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Lower extremity neuromuscular compensations during instrumented single leg hop testing 2–10 years following ACL reconstruction
The Knee 21 (2014) 1191–1197
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The Knee
Lower extremity neuromuscular compensations during instrumented single leg hop testing 2–10 years following ACL reconstruction John Nyland ⁎, Jeff Wera, Scott Klein, David N.M. Caborn Division of Sports Medicine, Department of Orthopaedic Surgery, University of Louisville, United States Athletic Training Program, Spalding University, 901 South 4th Street, Louisville, KY 40203-2188, United States
a r t i c l e
i n f o
Article history: Received 26 September 2013 Received in revised form 28 May 2014 Accepted 21 July 2014 Keywords: Electromyography Dynamic postural stability Allograft Perceived function Knee
a b s t r a c t Background: This study compared lower extremity EMG activation and sagittal plane kinematics of subjects at a minimum of 2 years post-successful ACL reconstruction and rehabilitation during instrumented single leg hop testing. Methods: Comparisons were made based on subject responses to the following question, “compared to prior to your knee injury how capable are you now in performing sports activities”? Group 1 = very capable, Group 2 = capable, and Group 3 = not capable. In addition to EMG (1000 Hz) and kinematic (60 Hz) data, subjective knee function, internal health locus of control, sports activity characteristics (intensity, frequency) pre-knee injury, and at follow-up were also compared. Results: Group 3 had lower perceived knee function, decreased perceived sports intensity, and more subjects with decreased sports activity intensity by two levels compared to pre-injury values. Perceived function scores, anterior laxity measurements and grades were similar between groups. During single leg hop propulsion and landing Group 1 (very capable) had greater involved lower extremity gluteus maximus and medial hamstring activation amplitudes than Group 3 (not capable). Perceived sports capability was related to better subjective knee function, and higher perceived sports activity intensity. Conclusion: Neuromuscular compensations suggesting a hip bias with increased gluteus maximus and medial hamstring activation were identified at the involved lower extremity among most subjects who perceived high perceived sports capability compared to pre-injury status. These compensations may be related to a permanent neurosensory deficit, and its influence on afferent pathway changes that influence CNS sensorimotor re-organization. © 2014 Elsevier B.V. All rights reserved.
1. Introduction No matter how well documented the functional deficits associated with ACL deficiency are, the etiologic factors have not been clarified [1]. There is growing evidence that supports the concept that in addition to mechanical deficiency, ACL rupture represents a de-afferentation injury that may lead to changes in ascending afferent pathway information leading to central nervous system (CNS) re-organization of sensorimotor programming [2–9]. The CNS has the capacity to adapt according to the stimulus it receives from the ascending afferent pathways. The ability of the brain to undergo any enduring morphological or functional cortical property re-organization is referred to as plasticity or neuroplasticity [1,4]. Although mechanical function is largely restored following surgical reconstruction, since neurosensory function is not re-established, ACL injury may influence lower extremity neuromuscular activation long after successful surgical reconstruction and rehabilitation [10–13]. ⁎ Corresponding author. Tel.: +1 502 873 4224; fax: +1 502 585 7149. E-mail address: [email protected] (J. Nyland).
http://dx.doi.org/10.1016/j.knee.2014.07.017 0968-0160/© 2014 Elsevier B.V. All rights reserved.
In studies of ACL deficient subjects and subjects following ACL injury and reconstruction, Valeriani et al. [2,3] identified altered somatosensory evoked potentials in a number of patients suggesting that ACL rupture lead to changes in ascending afferent pathway information and CNS re-organization. They suggested that deafferentation from ACL rupture could not be replaced by input from other knee joint somatosensory input or by the mechanical stability provided by reconstructive surgery [2]. In a study of 17 subjects with ACL deficiency, Courtney et al. [5] suggested that reduced knee proprioception was related to CNS re-organization of sensorimotor programming that facilitated motor program modifications to produce more efficient lower extremity neuromuscular activation synergies during gait. In a followup study they reported that ACL deficient subjects, who did not have impaired strength, resumed pre-injury function via altered lower extremity neuromuscular synergies and somatosensory evoked potentials [6]. In an electroencephalography study of 10 patients at N 1 year post-ACL reconstruction, Baumeister et al. [7] reported greater cortical activation in the parietal brain regions compared to healthy control subjects during a knee angle re-production task suggesting a greater need for focused attention to achieve effective task performance. In a later
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study comparing nine patients following ACL reconstruction with nine health control subjects they reported that the ACL reconstruction group required greater attentional control brain activation to reproduce 50% maximum voluntary quadriceps femoris isometric contraction forces at 90° knee flexion [8]. In a functional MRI study comparing the brain activation of 18 healthy volunteers with 17 subjects with chronic ACL deficiency, Kapreli et al. [1] reported that the ACL deficient subject group had diminished activation in several sensorimotor cortical areas and increased activation in the contralateral pre-supplementary motor area, contralateral posterior somatosensory area, and the ipsilateral posterior inferior temporal gyrus compared to the control group. They concluded that a likely explanation for this CNS re-organization of sensorimotor programming was the establishment of neurophysiologic changes in the ACL injury group [1]. Lower extremity neuromuscular extensor function, particularly at the quadriceps femoris, is compromised following ACL injury and reconstruction [14–17]. This impairs its ability to effectively attenuate impact forces, increasing knee injury or re-injury risk [16–18]. Since landing from a single leg hop for distance places high demands on the lower extremity extensor musculature to absorb sudden impact forces, this test is a widely-used clinical method for evaluating function following knee injury or surgery prior to release to sports [18–21]. The purpose of this component of a larger study [11,22,23] was to compare the involved and uninvolved lower extremity EMG activation amplitudes and sagittal plane kinematics of subjects at a minimum of two years post-successful ACL reconstruction and rehabilitation, during instrumented single leg hop for distance testing, and compare these findings by subject perceived sports capability level. Subjective knee function, internal health locus of control (IHLOC) and sports activity characteristics (intensity, frequency) pre-knee injury, and at time of follow-up were also compared. Based on previous work [11] and the work of others [1–3,5–9,24,25], the hypothesis was that lower extremity neuromuscular activation during single leg hop for distance testing would differ between the lower extremity that had undergone successful ACL reconstruction and rehabilitation and the uninvolved contralateral lower extremity between groups of differing perceived sports capability compared to pre-injury status. 2. Methods 2.1. Experimental design This was an evidence level IV therapeutic case series. 2.2. Subjects From a group of 206 potential subjects who responded to the survey portion of a larger study [11,22,23], 70 subjects (35 men, 35 women) agreed to participate in this clinical phase. To control for the possible influence of knee laxity on lower extremity neuromuscular activation, subjects who displayed a positive pivot shift glide [26] or a side-toside anterior translation knee laxity difference N4 mm were not included in this comparison decreasing the subject number to 65 (32 men, 33 women) subjects at 5.2 ± 2.9 years post-surgery. Subjects that participated in this clinical phase otherwise met the inclusion criteria of the survey study [22]. Medical institutional research review board approval was obtained, and subjects provided written informed consent. A minimum of two years had passed since subjects underwent unilateral primary ACL reconstruction with allograft tissue performed by the senior author using transtibial tunnel drilling and bioabsorbable interference screw fixation. Former patients who had undergone meniscal debridement, partial meniscectomy or meniscal repair (approximately 62%), or who had grade I to III chondral injury at the medial or lateral femoral condyle (approximately 10%) were allowed to participate. Patients who had a posterior cruciate ligament injury, had undergone collateral ligament surgery, had an impaired contralateral knee, or who had not
