Perturbation Training prior to ACL Reconstruction Improves Gait

Asymmetries in Non-Copers
Erin Hartigan, Michael J. Axe, Lynn Snyder-Mackler
Physical Therapy Department, and Biomechanics and Movement Sciences Program, University of Delaware, 301 McKinly Lab, Newark,
Delaware 19716-2591
Received 20 April 2008; accepted 11 July 2008
Published online 20 November 2008 in Wiley InterScience (www.interscience.wiley.com). DOI 10.1002/jor.20754

ABSTRACT: We investigated whether preoperative perturbation training would help anterior cruciate ligament (ACL) deficient individuals
who complain of knee instability (‘‘non-copers’’) regain quadriceps strength and walk normally after ACL reconstruction. Nineteen non-
copers with acute ACL injury were randomly assigned into a perturbation group (PERT) or a strengthening group (STR). The PERT group
received specialized neuromuscular training and progressive quadriceps strength training, whereas the STR group received progressive
quadriceps strength training only. We compared quadriceps strength indexes and knee excursions during the mid-stance phase of gait
preoperatively to data collected 6 months after ACL reconstruction. Analyses of Variance with repeated measures (time/limb) were
conducted to compare quadriceps strength index values over time (time
group) and differences in knee excursions in limbs between groups
over time (limb
time
group). If significance was found, post hoc analyses were performed using paired and independent t-tests.
Quadriceps strength indexes before intervention (Pert: 87.2%; Str: 75.8%) improved 6 months after ACL reconstruction in both groups
(Pert: 97.1%; Str: 94.4%). Non-copers who received perturbation training preoperatively had no differences in knee excursions between their
limbs 6 months after ACL reconstruction (p ¼ 0.14), whereas those who received just strength training continued to have smaller knee
excursions during the mid-stance phase of gait (p ¼ 0.007). Non-copers strength and knee excursions were more symmetrical 6 months
postoperatively in the group that received perturbation training and progressive quadriceps strength training than the group who received
strength training alone. ß 2008 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 27:724–729, 2009

Keywords: anterior cruciate ligament; intervention; quadriceps strength; gait

Internal knee lesions account for 44.8% of athletic Non-copers’ quadriceps strength influences the amount
injuries, with the anterior cruciate ligament (ACL) being of knee flexion used during gait when tested preopera-
the most prevalent structure treated.1 About 200,000 tively.11 Furthermore, there is a significant effect of
ACL injuries occur annually in the US.2 Quadriceps continued quadriceps weakness on diminished knee
strength deficits,3–7 functional decline,8–13 and altered angles and knee moments during walking following
gait patterns6,14,15 are ubiquitous after ACL rupture.16 ACL reconstruction.3
Only one third of symptomatic ACL-deficient recrea- Quadriceps weakness not only contributes to gait
tional athletes demonstrate the ability to stabilize the and functional decline, but also may be a contributing
knee joint without the ACL.17,18 Nonsurgical interven- factor to knee OA.26 ACL rupture is associated with early
tions have been unsuccessful in restoring stability and degenerative changes, which continue after ACL recon-
strength to patients who complain of knee instability struction.27,28 A myriad of therapeutic interventions
after ACL rupture7; thus athletes are generally coun- have been tested to ascertain the most effective way to
seled that reconstructive surgery is necessary for treat patients after ACL injury and reconstruction.29–32
return to full pre-injury activities.19 Nearly one billion The trauma of surgery exacerbates strength and gait
dollars are spent on ACL reconstructions alone,20 yet abnormalities acutely. A paucity of research exists
postoperative quadriceps strength deficits4,5,7 and al- exploring how best to resolve the strength deficits and
tered movement patterns21,22 persist, despite restoration gait abnormalities that persist in non-copers despite
of the passive restraint. In fact, in a long-term follow-up reconstructive surgery.
study, more knee osteoarthritis (OA) was found after A neuromuscular training program, called perturba-
ACL reconstruction compared to those treated conserva- tion training, has improved movement patterns during
tively, with similar activity levels in both groups.23 gait and dynamic knee stabilization in potential copers
A screening examination and classification system after training.33 Exposing non-copers, therefore, to
was developed at the University of Delaware. The system perturbations of support surfaces prior to surgery may
can be used early after injury as an effective way to also be effective for improving gait deviations for this
discriminate between those athletes who have good cohort after surgery. Furthermore, progressive quad-
dynamic knee stability and the potential to compensate riceps strength training may be required preoperatively
well after complete ACL rupture (potential copers) and postoperatively to maximize functional recovery.
from those who have poor dynamic knee stability (non- Our purpose was to investigate whether preoperative
copers).24,25 Non-copers present with knee instability physical therapy that included perturbation training
and truncated involved side knee motion during gait15 to and a progressive quadriceps strengthening program
a greater extent when compared to potential copers.6 would help non-copers regain more symmetrical quad-
riceps strength and knee excursions when measured
Correspondence to: L. Snyder-Mackler (T: 302-831-3613; F: 302- 6 months after ACL reconstruction. We defined quad-
831-4234; E-mail: [email protected]) riceps strength symmetry as a quadriceps index value
ß 2008 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. (involved limb/uninvolved limb) of 90% or greater. All

