentages represent the change score from pretesting to posttesting. d = 0.41; −0.47 to 1.30; Δ score tDCS = −12.1%; Δ score sham = −18.9% (t = 1.03, P = .31).

  • View in gallery

    The group averages of VL EMG activity at pretesting and posttesting for each condition. EMG indicates electromyography; tDCS, transcranial direct current stimulation; VL, vastus lateralis. *A significant (P < .05) time main effect inferring that there is a change in VL EMG activity regardless of the condition present during the trial. The percentages represent the change score from pretesting to posttesting. d = 0.47; −0.41 to 1.36; Δ score tDCS = −14.8%; Δ score sham = −25.9% (t = 1.323, P = .25).

  • View in gallery

    The group averages of isometric strength at pretesting and posttesting for each condition. MVIC indicates maximal voluntary isometric contraction; tDCS, transcranial direct current stimulation. *A significant (P < .05) time main effect inferring that there is a change in isometric strength regardless of the condition present during the trial. The percentages represent the change score from pretesting to posttesting. d = 0.12; −0.76 to 1.00; Δ score tDCS = −8.9%; Δ score sham = −10.1% (t = .336, P = .75). MVIC indicates maximal voluntary isometric contraction; tDCS, transcranial direct current stimulation.

  • View in gallery

    The group averages of percentage voluntary activation at pretesting and posttesting for each condition. The percentages represent the change score from pretesting to posttesting. CAR indicates central activation ratio; tDCS, transcranial direct current stimulation.

  • View in gallery

    The group averages of KOOS Pn score at pretesting and posttesting for each condition. KOOS Pn indicates Knee Injury Osteoarthritis Outcome Score on Pain. *A significant (P < .05) time main effect inferring that there is a change in KOOS Pn score activity regardless of the condition present during the trial. The percentages represent the change score from pretesting to posttesting.

  • View in gallery

    The group averages of KOOS Sx score at pretesting and posttesting for each condition. KOOS Sx indicates Knee Injury Osteoarthritis Outcome Score on disease-specific symptom scores.*A significant (P < .05) time main effect inferring that there is a change in KOOS Sx score regardless of the condition present during the trial. The percentages represent the change score from pretesting to posttesting.

  • 1.

    Griffin LY, Albohm MJ, Arendt EA, et al. Understanding and preventing noncontact anterior cruciate ligament injuries: a review of the Hunt Valley II meeting, January 2005. Am J Sports Med. 2006;34(9):15121532. doi:

    • Crossref
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    Salmon L, Russell V, Musgrove T, Pinczewski L, Refshauge K. Incidence and risk factors for graft rupture and contralateral rupture after anterior cruciate ligament reconstruction. Arthroscopy. 2005;21(8):948957. doi:

    • Crossref
    • PubMed
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    • Export Citation
  • 3.

    Lohmander LS, Ostenberg A, Englund M, Roos H. High prevalence of knee osteoarthritis, pain, and functional limitations in female soccer players twelve years after anterior cruciate ligament injury. Arthritis Rheum. 2004;50(10):31453152. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    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(6):806819. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Li RT, Lorenz S, Xu Y, Harner CD, Fu FH, Irrgang JJ. Predictors of radiographic knee osteoarthritis after anterior cruciate ligament reconstruction. Am J Sports Med. 2011;39(12):25952603. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Oiestad BE, Holm I, Aune AK, et al. Knee function and prevalence of knee osteoarthritis after anterior cruciate ligament reconstruction: a prospective study with 10 to 15 years of follow-up. Am J Sports Med. 2010;38(11):22012210.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Palmieri-Smith RM, Thomas AC, Wojtys EM. Maximizing quadriceps strength after ACL reconstruction. Clin Sports Med. 2008;27(3):405424. doi:

  • 8.

    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(6):828839. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Thomas AC, Villwock M, Wojtys EM, Palmieri-Smith RM. Lower extremity muscle strength after anterior cruciate ligament injury and reconstruction. J Athl Train. 2013;48(5):610620. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Pietrosimone BG, Lepley AS, Ericksen HM, Gribble PA, Levine J. Quadriceps strength and corticospinal excitability as predictors of disability after anterior cruciate ligament reconstruction. J Sport Rehabil. 2013;22(1):16. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Paterno MV, Schmitt LC, Ford KR, et al. 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. 2010;38(10):19681978. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    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(2):302311. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Needle AR, Lepley AS, Grooms DR. Central nervous system adaptation after ligamentous injury: a summary of theories, evidence, and clinical interpretation. Sports Med. 2017;47(7):12711288. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Hart JM, Pietrosimone B, Hertel J, Ingersoll CD. Quadriceps activation following knee injuries: a systematic review. J Athl Train. 2010;45(1):8797. doi:

  • 15.

    Hopkins JT, Ingersoll CD. Arthogenic muscle inhibition: a limiting factor in joint rehabilitation. J Sport Rehabil. 2000;9(2):135159. doi:

  • 16.