adhered to the standardized progressive rehabilitation program were excluded from study participation. Surgical intervention details and rehabilitation program functional milestone timetable information have been previously reported [11]. Review of medical charts and physical therapy records revealed that all subjects had complied with rehabilitation program recommendations and all had met or exceeded standard accepted return-to-sports activity goals of a minimum 85% bilateral equivalence with single leg hop for distance testing and 60°/s isokinetic peak knee extensor and flexor torque testing prior to release from care [12,19,27,28]. 2.3. Data collection procedures Clinical examination included knee joint palpation, passive knee range-of-motion assessment using a handheld goniometer, and anterior translational knee arthrometric testing at 133.4 N (KT-1000; MEDmetric, San Diego, CA, USA). Electromyographic (4-channel, MyoSystem 1200; Noraxon, Scottsdale, AZ, USA; 1000 Hz), and two-dimensional sagittal plane kinematic (SIMI Motion 2D, Unterschleissheim, Germany; 60 Hz) data were collected during single leg hop for distance testing. Gluteus maximus, vastus medialis, medial hamstrings and medial head of gastrocnemius EMG activation amplitudes were standardized to levels attained during single repetition, maximal volitional effort isometric contractions (%MVIC). Additional details regarding EMG data collection and analysis methods have been previously reported [11]. The primary investigator performed the clinical evaluation and administered all tests. Lower extremity test order was alternated between subjects to control for potential order effects. Passive knee flexion range of motion was evaluated with subjects in prone. Passive knee extension range of motion was evaluated with subjects in supine. In both cases subjects actively flexed or extended their knee as far as possible. Following this the primary investigator applied a slight pressure (approximately 22 N) to assure that complete range of motion was achieved. Prior to single leg hop for distance testing subjects performed two practice trials with each lower extremity. Only two practice trials were performed prior to data collection as all subjects had previous familiarity with test procedures. Testing was performed with unrestricted upper extremity movements using previously reported techniques [29]. Retro-reflective markers were secured over the shoe of the test lower extremity to depict the head of the fifth metatarsal, 2 cm distal to the protuberance of the lateral malleolus, over the joint line of the lateral knee, over gym shorts depicting the greater trochanter of the femur, and over the spinous process of the third lumbar vertebrae. Following practice subjects performed three test trials with each lower extremity (Fig. 1). A 3 m long by 2 m tall calibration space was used for hip, knee, and ankle kinematic displacement measurement calculations at single leg hop for distance landing. Following marker digitization and tracking, marker paths were smoothed once using a low-pass digital filter. Peak displacement of the hip, knee, and ankle was measured manually by the primary investigator using a software curser function. Sports activity participation level intensity and frequency prior to ACL injury and at time of follow-up were measured using the Knee Outcome Survey Sports Activity Scale [11,22] and IHLOC was measured using Multidimensional Health Locus of Control Survey Form C scores [23,31,32]. The International Knee Documentation Committee (IKDC) Subjective Knee Form was used to determine perceived knee function [33]. 2.4. Subject grouping Subject group assignments were made based on how they responded to the following question: “Compared to prior to your knee injury how capable are you now in performing sports activities”, very capable (group 1), capable (group 2), or not capable (group 3)? Most study subjects perceived that they had returned back to their preferred sport at
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Pilot testing of 6 subjects (3 men, 3 women) with similar demographics as study subjects (very capable = 2, capable = 2, not capable = 2) revealed that surface EMG measurements had excellent test–retest reliability with intraclass correlation coefficients of 0.95–0.99 with comparable reliability noted for both single leg hop for distance test propulsion and landing phases. Intra-rater test–retest reliability for passive knee range of motion measurements of the same subjects by the primary investigator using a handheld goniometer was 0.95 for knee extension and 0.97 for knee flexion. Two-dimensional sagittal plane kinematic displacement measurements of the same subjects displayed very good test–retest reliability with intraclass correlation coefficients ranging from 0.92 to 0.96. Minimal detectable differences were calculated (standard error of the mean × 1.65 × √2) as described by Ries et al. [30]. The minimal detectable side-to-side difference (90% confidence interval) for uninvolved and involved lower extremity gluteus maximus, vastus medialis, medial hamstrings, and medial head of gastrocnemius standardized surface EMG values (propulsion-landing) were 0.18–0.19, 0.16–0.17, 0.12–0.13, and 0.18–0.19 %MVIC, respectively. 2.6. Statistical analysis Chi-square or Fisher's exact tests were used to determine categorical group differences for gender distribution, the proportion of subjects in each group whose perceived sports activity intensity or frequency differed from pre-injury values, allograft use frequency (bone-patellar tendon-bone, hamstring, or tibialis anterior), anterior knee translation laxity grade (A = ≤2 mm, B = N2–5 mm, C = N 5 mm), and IKDC Subjective Knee Survey grades (A = ≥ 90, B = 89–80, C = 79–70, D = b70). A series of one-way ANOVA and Scheffe post-hoc tests were used to evaluate continuous group demographic variables including age at surgery, time post-surgery, height, weight, IKDC Subjective Knee Form scores, IHLOC Survey scores, and sports activity participation intensity and frequency differences (follow-up level–pre-injury level). Group differences between lower extremities for standardized EMG activation amplitudes, and peak lower extremity joint displacements during single leg hop for distance testing were also evaluated using one-way ANOVA and Scheffe post-hoc tests. An alpha level of P ≤ 0.05 was selected to indicate statistical significance. All statistical analysis was performed using SPSS version 22.0 (IBM-SPSS, Armonk, NY, USA) software.
Fig. 1. Instrumented single leg hop for distance test. Retro-reflective markers enabled twodimensional kinematic data analysis during landing phase. Surface EMG electrodes positioned over the gluteus maximus, vastus medialis, medial hamstrings, and medial head of gastrocnemius muscles enabled neuromuscular activation data analysis during propulsion and landing phases.
pre-injury performance levels immediately following successful ACL reconstruction and rehabilitation (Table 1).
2.5. Global question validation, measurement reliability, and EMG minimal detectable differences Pilot testing of the simple, global question regarding perceived sports activity capability was performed among 30 subjects who only participated in the larger survey study [22] at a minimum of two years postACL reconstruction (group 1, n = 10, mean = 6.2 [95% CI = 3.4, 9] years post-surgery, group 2, n = 8, mean = 7.3 [95% CI = 4.5, 10.1] years post-surgery, and group 3, n = 9, mean = 5.1 [95% CI = 2.5, 7.7] years post-surgery. Significant IKDC Subjective Knee Form score group differences were observed between each group (96, 81.5, and 70.2, respectively, P = 0.02).
3. Results Knee palpation revealed that no subject had point tenderness or effusion at either knee at the time of testing. Subject demographic information, IKDC Subjective Knee Survey scores, IHLOC Survey scores, and perceived sports intensity and frequency changes
Table 1 Athletic activity at time of index knee injury and subjects who perceived recovery to preferred sport at pre-injury level following rehabilitation grouped by current perception of sports activity capability compared to prior to knee injury. # = subject number. Group 1 (very capable) Athletic activity at time of index knee injury American football Soccer Basketball Volleyball Skiing Baseball or softball Lacrosse Horseback riding Ice hockey Tennis
#
5 4 3 2 1 1 1 1 1 1 20
Group 2 (capable) Subjects who perceived recovery to preferred sport at pre-injury level (#)
Athletic activity at time of index knee injury
3 3 3 2 1 1 1 1 1 1
American football Skiing Basketball Physical labor Gymnastics/cheerleading Rough play Soccer Field hockey Rollerskating
17 (85%)
Group 3 (not capable) #
5 5 3 3 2 2 1 1 1
23
Subjects who perceived recovery to preferred sport at pre-injury level (#)
Athletic activity at time of index knee injury
#
Subjects who perceived recovery to preferred sport at pre-injury level (#)
4 4 3 3 2 2 0 1 1
Basketball American football Motorcycle or ATV accident Baseball or softball Volleyball Gymnastics/cheerleading Skiing Rough play Physical labor Running Bowling
4 3 3 2 2 2 2 1 1 1 1 22
3 2 3 2 2 2 1 1 1 1 1 19 (86%)
20 (87%)
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are reported in Table 2. Subjects perceived themselves to be very capable of performing sports activities (Group 1, n = 20); capable of performing sports activities (Group 2, n = 23), or not capable of performing sports activities (Group 3, n = 22). Groups displayed comparable demographic factors; however, Group 3 had significantly lower mean IKDC Subjective Knee Form scores than Group 1 (P = 0.016) and had significantly decreased perceived sports intensity level changes compared to Groups 1 and 2 (P = 0.004). Group 3 also had a higher than expected proportion of subjects that reduced their sports activity intensity by two levels at time of follow-up compared to their preinjury status (Fisher's exact test statistic = 8.8, P = 0.01). Pre-injury and follow-up sports activity frequency change differences did not display statistically significant group differences. Group comparisons for passive knee extension, passive knee flexion, anterior knee laxity, and single leg hop for distance did not display significant differences (Table 3). Although groups with higher perceived sports capability displayed greater mean single leg hop distances, significant group differences between the involved and uninvolved lower extremities were not evident (P = 0.77). Groups also displayed comparable IKDC single leg hop grade frequency distributions (Fisher's exact test = 8.0, P = 0.23), IKDC Subjective Knee Survey grade distributions (Fisher's exact test = 7.7, P = 0.25), allograft type use distributions (Fisher's exact test = 3.7, P = 0.46) and anterior knee laxity grade (Fisher's exact test statistic = 1.6, P = 0.46). Peak hip flexion, knee flexion, and ankle dorsiflexion displacements during instrumented single leg hop for distance landings also did not differ between groups (P ≥ 0.42). Involved–uninvolved lower extremity comparisons of standardized mean EMG activation amplitudes during single leg hop for distance propulsion and landing are reported in Tables 4a and 5a, respectively. During both single leg hop for distance propulsion and landing, Group 1 had increased involved lower extremity gluteus maximus and medial hamstring standardized EMG activation amplitudes compared to Group 3. Chi-square tests revealed that during both single leg hop propulsion and landing a significantly greater proportion of Group 1 subjects displayed increased involved lower extremity gluteus maximus (Tables 4b, 5b) and hamstring (Table 4c, 5c) standardized EMG amplitudes compared to Group 2 and Group 3. Post-priori statistical power calculations based on a minimum of 20 subjects/group and an alpha level of 0.05 revealed ≥0.86 statistical power (1 − β) for comparisons between Groups 1 and 3 for gluteus maximus and medial hamstring standardized EMG activation amplitude side-to-side differences, with the exception of a statistical power of 0.66 for medial hamstring standardized EMG activation amplitude during single leg hop for distance landing. Uninvolved and involved lower extremity vastus medialis and medial head of gastrocnemius EMG activation amplitude differences were comparable between groups.