724 JOURNAL OF ORTHOPAEDIC RESEARCH JUNE 2009

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PERTURBATION TRAINING PRIOR TO ACL RECONSTRUCTION 725

preoperative data were compared to data collected quadriceps strength training only (average of 3.1 weeks to
6 months after surgery. We hypothesized that complete). The perturbation group received 10 sessions
subjects would demonstrate a difference in preoperative of physical therapy including specialized neuromuscular
quadriceps strength indexes compared to postoperative exercises involving systematic translation of support surfaces
(Fig. 1) and progressive quadriceps strength training (average
values. We also tested whether knee excursions during
of 3.7 weeks to complete). We followed the University of
the mid-stance phase of gait continued to be altered Delaware guidelines for perturbation training,34 the goal
6 months after ACL reconstruction. We hypothesized being to break up generalized muscle stiffness as subjects
that non-copers who received preoperative perturbation were tactilely and verbally cued to elicit selective lower
training would exhibit symmetrical knee excursions extremity muscle contraction while balancing on a support
during mid-stance when tested after surgery, whereas surface that the physical therapist perturbed.
the group not receiving preoperative perturbation train- The goal of strength training was to maximize quadriceps
ing would continue to exhibit gait asymmetries. force output using high-intensity and low repetitions. Preoper-
atively, we obtained subjects’ one repetition maximum weight
lifted on the injured side while on the leg press and leg extension
METHODS
machines. Subjects then completed three sets of six repetitions
Subjects
at 75% of their one repetition maximum weight. Subjects
Nineteen subjects (13 males, 6 females between the ages of
performed lateral and forward step downs starting at a 4-inch
17 and 50 years old) with complete, acute, isolated ACL
step and progressing in step height when they demonstrated
rupture were recruited from the University of Delaware
proper technique (knee behind the toes, the mid-line of the
Physical Therapy clinic. One surgeon (M.J.A.) referred all
patella in alignment with the second toe, the hips level, and
subjects and diagnosed all ACL tears via clinical examination
touching the heel down softly to the floor). Lastly, subjects
and MRI findings. Subjects were regular participants in Level
completed an isokinetic spectrum routine on a dynamometer
I or II activities (activities involving jumping, cutting, and
(KIN-COM; Chattanooga Corp., Chattanooga, TN). Subjects
lateral motion) prior to injury.27 Exclusion criteria were full
were encouraged to exert full effort implementing both verbal
thickness chondral defects >1 cm, repairable meniscal tears,
and visual feedback as motivation (Table 1).
or concomitant grade III ruptures to other knee ligaments. Our
After the 10 preoperative sessions were completed, the
screening examination24 was administered, and only subjects
surgeon (M.J.A.) performed ACL reconstruction using
who had been classified as non-copers15 were recruited.
either semitendonosis-gracilis autograft or soft tissue allograft.
Subjects were randomly assigned into a perturbation group
Graft placement and fixation were similar for all subjects.
(N ¼ 9) or a strengthening group (N ¼ 10). The perturbation
After surgery, the University of Delaware postoperative ACL
group consisted of 5 males and 3 females (28  10.7 years),
protocol was followed by all subjects regardless of group.35
averaging 9.8  9.5 weeks from the time of injury to the screen.
The strength group included 7 males and 3 females (30  Quadriceps strength percentage, knee effusion grades, and
soreness were used as guidelines to progress the subject
9.4 years) and 12.6  13.1 weeks from the time of injury to the
screen. The study was approved by the University’s Institu- through the clinical milestones.
tional Human Subjects Review Board; each subject gave
informed consent. Quadriceps Maximum Volitional Isometric Contraction
(MVIC) Testing
Intervention Injured and uninjured limb quadriceps forces were assessed
No subjects exercised their lower extremities outside of with MVIC testing using the burst superimposition technique
therapy while participating in the preoperative intervention to assure maximal muscle activation.36 Subjects were tested on
phase. The strength group received 10 sessions of progressive the KIN-COM dynamometer using the University of Delaware