    Ingelsrud LH, Terwee CB, Terluin B, et al. Meaningful change scores in the knee injury and osteoarthritis outcome score in patients undergoing anterior cruciate ligament reconstruction. Am J Sports Med. 2018;46(5):11201128. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    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(3):736742. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Pietrosimone B, Lepley AS, Harkey MS, et al. Quadriceps strength predicts self-reported function post-ACL reconstruction. Med Sci Sports Exerc. 2016;48(9):16711677. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Pietrosimone B, McLeod MM, Florea D, Gribble PA, Tevald MA. Immediate increases in quadriceps corticomotor excitability during an electromyography biofeedback intervention. J Electromyogr Kinesiol. 2015;25(2):316322. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Pietrosimone BG, McLeod MM, Lepley AS. A theoretical framework for understanding neuromuscular response to lower extremity joint injury. Sports Health. 2012;4(1):3135. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Ward S, Pearce AJ, Pietrosimone B, Bennell K, Clark R, Bryant AL. Neuromuscular deficits after peripheral joint injury: a neurophysiological hypothesis. Muscle Nerve. 2015;51(3):327332. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Rice DA, McNair PJ. Quadriceps arthrogenic muscle inhibition: neural mechanisms and treatment perspectives. Semin Arthritis Rheum. 2010;40(3):250266. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Ziemann U, Paulus W, Nitsche MA, et al. Consensus: motor cortex plasticity protocols. Brain Stimul. 2008;1(3):164182. doi:

  • 24.

    Borckardt JJ, Reeves ST, Robinson SM, et al. Transcranial direct current stimulation (tDCS) reduces postsurgical opioid consumption in total knee arthroplasty (TKA). Clin J Pain. 2013;29(11):925928. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Chang WJ, Bennell KL, Hodges PW, et al. Addition of transcranial direct current stimulation to quadriceps strengthening exercise in knee osteoarthritis: a pilot randomised controlled trial. PLoS One. 2017;12(6):e0180328. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Krishnan C, Washabaugh EP, Dutt-Mazumder A, Brown SR, Wojtys EM, Palmieri-Smith RM. Conditioning brain responses to improve quadriceps function in an individual with anterior cruciate ligament reconstruction. Sports Health. 2019;11(4):306315. doi:

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27.

    Kuenze CM, Hertel J, Hart JM. Quadriceps muscle function after exercise in men and women with a history of anterior cruciate ligament reconstruction. J Athl Train. 2014;49(6):740746. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    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(5):475485. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Cogiamanian F, Marceglia S, Ardolino G, Barbieri S, Priori A. Improved isometric force endurance after transcranial direct current stimulation over the human motor cortical areas. Eur J Neurosci. 2007;26(1):242249. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Angius L, Pageaux B, Hopker J, Marcora SM, Mauger AR. Transcranial direct current stimulation improves isometric time to exhaustion of the knee extensors. Neuroscience. 2016;339:363375. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Vargas VZ, Baptista AF, Pereira GOC, et al. Modulation of isometric quadriceps strength in soccer players with transcranial direct current stimulation: a crossover study. J Strength Cond Res. 2018;32(5):13361341. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Zarrouk N, Rebai H, Yahia A, Souissi N, Hug F, Dogui M. Comparison of recovery strategies on maximal force-generating capacity and electromyographic activity level of the knee extensor muscles. J Athl Train. 2011;46(4):386394. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Pedersen BK, Saltin B. Exercise as medicine—evidence for prescribing exercise as therapy in 26 different chronic diseases. Scand J Med Sci Sports. 2015;25(suppl 3):172. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Collins NJ, Misra D, Felson DT, Crossley KM, Roos EM. Measures of knee function: International Knee Documentation Committee (IKDC) subjective knee evaluation form, Knee Injury and Osteoarthritis Outcome Score (KOOS), Knee Injury and Osteoarthritis Outcome Score Physical Function Short form (KOOS-PS), Knee Outcome Survey Activities of Daily Living Scale (KOS-ADL), Lysholm Knee Scoring Scale, Oxford Knee Score (OKS), Western Ontario and McMaster Universities Osteoarthritis Index (WOMAC), Activity Rating Scale (ARS), and Tegner Activity Score (TAS). Arthritis Care Res. 2011;63(suppl 11):S208S228. doi:

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35.

    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(5):12671278. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Lepley AS, Bahhur NO, Murray AM, Pietrosimone BG. Quadriceps corticomotor excitability following an experimental knee joint effusion. Knee Surg Sports Traumatol Arthrosc. 2015;23(4):10101017. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Lepley AS, Gribble PA, Thomas AC, Tevald MA, Sohn DH, Pietrosimone BG. Longitudinal evaluation of stair walking biomechanics in patients with ACL injury. Med Sci Sports Exerc. 2016;48(1):715. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Pietrosimone BG, Lepley AS, Ericksen HM, Clements A, Sohn DH, Gribble PA. Neural excitability alterations after anterior cruciate ligament reconstruction. J Athl Train. 2015;50(6):665674. doi:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
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