4. Discussion Subjects that perceived themselves to be very capable with current sports activity function compared to prior to their knee injury had increased involved lower extremity gluteus maximus and medial hamstring muscle group neuromuscular activation during single leg hop performance. IKDC subjective knee function grades, single leg hop for distance test results and anterior knee laxity side-to-side differences and grades were comparable between groups. These findings were evident at an overall mean of N 5 years after successful ACL reconstruction and rehabilitation. These observations observed in subjects with higher perceived sports capability suggest the use of compensatory involved lower extremity neuromuscular activation to enhance single leg hop for distance test performance [34]. These compensations following successful surgery, rehabilitation, and non-impaired knee laxity that lead to most subjects being able to return to their preferred sport at their preinjury level immediately following rehabilitation may be related to a permanent neurosensory deficit at the reconstructed ACL [1,2,5–8,11], its influence on the afferent pathway and on CNS re-organization of
sensorimotor programming. With practice, patients who have undergone ACL reconstruction may become better at coping with higher level sport movements through the development of compensatory lower extremity neuromuscular activation patterns [1,2,5–8,11]. Improving our understanding of these strategies may improve the results of post-surgical and non-surgical rehabilitation and help construct new motor control learning criteria prior to advancing patients through sport specific training and eventual release back to unrestricted sport activities [4]. Perceived higher level sports capability compared to pre-knee injury status was associated with increased lower extremity neuromuscular compensations through hip muscle groups. Hip joint afferent function remains non-impaired, decreasing dependence on the sensory-impaired knee region. During maximum effort movements such as a single leg hop for distance ipsilateral hip neuromuscular activation (gluteus maximus and medial hamstrings) may be up-regulated to enable successful task performance while placing lesser dependence on local knee extensor activation [34]. With greater understanding that ACL deficiency changes afferent pathway information leading to CNS reorganization of sensorimotor programming [1,4], and ACL reconstruction restores mechanical, but not neurosensory function [2], rehabilitation should focus more on CNS re-education rather than solely attempting to optimize peripheral neuromuscular function. Rehabilitation clinicians should take greater advantage of adaptive CNS characteristics, identifying patient sports movement goals and providing guided rehabilitation exercise experiences that stimulate motor learning thereby helping the re-programmed CNS find effective solutions [1]. This may be especially important during the latter stages of rehabilitation and during return to sport-specific training. Criteria-based neuromuscular re-training programs directed at motivated patients may improve functional lower extremity extensor muscle balance between the hip, knee and ankle joints at the involved lower extremity following ACL reconstruction [14,25,28]. However, given that grafts used for ACL reconstruction (allograft or autograft) do not restore native ACL neurosensory properties it is unlikely that a long-term restoration to premorbid sensorimotor relationships can be achieved [1,2,5–8, 11]. As patients learn to cope with progressively more challenging sports movement tasks in the presence of modified afferent information during rehabilitation and following return to play they may begin to develop more effective use of compensatory lower extremity extensor neuromuscular activation through the hip. 5. Study limitations This study has several important limitations. Asking subjects to recall their perception of whether or not they successfully returned to their preferred sport at their pre-injury level following surgery and rehabilitation at approximately five years post-surgery may have led to recall bias. Some subjects may have either over- or under-estimated their true performance capability [35]. To minimize the potential influence of excessive anterior knee laxity on lower extremity neuromuscular activation amplitudes of the 70 subjects who agreed to participate,
Table 2 Subject demographic data, IKDC Subjective Knee Survey score, Internal Health Locus of Control Survey score, and perceived sports activity intensity and frequency change comparison by perceived sports involvement level group. Mean [95% confidence interval]. * = P b 0.05.
Gender (#, % men) Age at surgery (yrs) Time post-surgery (yrs) Height (cm) Weight (kg) IKDC subjective knee survey score Internal health locus of control survey score Perceived sports activity intensity change (current–pre-injury) Perceived sports activity frequency change (current–pre-injury)
Group 1
Group 2
Group 3
P
20, 50% 26.5 [21.9, 31.8] 4.6 [2.8, 6.2] 176.5 [170.4, 180.1] 76.8 [67.4, 80.3] 91.0 [84.1, 94.6] 28.8 [25.0, 30.9] −0.35 [−0.77, −0.10] −0.30 [−0.77, −0.10]
23, 52.2% 29.3 [24.1, 34.4] 5.4 [4.2, 6.6] 172.8 [168.4, 177.3] 76.8 [68.3, 85.2] 87.2 [82.1, 92.4] 26.7 [24.1, 29.2] −0.41 [−0.67, −0.15] −0.54 [−0.90, −0.19]
22, 45.5% 33.6 [26.4, 39.1] 5.2 [3.8, 6.5] 172.1 [167.1, 177.1] 79.7 [68.0, 91.3] 78.6 [71.7, 85.5] 24.9 [22.0, 27.7] −1.10 [−1.6, −0.65] −0.60 [−1.0, −0.25]
0.95 0.20 0.56 0.38 0.86 0.016* (Groups 1 N 3) 0.44 0.004* Groups 1,2 N 3) 0.56
Table 3 Clinical examination results. Uninvolved–involved lower extremity for passive knee extension and flexion difference; involved–uninvolved lower extremity for knee laxity and single leg hop for distance differences. Mean [95% confidence interval]. UI = uninvolved lower extremity. I = involved lower extremity. Diff. = difference. Mean [95% confidence interval]. Group 1
Knee extension (°) Knee flexion (°) Knee laxity (mm) Single-leg hop for distance (m)
Group 2
Group 3
UI
I
Diff.
UI
I
Diff.
UI
I
Diff.
P
1.9 [−0.1, 3.2] 143.6 [142, 147.4] 5.4 [4.6, 6.8] 1.27 [1.13, 1.51]
1.2 [−0.7, 2.2] 142.1 [140.1, 146.4] 6.7 [5.7, 7.9] 1.27 [1.14, 1.48]
0.7 [−0.5, 2.7] 1.5 [−0.4, 4.2] 1.3 [−0.2, 1.6] 0.0 [−0.9, 1.1]
1.8 [0.4, 3.1] 143.0 [138.9, 147] 5.4 [4.4, 6.5] 1.06 [0.85, 1.26]
0.9 [−0.6, 2.1] 139.0 [135.2, 142.8] 6.9 [5.9, 7.8] 1.10 [0.91, 1.29]
0.9 [−0.2, 1.0] 4.0 [1.0, 7.5] 1.5 [0.9, 2.4] 0.04 [−0.9, 1.0]
2.6 [1.2, 3.3] 139.7 [135.8, 143.8] 5.4 [4.3, 6.5] 0.95 [0.79, 1.11]
1.9 [0.5, 3.3] 137.3 [132.9, 142.4] 7. 0 [5.9, 8.2] 0.82 [0.67, 0.97]
0.7 [−0.7, 1.7] 2.4 [−1.0, 6.9] 1.6 [0.5, 2.4] −0.13 [−0.8, 1.1]
0.78 0.82 0.25 0.77
Table 4a Group 1
GM VM MH G
Group 2
J. Nyland et al. / The Knee 21 (2014) 1191–1197
Table 4 Standardized EMG amplitudes during single leg hop for distance propulsion [%MVIC involved lower extremity − %MVIC uninvolved lower extremity]. GM = gluteus maximus, VM = vastus medialis, MH = medial hamstrings, G = gastrocnemius. * = P b 0.05.