Figure 1. Pictures of a subject receiving perturbation training under three conditions (rockerboard, rollerboard, and rollerboard and
platform).

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726 HARTIGAN ET AL.

Table 1. Subjects Completed 10 Repetitions at the Str: 75.8%) improved 6 months after ACL reconstruc-
Speeds Shown while Performing Both Eccentric and tion in both groups (Pert: 97.1%; Str: 94.4%) (Fig. 2).
Concentric Quadriceps Muscle Contractions through Significant differences were also found in knee
10 to 1008 of Knee Flexion excursions between limbs (F ¼ 15.98, observed power ¼
0.96, p ¼ 0.001) and over time (F ¼ 7.52, observed
power ¼ 0.73, p ¼ 0.014). Knee excursions at mid-stance
were smaller on the involved side prior to surgery in both
groups. The involved limb moved through less flexion in
the perturbation groups (Mean: 5.98; 95% CI: 10.2 to 1.5;
p ¼ 0.026) and strength (Mean: 5.68; 95% CI: 10.5 to 0.6;
p ¼ 0.031) during mid-stance. The perturbation group
demonstrated an increase in knee excursion at mid-
testing procedure,37 with practice trials, verbal encourage- stance compared to the uninvolved side, resulting in no
ment, and visual targeting used to facilitate maximal effort. significant difference between limbs 6 months after
Quadriceps strength testing was performed prior to the surgery (Mean: 3.58; 95% CI: 8.3 to 1.4; p ¼ 0.14). The
intervention and 6 months after ACL reconstruction. mid-stance knee excursions continued to be significantly
different between limbs in the strength group 6 months
Motion Analysis
after surgery (Mean 7.08; 95% CI: 11.6 to 2.5; p ¼ 0.007)
Kinematic data were collected with a passive, eight camera
3-D motion analysis system (VICON; Oxford Metrics Ltd., (Fig. 3).
London, UK). Retro-reflective markers were attached over
bony prominences to define the hip, knee, and ankle joint DISCUSSION
centers with tracking shells affixed with cover rolls15 (Fab- Quadriceps Strength
rifoam Products, Exton, PA). Kinetic data were collected using
As hypothesized, all subjects demonstrated successful
a six-component force plate (Bertec Corp., Worthington, OH).
quadriceps strength gains 6 months after ACL recon-
Kinematic and kinetic data were collected, filtered, and
processed as described prevoiusly.15 Motion capture began struction. We operationally defined success as achieving
once speed over a 13-m walkway was consistent and the foot a quadriceps strength index of 90% or greater, a
contacted the force plate without targeting or altering the step clinically meaningful change achieved by both groups.
pattern. Subjects walked with the markers and tracking shells Our subjects’ successful gains support earlier findings of
attached until they were familiar with the task and gait speed improved quadriceps strength indexes 6 months after
was recorded. Variation of only 5% was allowed from that ACL reconstruction,5 though many investigators report
speed. There was no difference in inter-subject gait speed deficits 6 months after ACL reconstruction.3–5,7,31
between groups. The kinematic variable of interest was knee These conflicting results are likely due to discrep-
excursion during the mid-stance phase of gait. ancies in quadriceps strength testing and strengthening
protocols. Some investigators reported isometric muscle
Data Management and Analysis force represented as a quadriceps symmetry index,31,38
The quadriceps strength index was calculated using the while others reported isokinetic strength values of
highest quadriceps MVIC force output from each limb. The quadriceps symmetry.4,5,7 Our preoperative program
quadriceps index is a ratio of the involved side/uninvolved
side reported as a percentage for each subject. Knee motion
was calculated using rigid body analysis with Euler angles
(C-Motion, Inc., Rockville, MD). A customized LabVIEW
software program was written to analyze the kinematic data.
Five walking trials were averaged for each limb after the data
were normalized to 100% of stance. The first minimum value
after initial contact in the sagittal plane knee angle curve
denoted peak knee flexion, and the maximum value indicated
peak knee extension. The knee excursion during mid-stance
was obtained by calculating peak knee extension minus
peak knee flexion. Group means were calculated for quad-
riceps index and kinematics data. Mixed ANOVAs with
repeated measures (limb
group
time) were conducted
using a statistical software package (SPSS, Chicago, IL) to
compare differences between groups over time. If significance
was found, post hoc analysis was performed using paired and
independent t-tests. Significance was set at p < 0.05.