Group 3
UI
I
Difference
UI
I
Difference
UI
I
Difference
P
0.97 [0.87, 1.07] 1.31 [1.13, 1.48] 0.77 [0.62, 0.93] 1.32 [1.01, 1.42]
1.2 [1.02, 1.32] 1.21 [1.13, 1.46] 0.91 [0.76, 1.05] 1.38 [1.28, 1.48]
0.23 [0.07, 0.40] −0.1 [−0.42, 0.21] 0.14 [−0.08, 0.36] 0.06 [−0.19, 0.30]
0.98 [0.90, 1.06] 1.36 [1.21, 1.51] 1.08 [0.79, 1.05] 1.20 [1.11, 1.28]
1.1 [1.07, 1.23] 1.16 [1.02, 1.3] 1.16 [1.04, 1.29] 1.29 [1.21, 1.37]
0.12 [−0.08, 0.26] −0.2 [−0.60, 0.13] 0.08 [−0.17, 0.30] 0.09 [−0.08, 0.29]
1.09 [0.99, 1.19] 1.51 [1.34, 1.69] 1.27 [1.12, 1.43] 1.30 [1.2, 1.41]
1.00 [0.79, 1.15] 1.45 [1.28, 1.62] 0.97 [0.82, 1.12] 1.18 [1.09, 1.28]
−0.09 [−0.31, 0.11] −0.06 [−0.33, 0.19] −0.3 [−0.63, −0.07] −0.12 [−0.30, 0.05]
Group 1 N 3, P = 0.036* 0.72 Group 1 N 3, P = 0.011* 0.20
Table 4b
Increased gluteus maximus activation amplitude at involved lower extremity No change or decreased gluteus maximus activation amplitude at the involved lower extremity
Group 1
Group 2
Group 3
Total
16 [11.4]* 4 [8.6] 20
13 [13.1] 10 [9.9] 23
8 [12.5] 14 [9.5] 22
37 [37] 28 [28] 65 [65]
11 [7.7]* 9 [12.3] 20
10 [8.8] 13 [14.2] 23
4 [8.5] 18 [13.5] 22
25 [25] 40 [40] 65 [65]
Chi-Square = 8.1, P = 0.019* Table 4c Increased hamstring activation amplitude at involved lower extremity No change or decreased hamstring activation amplitude at the involved lower extremity
1195
Chi-Square = 6.4, P = 0.041*
only those with a negative pivot shift test or ≤4 mm side-to-side anterior knee laxity difference were included in this analysis. Therefore, 5 subjects that demonstrated a positive pivot shift test were eliminated from statistical analysis, leaving 65 subjects out of a pool of 206 subjects who responded to the survey arm of the study [22]. The initial survey study sample consisted of 335 consecutive former patients. Although the subjects who participated in this study phase displayed similar demographics to the overall subject pool the possibility of selection and/or sampling bias exists [35,36]. Additionally, the post-test design used in this prospective study relied on the opposite lower extremity as a control. Ideally, a separate healthy, age-matched control group or an otherwise healthy group of ACL deficient patients would have been included in the study design. Clinical lower extremity functional performance tests such as single leg hop for distance testing however generally rely on comparisons with the contralateral, uninjured lower extremity [19,27,29,37,38]. This study only evaluated the single leg hop for distance. Other functional tests should be considered with future research in this area [21], using a longitudinal design and repeated measures that evaluate changes throughout early and late rehabilitation, sport specific training, and return to sport phases. Thigh girth measurements were not performed in this study. Thigh girth measurements may have provided additional insight regarding subject thigh muscle mass and the magnitude of fast twitch muscle fiber atrophy. However, without supporting cross-sectional magnetic resonance imaging to ascertain lean versus fat tissues it would have been difficult to accurately delineate muscle volume. Additionally, this study represents a small subject group consisting of former patients who had their ACL reconstructed by the same fellowship trained knee surgeon using exclusively allograft tissue. Therefore these results may not generalize to other populations. Use of allograft tissue however negates the potential influence of autogenous tendon harvest for ACL graft harvest on quadriceps femoris or hamstring muscle group function and screening to ensure the absence of a positive pivot shift test or excessive side-to-side anterior knee laxity differences minimized the influence of laxity on study findings. Another study limitation is use of two-dimensional sagittal kinematic analysis. Although three-dimensional kinematic analysis would have provided more accurate depictions of lower extremity joint movements, two-dimensional analysis remains useful and clinically practical as a screening tool for primarily uniplanar movements such as single leg hop for distance testing. Lastly, neither ground reaction force nor inverse dynamic moment analysis was performed. This addition would have provided a more comprehensive representation of lower extremity joint contributions to single leg hop for distance test performance.
4 [8.5] 18 [13.5] 22 [22]
25 [25] 40 [40] 65 [65]
37 [37] 28 [28] 65 [65]
9 [8.8] 14 [14.2] 23 [23]
10 [12.5] 12 [9.5] 22 [22]
6. Conclusion Lower extremity neuromuscular compensations suggesting a hip bias with increased gluteus maximus and medial hamstring activation was identified at the involved lower extremity among most subjects who perceived high perceived sports capability compared to preinjury status. These compensations may be related to a permanent neurosensory deficit, and its influence on afferent pathway changes that influence CNS sensorimotor re-organization. Further prospective, longitudinal research is needed. Chi-square = 7.7, P = 0.021
12 [7.7] 8 [12.3] 20 [20] Table 5c
Chi-square = 6.3, P = 0.048
Increased hamstring activation amplitude at involved lower extremity No change or decreased hamstring activation amplitude at the involved lower extremity
11 [13.1] 12 [9.9] 23 [23] 16 [11.4] 4 [8.6] 20 [20]
Group 2 Group 1 Table 5b
1.61 [1.47, 1.89] 1.31 [1.20, 1.50] 1.50 [1.32, 1.69] 1.28 [1.17, 1.39]
Increased gluteus maximus activation amplitude at involved lower extremity No change or decreased gluteus maximus activation amplitude at the involved lower extremity
Total
Group 1 N 3, P = 0.041* 0.80 Group 1 N 3, P = 0.023* 0.26
Group 3
P Difference
1.14 [0.90, 1.39] 1.63 [1.45, 1.80] 1.23 [1.01, 1.44] 1.25 [1.12, 1.39]
UI
1.37 [1.18, 1.69] 1.58 [1.40, 1.77] 1.6 [1.51, 2.08] 1.32 [1.18, 1.46] 1.33 [1.06, 1.49] 1.46 [1.29, 1.60] 1.36 [1.17, 1.55] 1.26 [1.15, 1.38] 0.37 [−0.08, 0.82] −0.13 [−.46, 0.21] 0.12 [−0.20, 0.44] 0.23 [−0.06, 0.53] 1.51 [1.36, 1.83] 1.39 [1.21, 1.55] 1.17 [0.97, 1.39] 1.23 [1.17, 1.54] 1.14 [0.88, 1.39] 1.52 [1.20, 1.57] 1.05 [0.84, 1.30] 1.00 [0.86, 1.14] GM VM MH G
I UI
Group 1
0.28 [−0.18, 0.34] −0.15 [−0.46, 0.16] −0.16 [−0.51, 0.19] 0.02 [−0.27, 0.31]
Group 3
UI
Difference Group 2
Difference I
I
−0.23 [−0.42, 0.06] 0.05 [−0.28, 0.22] −0.37 [−1.11, −0.17] −0.07 [−0.44, 0.21]
J. Nyland et al. / The Knee 21 (2014) 1191–1197
Table 5a
Table 5 Standardized EMG amplitudes during single leg hop for distance landing [%MVIC involved lower extremity − %MVIC uninvolved lower extremity]. GM = gluteus maximus, VM = vastus medialis, MH = medial hamstrings, G = gastrocnemius. Mean [95% confidence interval]. * = P b 0.05.
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J. Nyland et al. / The Knee 21 (2014) 1191–1197 [4] Kapreli E, Athanasopoulos S. The anterior cruciate ligament deficiency as a model of brain plasticity. Med Hypotheses 2006;67:645–50. [5] Courtney C, Rine RM, Kroll P. Central somatosensory changes and altered muscle synergies in subjects with anterior cruciate ligament deficiency. Gait Posture 2005; 22:69–74. [6] Courtney CA, Rine RM. Central somatosensory changes associated with improved dynamic balance in subjects with anterior cruciate ligament deficiency. Gait Posture 2006;24:190–5. [7] Baumeister J, Reinecke K, Weiss M. Changed cortical activity after anterior cruciate ligament reconstruction in a joint position paradigm: an EEG study. Scand J Med Sci Sports 2008;18:473–84. [8] Baumeister J, Reinecke K, Schubert M, Weiss M. Altered electrocortical brain activity after ACL reconstruction during force control. J Orthop Res 2011;29:1383–9. [9] Johansson H, Sjolander P, Sojka P. A sensory role for the cruciate ligaments. Clin Orthop Relat Res 1991;268:161–78. [10] Nyland J, Fisher B, Brand E, Krupp R, Caborn DN. Osseous deficits after anterior cruciate ligament injury and reconstruction: a systematic review with suggestions to improve osseous homeostasis. Arthroscopy 2010;26:1248–57. [11] Nyland J, Klein S, Caborn DN. Lower extremity compensatory neuromuscular and biomechanical adaptations 2 to 11 years after anterior cruciate ligament reconstruction. Arthroscopy 2010;26:1212–25. [12] Paterno MV, Ford KR, Myer GD, Heyl R, Hewett TE. Limb asymmetries in landing and jumping 2 years following anterior cruciate ligament reconstruction. Clin J Sports Med 2007;17:258–62. [13] Wojtys EM, Huston LJ. Longitudinal effects of anterior cruciate ligament injury and patellar tendon autograft reconstruction on neuromuscular performance. Am J Sports Med 2000;28:336–44. [14] Eastlack ME, Axe MJ, Snyder-Mackler L. Laxity, instability, and functional outcome after ACL injury: copers versus noncopers. Med Sci Sports Exerc 1999;31:210–5. [15] McHugh MP, Tyler TF, Nicholas SJ, Browne MG, Gleim GW. Electromyographic analysis of quadriceps fatigue after anterior cruciate ligament reconstruction. J Orthop Sports Phys Ther 2001;31:25–32. [16] McHugh MP, Tyler TF, Browne MG, Gleim GW, Nicholas SJ. Electromyographic predictors of residual quadriceps muscle weakness after anterior cruciate ligament reconstruction. Am J Sports Med 2002;30:334–9. [17] Risberg MA, Moksnes H, Storevold A, Holm I, Snyder-Mackler L. Rehabilitation after anterior cruciate ligament injury influences joint loading during walking but not hopping. Br J Sports Med 2009;43:423–8. [18] Orishimo KF, Kremenic IJ, Mullaney MJ, McHugh MP, Nicholas SJ. Adaptations in single-leg hop biomechanics following anterior cruciate ligament reconstruction. Knee Surg Sports Traumatol Arthrosc 2010;18:1587–93. [19] Barber SD, Noyes FR, Mangine RE, McCloskey JW, Hartman W. Quantitative assessment of functional limitations in normal and anterior cruciate ligament-deficient knees. Clin Orthop Relat Res 1990;255:204–14. [20] Engelen-van Melick N, van Cingel RE, Tijssen MP, Nijhuis-van der Sanden MW. Assessment of functional performance after anterior cruciate ligament reconstruction: a systematic review of measurement procedures. Knee Surg Sports Traumatol Arthrosc 2012;21:869–79.
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[21] Eitzen I, Moksnes H, Snyder-Mackler L, Engebretsen L, Risberg MA. Functional tests should be accentuated more in the decision for ACL reconstruction. Knee Surg Sports Traumatol Arthrosc 2010;18:1517–25. [22] Harreld K, Nyland J, Cottrell B, Caborn D. Self-reported patient outcomes after ACL reconstruction with allograft tissue. Med Sci Sports Exerc 2006;38:2058–67. [23] Nyland J, Cottrell B, Harreld K, Caborn DNM. Self-reported outcomes after anterior cruciate ligament reconstruction: an internal health locus of control score comparison. Arthroscopy 2006;22:1225–32. [24] Gokeler AHA, Arnold MP, Dijkstra PU, Postema K, Otten E. Abnormal landing strategies after ACL reconstruction. Scand J Med Sci Sports 2010;20:e12–9. [25] Schmitt LC, Paterno MV, Hewett TE. The impact of quadriceps femoris strength asymmetry on functional performance at return to sport following anterior cruciate ligament reconstruction. J Orthop Sports Phys Ther 2012;42:750–9. [26] Kocher MS, Steadman JR, Briggs KK, Sterett WI, Hawkins RJ. Relationships between objective assessment of ligament stability and subjective assessment of symptoms and function after anterior cruciate ligament reconstruction. Am J Sports Med 2004;32:629–34. [27] Barber-Westin SD, Noyes FR. Factors used to determine return to unrestricted sports activities after anterior cruciate ligament reconstruction. Arthroscopy 2011; 27:1697–705. [28] Myer GD, Martin Jr L, Ford KR, Paterno MV, Schmitt LC, Heidt Jr RS, et al. No association of time from surgery with functional deficits in athletes after anterior cruciate ligament reconstruction: evidence of objective return-to-sport criteria. Am J Sports Med 2012;40:2256–63. [29] Reid A, Birmingham TB, Stratford PW, Alcock GK, Giffin JR. Hop testing provides a reliable and valid outcome measure during rehabilitation after anterior cruciate ligament reconstruction. Phys Ther 2007;87:337–49. [30] Ries JD, Echternach JL, Nof L, Gagnon Blodgett M. Test–retest reliability and minimal detectable change scores for the timed “up & go” test, the six-minute walk test, and gait speed in people with Alzheimer disease. Phys Ther 2009;89:569–79. [31] Steptoe A, Wardle J. Locus of control and health behavior revisited: a multivariate analysis of young adults from 18 countries. Brit J Psychol 2001;92:659–72. [32] Wallston KA. The validity of the multidimensional health locus of control scales. J Health Psychol 2005;10:623–31. [33] Irrgang JJ, Anderson AF, Boland AL, Harner CD, Kurosaka M, Neyret P, et al. Development and validation of the International Knee Documentation Committee Subjective Knee Form*. Am J Sports Med 2001;29:600–13. [34] Brughelli M, Cronin J, Mendiguchia J, Kinsella D, Nosaka K. Contralateral leg deficits in kinetic kinematic variables during running in Australian rules football players with previous hamstring injuries. J Strength Cond Res 2010;24:2539–44. [35] Sica GT. Bias in research studies. Radiology 2006;238:780–9. [36] Pannucci CJ, Wilkins EG. Identifying and avoiding bias in research. Plast Reconstr Surg 2010;126:619–25. [37] Derr J. Valid paired data designs: make full use of data without “double dipping”. J Orthop Sports Phys Ther 2006;36:42–4. [38] Van der Harst JJ, Gokeler A, Hof AL. Leg kinematics and kinetics in landing from a single-leg hop for distance. A comparison between dominant and non-dominant leg. Clin Biomech 2007;22:674–80 [Bristol, Avon].
Contents lists available at ScienceDirect
The Knee
Lower extremity neuromuscular compensations during instrumented single leg hop testing 2–10 years following ACL reconstruction John Nyland ⁎, Jeff Wera, Scott Klein, David N.M. Caborn Division of Sports Medicine, Department of Orthopaedic Surgery, University of Louisville, United States Athletic Training Program, Spalding University, 901 South 4th Street, Louisville, KY 40203-2188, United States
a r t i c l e
i n f o
Article history: Received 26 September 2013 Received in revised form 28 May 2014 Accepted 21 July 2014 Keywords: Electromyography Dynamic postural stability Allograft Perceived function Knee
a b s t r a c t Background: This study compared lower extremity EMG activation and sagittal plane kinematics of subjects at a minimum of 2 years post-successful ACL reconstruction and rehabilitation during instrumented single leg hop testing. Methods: Comparisons were made based on subject responses to the following question, “compared to prior to your knee injury how capable are you now in performing sports activities”? Group 1 = very capable, Group 2 = capable, and Group 3 = not capable. In addition to EMG (1000 Hz) and kinematic (60 Hz) data, subjective knee function, internal health locus of control, sports activity characteristics (intensity, frequency) pre-knee injury, and at follow-up were also compared. Results: Group 3 had lower perceived knee function, decreased perceived sports intensity, and more subjects with decreased sports activity intensity by two levels compared to pre-injury values. Perceived function scores, anterior laxity measurements and grades were similar between groups. During single leg hop propulsion and landing Group 1 (very capable) had greater involved lower extremity gluteus maximus and medial hamstring activation amplitudes than Group 3 (not capable). Perceived sports capability was related to better subjective knee function, and higher perceived sports activity intensity. Conclusion: Neuromuscular compensations suggesting a hip bias with increased gluteus maximus and medial hamstring activation were identified at the involved lower extremity among most subjects who perceived high perceived sports capability compared to pre-injury status. These compensations may be related to a permanent neurosensory deficit, and its influence on afferent pathway changes that influence CNS sensorimotor re-organization. © 2014 Elsevier B.V. All rights reserved.
1. Introduction No matter how well documented the functional deficits associated with ACL deficiency are, the etiologic factors have not been clarified [1]. There is growing evidence that supports the concept that in addition to mechanical deficiency, ACL rupture represents a de-afferentation injury that may lead to changes in ascending afferent pathway information leading to central nervous system (CNS) re-organization of sensorimotor programming [2–9]. The CNS has the capacity to adapt according to the stimulus it receives from the ascending afferent pathways. The ability of the brain to undergo any enduring morphological or functional cortical property re-organization is referred to as plasticity or neuroplasticity [1,4]. Although mechanical function is largely restored following surgical reconstruction, since neurosensory function is not re-established, ACL injury may influence lower extremity neuromuscular activation long after successful surgical reconstruction and rehabilitation [10–13]. ⁎ Corresponding author. Tel.: +1 502 873 4224; fax: +1 502 585 7149. E-mail address: [email protected] (J. Nyland).
http://dx.doi.org/10.1016/j.knee.2014.07.017 0968-0160/© 2014 Elsevier B.V. All rights reserved.