RESULTS
Quadriceps strength indexes improved over time Figure 2. Quadriceps Strength Index (involved force/uninvolved
force expressed as a percent) prior to intervention and 6 months
(F ¼ 16.5, observed power ¼ 0.961, p ¼ 0.002). Quadri- after ACL reconstruction for each group. Error bars represent
ceps strength indexes before intervention (Pert: 87.2%; standard deviation.

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PERTURBATION TRAINING PRIOR TO ACL RECONSTRUCTION 727

Perturbation training increases motion and decreases

muscle co-contractions in the involved limb during the
weight acceptance phase of gait in potential copers after
acute ACL rupture.41 Thus, reduction in co-contraction
values may be related with our findings of increased
motion.
Loss of feedback from mechanoreceptors after ACL
rupture and abnormalities in gamma loop information
may explain quadriceps weakness.42 Subjects who
received perturbation training were trained to focus on
the somatosensory input from the weight distribution of
the foot contact on the board and the afferent information
coming from the lower extremity (joint proprioception
and muscle response). The focused awareness of the body
in space, along with tactile and verbal feed-forward
and feed-back cues during training may have modified
gamma loop function. Training may have improved
gamma loop feedback and decreased antagonistic muscle
Figure 3. Involved knee excursions prior to intervention (Pre)
and 6 months after ACL reconstruction (Post) for the involved and activity, enhancing the quadriceps’ ability to stabilize
uninvolved limb for each group. Error bars represent standard the knee dynamically during gait.
deviation.
The strength gains demonstrated by both groups may
decrease the risk of knee OA. Quadriceps weakness has
been shown to be related to the development of knee OA
focused on intense, progressive quadriceps strengthen- in women.43 However, perturbation training may
ing on the involved side only with all subjects reporting enhance the sensorimotor characteristics of the muscle
muscle fatigue after each treatment followed by delayed more than strengthening alone. Hurley26 inferred that
onset quadriceps soreness. Keays and colleagues7 pro- both motor and sensory dysfunction of a muscle are
vided preoperative quadriceps strengthening, though important factors in cartilage degradation. Further-
this was predominately home-based and exercise inten- more, Hurley26 surmised that rehabilitation exercises
sity was not specified. Our postoperative protocol35 may reverse sensorimotor dysfunction, thereby delaying
focused on the importance of early strength gains using or preventing the onset of OA.
neuromuscular electrical stimulation that facilitates The improved inter-limb symmetry displayed during
quadriceps strength gains more than volitional exercises gait by the perturbation group may also have positive
alone.39,40 implications on joint health. Chaudhari et al.14 surmised
that mechanical changes may be the precipitating cause
Gait Kinematics of knee OA as loads shift to areas of cartilage not typically
As hypothesized, subjects receiving perturbation train- loaded. They documented that cartilage appears to be
ing demonstrated no difference in knee excursions conditioned to load history and that conditioned cartilage
during mid-stance 6 months after ACL reconstruction. likely has different abilities to respond to loads.14 In vivo
We previously reported preoperative findings of studies of non-copers indicate that ACL-deficient limbs