In studies of ACL deficient subjects and subjects following ACL injury and reconstruction, Valeriani et al. [2,3] identified altered somatosensory evoked potentials in a number of patients suggesting that ACL rupture lead to changes in ascending afferent pathway information and CNS re-organization. They suggested that deafferentation from ACL rupture could not be replaced by input from other knee joint somatosensory input or by the mechanical stability provided by reconstructive surgery [2]. In a study of 17 subjects with ACL deficiency, Courtney et al. [5] suggested that reduced knee proprioception was related to CNS re-organization of sensorimotor programming that facilitated motor program modifications to produce more efficient lower extremity neuromuscular activation synergies during gait. In a followup study they reported that ACL deficient subjects, who did not have impaired strength, resumed pre-injury function via altered lower extremity neuromuscular synergies and somatosensory evoked potentials [6]. In an electroencephalography study of 10 patients at N 1 year post-ACL reconstruction, Baumeister et al. [7] reported greater cortical activation in the parietal brain regions compared to healthy control subjects during a knee angle re-production task suggesting a greater need for focused attention to achieve effective task performance. In a later
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study comparing nine patients following ACL reconstruction with nine health control subjects they reported that the ACL reconstruction group required greater attentional control brain activation to reproduce 50% maximum voluntary quadriceps femoris isometric contraction forces at 90° knee flexion [8]. In a functional MRI study comparing the brain activation of 18 healthy volunteers with 17 subjects with chronic ACL deficiency, Kapreli et al. [1] reported that the ACL deficient subject group had diminished activation in several sensorimotor cortical areas and increased activation in the contralateral pre-supplementary motor area, contralateral posterior somatosensory area, and the ipsilateral posterior inferior temporal gyrus compared to the control group. They concluded that a likely explanation for this CNS re-organization of sensorimotor programming was the establishment of neurophysiologic changes in the ACL injury group [1]. Lower extremity neuromuscular extensor function, particularly at the quadriceps femoris, is compromised following ACL injury and reconstruction [14–17]. This impairs its ability to effectively attenuate impact forces, increasing knee injury or re-injury risk [16–18]. Since landing from a single leg hop for distance places high demands on the lower extremity extensor musculature to absorb sudden impact forces, this test is a widely-used clinical method for evaluating function following knee injury or surgery prior to release to sports [18–21]. The purpose of this component of a larger study [11,22,23] was to compare the involved and uninvolved lower extremity EMG activation amplitudes and sagittal plane kinematics of subjects at a minimum of two years post-successful ACL reconstruction and rehabilitation, during instrumented single leg hop for distance testing, and compare these findings by subject perceived sports capability level. Subjective knee function, internal health locus of control (IHLOC) and sports activity characteristics (intensity, frequency) pre-knee injury, and at time of follow-up were also compared. Based on previous work [11] and the work of others [1–3,5–9,24,25], the hypothesis was that lower extremity neuromuscular activation during single leg hop for distance testing would differ between the lower extremity that had undergone successful ACL reconstruction and rehabilitation and the uninvolved contralateral lower extremity between groups of differing perceived sports capability compared to pre-injury status. 2. Methods 2.1. Experimental design This was an evidence level IV therapeutic case series. 2.2. Subjects From a group of 206 potential subjects who responded to the survey portion of a larger study [11,22,23], 70 subjects (35 men, 35 women) agreed to participate in this clinical phase. To control for the possible influence of knee laxity on lower extremity neuromuscular activation, subjects who displayed a positive pivot shift glide [26] or a side-toside anterior translation knee laxity difference N4 mm were not included in this comparison decreasing the subject number to 65 (32 men, 33 women) subjects at 5.2 ± 2.9 years post-surgery. Subjects that participated in this clinical phase otherwise met the inclusion criteria of the survey study [22]. Medical institutional research review board approval was obtained, and subjects provided written informed consent. A minimum of two years had passed since subjects underwent unilateral primary ACL reconstruction with allograft tissue performed by the senior author using transtibial tunnel drilling and bioabsorbable interference screw fixation. Former patients who had undergone meniscal debridement, partial meniscectomy or meniscal repair (approximately 62%), or who had grade I to III chondral injury at the medial or lateral femoral condyle (approximately 10%) were allowed to participate. Patients who had a posterior cruciate ligament injury, had undergone collateral ligament surgery, had an impaired contralateral knee, or who had not
adhered to the standardized progressive rehabilitation program were excluded from study participation. Surgical intervention details and rehabilitation program functional milestone timetable information have been previously reported [11]. Review of medical charts and physical therapy records revealed that all subjects had complied with rehabilitation program recommendations and all had met or exceeded standard accepted return-to-sports activity goals of a minimum 85% bilateral equivalence with single leg hop for distance testing and 60°/s isokinetic peak knee extensor and flexor torque testing prior to release from care [12,19,27,28]. 2.3. Data collection procedures Clinical examination included knee joint palpation, passive knee range-of-motion assessment using a handheld goniometer, and anterior translational knee arthrometric testing at 133.4 N (KT-1000; MEDmetric, San Diego, CA, USA). Electromyographic (4-channel, MyoSystem 1200; Noraxon, Scottsdale, AZ, USA; 1000 Hz), and two-dimensional sagittal plane kinematic (SIMI Motion 2D, Unterschleissheim, Germany; 60 Hz) data were collected during single leg hop for distance testing. Gluteus maximus, vastus medialis, medial hamstrings and medial head of gastrocnemius EMG activation amplitudes were standardized to levels attained during single repetition, maximal volitional effort isometric contractions (%MVIC). Additional details regarding EMG data collection and analysis methods have been previously reported [11]. The primary investigator performed the clinical evaluation and administered all tests. Lower extremity test order was alternated between subjects to control for potential order effects. Passive knee flexion range of motion was evaluated with subjects in prone. Passive knee extension range of motion was evaluated with subjects in supine. In both cases subjects actively flexed or extended their knee as far as possible. Following this the primary investigator applied a slight pressure (approximately 22 N) to assure that complete range of motion was achieved. Prior to single leg hop for distance testing subjects performed two practice trials with each lower extremity. Only two practice trials were performed prior to data collection as all subjects had previous familiarity with test procedures. Testing was performed with unrestricted upper extremity movements using previously reported techniques [29]. Retro-reflective markers were secured over the shoe of the test lower extremity to depict the head of the fifth metatarsal, 2 cm distal to the protuberance of the lateral malleolus, over the joint line of the lateral knee, over gym shorts depicting the greater trochanter of the femur, and over the spinous process of the third lumbar vertebrae. Following practice subjects performed three test trials with each lower extremity (Fig. 1). A 3 m long by 2 m tall calibration space was used for hip, knee, and ankle kinematic displacement measurement calculations at single leg hop for distance landing. Following marker digitization and tracking, marker paths were smoothed once using a low-pass digital filter. Peak displacement of the hip, knee, and ankle was measured manually by the primary investigator using a software curser function. Sports activity participation level intensity and frequency prior to ACL injury and at time of follow-up were measured using the Knee Outcome Survey Sports Activity Scale [11,22] and IHLOC was measured using Multidimensional Health Locus of Control Survey Form C scores [23,31,32]. The International Knee Documentation Committee (IKDC) Subjective Knee Form was used to determine perceived knee function [33]. 2.4. Subject grouping Subject group assignments were made based on how they responded to the following question: “Compared to prior to your knee injury how capable are you now in performing sports activities”, very capable (group 1), capable (group 2), or not capable (group 3)? Most study subjects perceived that they had returned back to their preferred sport at
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Pilot testing of 6 subjects (3 men, 3 women) with similar demographics as study subjects (very capable = 2, capable = 2, not capable = 2) revealed that surface EMG measurements had excellent test–retest reliability with intraclass correlation coefficients of 0.95–0.99 with comparable reliability noted for both single leg hop for distance test propulsion and landing phases. Intra-rater test–retest reliability for passive knee range of motion measurements of the same subjects by the primary investigator using a handheld goniometer was 0.95 for knee extension and 0.97 for knee flexion. Two-dimensional sagittal plane kinematic displacement measurements of the same subjects displayed very good test–retest reliability with intraclass correlation coefficients ranging from 0.92 to 0.96. Minimal detectable differences were calculated (standard error of the mean × 1.65 × √2) as described by Ries et al. [30]. The minimal detectable side-to-side difference (90% confidence interval) for uninvolved and involved lower extremity gluteus maximus, vastus medialis, medial hamstrings, and medial head of gastrocnemius standardized surface EMG values (propulsion-landing) were 0.18–0.19, 0.16–0.17, 0.12–0.13, and 0.18–0.19 %MVIC, respectively. 2.6. Statistical analysis Chi-square or Fisher's exact tests were used to determine categorical group differences for gender distribution, the proportion of subjects in each group whose perceived sports activity intensity or frequency differed from pre-injury values, allograft use frequency (bone-patellar tendon-bone, hamstring, or tibialis anterior), anterior knee translation laxity grade (A = ≤2 mm, B = N2–5 mm, C = N 5 mm), and IKDC Subjective Knee Survey grades (A = ≥ 90, B = 89–80, C = 79–70, D = b70). A series of one-way ANOVA and Scheffe post-hoc tests were used to evaluate continuous group demographic variables including age at surgery, time post-surgery, height, weight, IKDC Subjective Knee Form scores, IHLOC Survey scores, and sports activity participation intensity and frequency differences (follow-up level–pre-injury level). Group differences between lower extremities for standardized EMG activation amplitudes, and peak lower extremity joint displacements during single leg hop for distance testing were also evaluated using one-way ANOVA and Scheffe post-hoc tests. An alpha level of P ≤ 0.05 was selected to indicate statistical significance. All statistical analysis was performed using SPSS version 22.0 (IBM-SPSS, Armonk, NY, USA) software.
Fig. 1. Instrumented single leg hop for distance test. Retro-reflective markers enabled twodimensional kinematic data analysis during landing phase. Surface EMG electrodes positioned over the gluteus maximus, vastus medialis, medial hamstrings, and medial head of gastrocnemius muscles enabled neuromuscular activation data analysis during propulsion and landing phases.
pre-injury performance levels immediately following successful ACL reconstruction and rehabilitation (Table 1).
2.5. Global question validation, measurement reliability, and EMG minimal detectable differences Pilot testing of the simple, global question regarding perceived sports activity capability was performed among 30 subjects who only participated in the larger survey study [22] at a minimum of two years postACL reconstruction (group 1, n = 10, mean = 6.2 [95% CI = 3.4, 9] years post-surgery, group 2, n = 8, mean = 7.3 [95% CI = 4.5, 10.1] years post-surgery, and group 3, n = 9, mean = 5.1 [95% CI = 2.5, 7.7] years post-surgery. Significant IKDC Subjective Knee Form score group differences were observed between each group (96, 81.5, and 70.2, respectively, P = 0.02).
3. Results Knee palpation revealed that no subject had point tenderness or effusion at either knee at the time of testing. Subject demographic information, IKDC Subjective Knee Survey scores, IHLOC Survey scores, and perceived sports intensity and frequency changes
Table 1 Athletic activity at time of index knee injury and subjects who perceived recovery to preferred sport at pre-injury level following rehabilitation grouped by current perception of sports activity capability compared to prior to knee injury. # = subject number. Group 1 (very capable) Athletic activity at time of index knee injury American football Soccer Basketball Volleyball Skiing Baseball or softball Lacrosse Horseback riding Ice hockey Tennis
#
5 4 3 2 1 1 1 1 1 1 20
Group 2 (capable) Subjects who perceived recovery to preferred sport at pre-injury level (#)
Athletic activity at time of index knee injury
3 3 3 2 1 1 1 1 1 1
American football Skiing Basketball Physical labor Gymnastics/cheerleading Rough play Soccer Field hockey Rollerskating
17 (85%)
Group 3 (not capable) #
5 5 3 3 2 2 1 1 1
23
Subjects who perceived recovery to preferred sport at pre-injury level (#)
Athletic activity at time of index knee injury
#
Subjects who perceived recovery to preferred sport at pre-injury level (#)
4 4 3 3 2 2 0 1 1
Basketball American football Motorcycle or ATV accident Baseball or softball Volleyball Gymnastics/cheerleading Skiing Rough play Physical labor Running Bowling
4 3 3 2 2 2 2 1 1 1 1 22
3 2 3 2 2 2 1 1 1 1 1 19 (86%)
20 (87%)
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are reported in Table 2. Subjects perceived themselves to be very capable of performing sports activities (Group 1, n = 20); capable of performing sports activities (Group 2, n = 23), or not capable of performing sports activities (Group 3, n = 22). Groups displayed comparable demographic factors; however, Group 3 had significantly lower mean IKDC Subjective Knee Form scores than Group 1 (P = 0.016) and had significantly decreased perceived sports intensity level changes compared to Groups 1 and 2 (P = 0.004). Group 3 also had a higher than expected proportion of subjects that reduced their sports activity intensity by two levels at time of follow-up compared to their preinjury status (Fisher's exact test statistic = 8.8, P = 0.01). Pre-injury and follow-up sports activity frequency change differences did not display statistically significant group differences. Group comparisons for passive knee extension, passive knee flexion, anterior knee laxity, and single leg hop for distance did not display significant differences (Table 3). Although groups with higher perceived sports capability displayed greater mean single leg hop distances, significant group differences between the involved and uninvolved lower extremities were not evident (P = 0.77). Groups also displayed comparable IKDC single leg hop grade frequency distributions (Fisher's exact test = 8.0, P = 0.23), IKDC Subjective Knee Survey grade distributions (Fisher's exact test = 7.7, P = 0.25), allograft type use distributions (Fisher's exact test = 3.7, P = 0.46) and anterior knee laxity grade (Fisher's exact test statistic = 1.6, P = 0.46). Peak hip flexion, knee flexion, and ankle dorsiflexion displacements during instrumented single leg hop for distance landings also did not differ between groups (P ≥ 0.42). Involved–uninvolved lower extremity comparisons of standardized mean EMG activation amplitudes during single leg hop for distance propulsion and landing are reported in Tables 4a and 5a, respectively. During both single leg hop for distance propulsion and landing, Group 1 had increased involved lower extremity gluteus maximus and medial hamstring standardized EMG activation amplitudes compared to Group 3. Chi-square tests revealed that during both single leg hop propulsion and landing a significantly greater proportion of Group 1 subjects displayed increased involved lower extremity gluteus maximus (Tables 4b, 5b) and hamstring (Table 4c, 5c) standardized EMG amplitudes compared to Group 2 and Group 3. Post-priori statistical power calculations based on a minimum of 20 subjects/group and an alpha level of 0.05 revealed ≥0.86 statistical power (1 − β) for comparisons between Groups 1 and 3 for gluteus maximus and medial hamstring standardized EMG activation amplitude side-to-side differences, with the exception of a statistical power of 0.66 for medial hamstring standardized EMG activation amplitude during single leg hop for distance landing. Uninvolved and involved lower extremity vastus medialis and medial head of gastrocnemius EMG activation amplitude differences were comparable between groups.
4. Discussion Subjects that perceived themselves to be very capable with current sports activity function compared to prior to their knee injury had increased involved lower extremity gluteus maximus and medial hamstring muscle group neuromuscular activation during single leg hop performance. IKDC subjective knee function grades, single leg hop for distance test results and anterior knee laxity side-to-side differences and grades were comparable between groups. These findings were evident at an overall mean of N 5 years after successful ACL reconstruction and rehabilitation. These observations observed in subjects with higher perceived sports capability suggest the use of compensatory involved lower extremity neuromuscular activation to enhance single leg hop for distance test performance [34]. These compensations following successful surgery, rehabilitation, and non-impaired knee laxity that lead to most subjects being able to return to their preferred sport at their preinjury level immediately following rehabilitation may be related to a permanent neurosensory deficit at the reconstructed ACL [1,2,5–8,11], its influence on the afferent pathway and on CNS re-organization of
sensorimotor programming. With practice, patients who have undergone ACL reconstruction may become better at coping with higher level sport movements through the development of compensatory lower extremity neuromuscular activation patterns [1,2,5–8,11]. Improving our understanding of these strategies may improve the results of post-surgical and non-surgical rehabilitation and help construct new motor control learning criteria prior to advancing patients through sport specific training and eventual release back to unrestricted sport activities [4]. Perceived higher level sports capability compared to pre-knee injury status was associated with increased lower extremity neuromuscular compensations through hip muscle groups. Hip joint afferent function remains non-impaired, decreasing dependence on the sensory-impaired knee region. During maximum effort movements such as a single leg hop for distance ipsilateral hip neuromuscular activation (gluteus maximus and medial hamstrings) may be up-regulated to enable successful task performance while placing lesser dependence on local knee extensor activation [34]. With greater understanding that ACL deficiency changes afferent pathway information leading to CNS reorganization of sensorimotor programming [1,4], and ACL reconstruction restores mechanical, but not neurosensory function [2], rehabilitation should focus more on CNS re-education rather than solely attempting to optimize peripheral neuromuscular function. Rehabilitation clinicians should take greater advantage of adaptive CNS characteristics, identifying patient sports movement goals and providing guided rehabilitation exercise experiences that stimulate motor learning thereby helping the re-programmed CNS find effective solutions [1]. This may be especially important during the latter stages of rehabilitation and during return to sport-specific training. Criteria-based neuromuscular re-training programs directed at motivated patients may improve functional lower extremity extensor muscle balance between the hip, knee and ankle joints at the involved lower extremity following ACL reconstruction [14,25,28]. However, given that grafts used for ACL reconstruction (allograft or autograft) do not restore native ACL neurosensory properties it is unlikely that a long-term restoration to premorbid sensorimotor relationships can be achieved [1,2,5–8, 11]. As patients learn to cope with progressively more challenging sports movement tasks in the presence of modified afferent information during rehabilitation and following return to play they may begin to develop more effective use of compensatory lower extremity extensor neuromuscular activation through the hip. 5. Study limitations This study has several important limitations. Asking subjects to recall their perception of whether or not they successfully returned to their preferred sport at their pre-injury level following surgery and rehabilitation at approximately five years post-surgery may have led to recall bias. Some subjects may have either over- or under-estimated their true performance capability [35]. To minimize the potential influence of excessive anterior knee laxity on lower extremity neuromuscular activation amplitudes of the 70 subjects who agreed to participate,
Table 2 Subject demographic data, IKDC Subjective Knee Survey score, Internal Health Locus of Control Survey score, and perceived sports activity intensity and frequency change comparison by perceived sports involvement level group. Mean [95% confidence interval]. * = P b 0.05.
Gender (#, % men) Age at surgery (yrs) Time post-surgery (yrs) Height (cm) Weight (kg) IKDC subjective knee survey score Internal health locus of control survey score Perceived sports activity intensity change (current–pre-injury) Perceived sports activity frequency change (current–pre-injury)
Group 1
Group 2
Group 3
P
20, 50% 26.5 [21.9, 31.8] 4.6 [2.8, 6.2] 176.5 [170.4, 180.1] 76.8 [67.4, 80.3] 91.0 [84.1, 94.6] 28.8 [25.0, 30.9] −0.35 [−0.77, −0.10] −0.30 [−0.77, −0.10]
23, 52.2% 29.3 [24.1, 34.4] 5.4 [4.2, 6.6] 172.8 [168.4, 177.3] 76.8 [68.3, 85.2] 87.2 [82.1, 92.4] 26.7 [24.1, 29.2] −0.41 [−0.67, −0.15] −0.54 [−0.90, −0.19]
22, 45.5% 33.6 [26.4, 39.1] 5.2 [3.8, 6.5] 172.1 [167.1, 177.1] 79.7 [68.0, 91.3] 78.6 [71.7, 85.5] 24.9 [22.0, 27.7] −1.10 [−1.6, −0.65] −0.60 [−1.0, −0.25]
0.95 0.20 0.56 0.38 0.86 0.016* (Groups 1 N 3) 0.44 0.004* Groups 1,2 N 3) 0.56
Table 3 Clinical examination results. Uninvolved–involved lower extremity for passive knee extension and flexion difference; involved–uninvolved lower extremity for knee laxity and single leg hop for distance differences. Mean [95% confidence interval]. UI = uninvolved lower extremity. I = involved lower extremity. Diff. = difference. Mean [95% confidence interval]. Group 1
Knee extension (°) Knee flexion (°) Knee laxity (mm) Single-leg hop for distance (m)
Group 2
Group 3
UI
I
Diff.
UI
I
Diff.
UI
I
Diff.