decreased knee excursions in this group of non-copers.15 shift the contact point between tibia and femur with the
There were no differences in knee effusion grades tibial point moving more anterior with knee extension.44
during preoperative testing or 6 months following ACL Hence, altered knee kinematic changes observed in the
reconstruction between groups, and no subject com- sagittal plane may also lead to shift joint load to an
plained of pain or soreness during gait analysis. infrequently loaded area. Breaking the typical low
Furthermore, all had symmetrical quadriceps strength knee flexion excursion strategy while walking may be
and knee range of motion without clinically observed advantageous, as joint loads may be distributed over a
antalgic gait patterns, complaints of instability, or larger contact area more in line with the conditioned
episodes of giving way when tested 6-months post- cartilage regions adapted to handle the pre-injury
operatively. Yet the strength group continued to display loading pattern.
less knee excursion during mid-stance on the involved Despite symmetrical strength achieved by both of our
side. groups, the strength group demonstrated differences
in knee excursions between limbs during mid-stance
Interpreting Findings 6 months after ACL reconstruction. This suggests that
The quadriceps plays an integral role in concentrically the neuromuscular system is not controlling the involved
advancing the knee through extension during mid- limb the same way as the uninvolved limb in both groups.
stance. The perturbation group demonstrated enhanced Improved mid-stance excursion in the perturbation
ability to use the quadriceps strength gains by moving group is a promising first indication that neuromuscular
the involved limb similarly to the uninvolved limb. training rehabilitation programs can improve movement

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728 HARTIGAN ET AL.

patterns in the involved limb after ACL reconstruction in 15. Hurd WJ, Snyder-Mackler L. 2007. Knee instability after
non-copers. Investigations that include electromyogra- acute ACL rupture affects movement patterns during the
phy are warranted to determine the neuromuscular mid-stance phase of gait. J Orthop Res 25:1369–1377.
changes responsible for the perturbation group’s gait 16. Patel RR, Hurwitz DE, Bush-Joseph CA, et al. 2003.
Comparison of clinical and dynamic knee function in patients
adaptations. with anterior cruciate ligament deficiency. Am J Sports Med
31:68–74.
ACKNOWLEDGMENTS 17. Noyes FR, Matthews DS, Mooar PA, et al. 1983. The
This research was supported by the National Institutes of symptomatic anterior cruciate-deficient knee. Part II: the
Health (R01AR048212; S10RR022396) and the Foundation of results of rehabilitation, activity modification, and counseling
Physical Therapy (PODS I). We acknowledge Sarah Trager for on functional disability. J Bone Joint Surg [Am] 65:163–
her software programming support, Kyle Fettemore and Greg 174.
Seymour for their assistance with data collections and data 18. Noyes FR, Mooar PA, Matthews DS, et al. 1983. The
processing, and the University of Delaware Physical Therapy symptomatic anterior cruciate-deficient knee. Part I: the
Clinic for assistance with subject training. long-term functional disability in athletically active individ-
uals. J Bone Joint Surg [Am] 65:154–162.
19. Marx RG, Jones EC, Angel M, et al. 2003. Beliefs and
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