P
1.9 [−0.1, 3.2] 143.6 [142, 147.4] 5.4 [4.6, 6.8] 1.27 [1.13, 1.51]
1.2 [−0.7, 2.2] 142.1 [140.1, 146.4] 6.7 [5.7, 7.9] 1.27 [1.14, 1.48]
0.7 [−0.5, 2.7] 1.5 [−0.4, 4.2] 1.3 [−0.2, 1.6] 0.0 [−0.9, 1.1]
1.8 [0.4, 3.1] 143.0 [138.9, 147] 5.4 [4.4, 6.5] 1.06 [0.85, 1.26]
0.9 [−0.6, 2.1] 139.0 [135.2, 142.8] 6.9 [5.9, 7.8] 1.10 [0.91, 1.29]
0.9 [−0.2, 1.0] 4.0 [1.0, 7.5] 1.5 [0.9, 2.4] 0.04 [−0.9, 1.0]
2.6 [1.2, 3.3] 139.7 [135.8, 143.8] 5.4 [4.3, 6.5] 0.95 [0.79, 1.11]
1.9 [0.5, 3.3] 137.3 [132.9, 142.4] 7. 0 [5.9, 8.2] 0.82 [0.67, 0.97]
0.7 [−0.7, 1.7] 2.4 [−1.0, 6.9] 1.6 [0.5, 2.4] −0.13 [−0.8, 1.1]
0.78 0.82 0.25 0.77
Table 4a Group 1
GM VM MH G
Group 2
J. Nyland et al. / The Knee 21 (2014) 1191–1197
Table 4 Standardized EMG amplitudes during single leg hop for distance propulsion [%MVIC involved lower extremity − %MVIC uninvolved lower extremity]. GM = gluteus maximus, VM = vastus medialis, MH = medial hamstrings, G = gastrocnemius. * = P b 0.05.
Group 3
UI
I
Difference
UI
I
Difference
UI
I
Difference
P
0.97 [0.87, 1.07] 1.31 [1.13, 1.48] 0.77 [0.62, 0.93] 1.32 [1.01, 1.42]
1.2 [1.02, 1.32] 1.21 [1.13, 1.46] 0.91 [0.76, 1.05] 1.38 [1.28, 1.48]
0.23 [0.07, 0.40] −0.1 [−0.42, 0.21] 0.14 [−0.08, 0.36] 0.06 [−0.19, 0.30]
0.98 [0.90, 1.06] 1.36 [1.21, 1.51] 1.08 [0.79, 1.05] 1.20 [1.11, 1.28]
1.1 [1.07, 1.23] 1.16 [1.02, 1.3] 1.16 [1.04, 1.29] 1.29 [1.21, 1.37]
0.12 [−0.08, 0.26] −0.2 [−0.60, 0.13] 0.08 [−0.17, 0.30] 0.09 [−0.08, 0.29]
1.09 [0.99, 1.19] 1.51 [1.34, 1.69] 1.27 [1.12, 1.43] 1.30 [1.2, 1.41]
1.00 [0.79, 1.15] 1.45 [1.28, 1.62] 0.97 [0.82, 1.12] 1.18 [1.09, 1.28]
−0.09 [−0.31, 0.11] −0.06 [−0.33, 0.19] −0.3 [−0.63, −0.07] −0.12 [−0.30, 0.05]
Group 1 N 3, P = 0.036* 0.72 Group 1 N 3, P = 0.011* 0.20
Table 4b
Increased gluteus maximus activation amplitude at involved lower extremity No change or decreased gluteus maximus activation amplitude at the involved lower extremity
Group 1
Group 2
Group 3
Total
16 [11.4]* 4 [8.6] 20
13 [13.1] 10 [9.9] 23
8 [12.5] 14 [9.5] 22
37 [37] 28 [28] 65 [65]
11 [7.7]* 9 [12.3] 20
10 [8.8] 13 [14.2] 23
4 [8.5] 18 [13.5] 22
25 [25] 40 [40] 65 [65]
Chi-Square = 8.1, P = 0.019* Table 4c Increased hamstring activation amplitude at involved lower extremity No change or decreased hamstring activation amplitude at the involved lower extremity
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Chi-Square = 6.4, P = 0.041*
only those with a negative pivot shift test or ≤4 mm side-to-side anterior knee laxity difference were included in this analysis. Therefore, 5 subjects that demonstrated a positive pivot shift test were eliminated from statistical analysis, leaving 65 subjects out of a pool of 206 subjects who responded to the survey arm of the study [22]. The initial survey study sample consisted of 335 consecutive former patients. Although the subjects who participated in this study phase displayed similar demographics to the overall subject pool the possibility of selection and/or sampling bias exists [35,36]. Additionally, the post-test design used in this prospective study relied on the opposite lower extremity as a control. Ideally, a separate healthy, age-matched control group or an otherwise healthy group of ACL deficient patients would have been included in the study design. Clinical lower extremity functional performance tests such as single leg hop for distance testing however generally rely on comparisons with the contralateral, uninjured lower extremity [19,27,29,37,38]. This study only evaluated the single leg hop for distance. Other functional tests should be considered with future research in this area [21], using a longitudinal design and repeated measures that evaluate changes throughout early and late rehabilitation, sport specific training, and return to sport phases. Thigh girth measurements were not performed in this study. Thigh girth measurements may have provided additional insight regarding subject thigh muscle mass and the magnitude of fast twitch muscle fiber atrophy. However, without supporting cross-sectional magnetic resonance imaging to ascertain lean versus fat tissues it would have been difficult to accurately delineate muscle volume. Additionally, this study represents a small subject group consisting of former patients who had their ACL reconstructed by the same fellowship trained knee surgeon using exclusively allograft tissue. Therefore these results may not generalize to other populations. Use of allograft tissue however negates the potential influence of autogenous tendon harvest for ACL graft harvest on quadriceps femoris or hamstring muscle group function and screening to ensure the absence of a positive pivot shift test or excessive side-to-side anterior knee laxity differences minimized the influence of laxity on study findings. Another study limitation is use of two-dimensional sagittal kinematic analysis. Although three-dimensional kinematic analysis would have provided more accurate depictions of lower extremity joint movements, two-dimensional analysis remains useful and clinically practical as a screening tool for primarily uniplanar movements such as single leg hop for distance testing. Lastly, neither ground reaction force nor inverse dynamic moment analysis was performed. This addition would have provided a more comprehensive representation of lower extremity joint contributions to single leg hop for distance test performance.
4 [8.5] 18 [13.5] 22 [22]
25 [25] 40 [40] 65 [65]
37 [37] 28 [28] 65 [65]
9 [8.8] 14 [14.2] 23 [23]
10 [12.5] 12 [9.5] 22 [22]
6. Conclusion Lower extremity neuromuscular compensations suggesting a hip bias with increased gluteus maximus and medial hamstring activation was identified at the involved lower extremity among most subjects who perceived high perceived sports capability compared to preinjury status. These compensations may be related to a permanent neurosensory deficit, and its influence on afferent pathway changes that influence CNS sensorimotor re-organization. Further prospective, longitudinal research is needed. Chi-square = 7.7, P = 0.021
12 [7.7] 8 [12.3] 20 [20] Table 5c
Chi-square = 6.3, P = 0.048
Increased hamstring activation amplitude at involved lower extremity No change or decreased hamstring activation amplitude at the involved lower extremity
11 [13.1] 12 [9.9] 23 [23] 16 [11.4] 4 [8.6] 20 [20]
Group 2 Group 1 Table 5b
1.61 [1.47, 1.89] 1.31 [1.20, 1.50] 1.50 [1.32, 1.69] 1.28 [1.17, 1.39]
Increased gluteus maximus activation amplitude at involved lower extremity No change or decreased gluteus maximus activation amplitude at the involved lower extremity
Total
Group 1 N 3, P = 0.041* 0.80 Group 1 N 3, P = 0.023* 0.26
Group 3
P Difference
1.14 [0.90, 1.39] 1.63 [1.45, 1.80] 1.23 [1.01, 1.44] 1.25 [1.12, 1.39]
UI
1.37 [1.18, 1.69] 1.58 [1.40, 1.77] 1.6 [1.51, 2.08] 1.32 [1.18, 1.46] 1.33 [1.06, 1.49] 1.46 [1.29, 1.60] 1.36 [1.17, 1.55] 1.26 [1.15, 1.38] 0.37 [−0.08, 0.82] −0.13 [−.46, 0.21] 0.12 [−0.20, 0.44] 0.23 [−0.06, 0.53] 1.51 [1.36, 1.83] 1.39 [1.21, 1.55] 1.17 [0.97, 1.39] 1.23 [1.17, 1.54] 1.14 [0.88, 1.39] 1.52 [1.20, 1.57] 1.05 [0.84, 1.30] 1.00 [0.86, 1.14] GM VM MH G
I UI
Group 1
0.28 [−0.18, 0.34] −0.15 [−0.46, 0.16] −0.16 [−0.51, 0.19] 0.02 [−0.27, 0.31]
Group 3
UI
Difference Group 2
Difference I
I
−0.23 [−0.42, 0.06] 0.05 [−0.28, 0.22] −0.37 [−1.11, −0.17] −0.07 [−0.44, 0.21]
J. Nyland et al. / The Knee 21 (2014) 1191–1197
Table 5a
Table 5 Standardized EMG amplitudes during single leg hop for distance landing [%MVIC involved lower extremity − %MVIC uninvolved lower extremity]. GM = gluteus maximus, VM = vastus medialis, MH = medial hamstrings, G = gastrocnemius. Mean [95% confidence interval]. * = P b 0.05.
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