Abstract
Background: Thigh muscle atrophy is a major impairment that occurs
early after reconstruction of the anterior cruciate ligament and persists for
several years. Eccentric resistance training has the potential to induce
considerable gains in muscle size and strength that could prove beneficial
during postoperative rehabilitation. The purpose of this study was to evaluate
the effects of progressive eccentric exercise on thigh muscle structure
following reconstruction of the anterior cruciate ligament.
Methods: Beginning three weeks after reconstruction of the anterior
cruciate ligament, forty patients were randomly assigned to a program
involving either twelve weeks of eccentric exercises or a standard
rehabilitation protocol. Patients were matched by surgical procedure, sex, and
age. The final series consisted of two cohorts of twenty patients each who had
been treated with one of two types of graft (semitendinosus-gracilis or
bone-patellar tendon-bone), with ten patients treated with each of the two
rehabilitation protocols in each graft cohort. To evaluate changes in muscle
structure, magnetic resonance images of the involved and uninvolved thighs
were acquired before and after training. The volume and peak cross-sectional
area of the quadriceps, hamstrings, and gracilis and the distal portion of the
gluteus maximus were calculated from these images.
Results: The volume and peak cross-sectional area of the quadriceps
and gluteus maximus, in both the involved and the uninvolved thighs and in the
patients treated with each type of graft, improved significantly more in the
eccentric-exercise group (p < 0.001). The magnitude of the volume change
was more than twofold greater in that group. No significant differences in any
hamstring or gracilis structural measurements were observed between the
rehabilitation groups. However, the volume and peak cross-sectional area of
the gracilis were markedly reduced, compared with the pretraining values, in
the patients who had undergone reconstruction with the semitendinosus-gracilis
graft.
Conclusions: Eccentric resistance training implemented three weeks
after reconstruction of the anterior cruciate ligament can induce structural
changes in the quadriceps and gluteus maximus that greatly exceed those
achieved with a standard rehabilitation protocol. The success of this
intervention can be attributed to the gradual and progressive exposure to
negative work through eccentric exercise, ultimately leading to production of
high muscle force.
Level of Evidence: Therapeutic Level I. See Instructions
to Authors for a complete description of levels of evidence.
Quadriceps atrophy and strength deficits are predominant impairments
following reconstruction of the anterior cruciate ligament. The magnitude of
atrophy and strength loss often exceeds 20% and 30%, respectively, during the
first three
months1-6.
Despite concentrated rehabilitation efforts, a 10% to 20% deficit in
quadriceps size and strength still persists for years after
surgery1,2,7-17.
The most important muscle group for lower-extremity function, the quadriceps,
is preferentially affected, although other lower-extremity muscles undergo
substantial atrophy as well. Deficits in hamstring and gracilis muscle volume
of 10% and 30% have been reported after surgical reconstruction with an
autologous semitendinosus-gracilis
graft17,18.
Like muscle wasting, muscle weakness is ubiquitous, with strength unlikely to
return to preinjury levels. Novel interventions that can safely, feasibly, and
effectively overload muscles early after surgery are needed to minimize
atrophy and weakness that become long-standing.
A muscle's force production ability, and hence its structural and
functional response, is greatest when an external force exceeds that of the
muscle and the muscle lengthens
eccentrically19.
The resulting work performed by the muscle is termed "negative
work" because the change in muscle length is opposite that of the muscle
force vector; hence, work (force × distance) is negative. The
application of a progressively increasing, high-force eccentric resistance has
been shown to safely increase muscle size and strength in healthy and clinical
populations and therefore may be suited for use after reconstruction of the
anterior cruciate
ligament20-25.
In a recent case report, we reported observing impressive gains in quadriceps
size and strength as a result of eccentric training following reconstruction
of the anterior cruciate
ligament20. We have
also shown that the gradual and progressive application of eccentrically
induced negative work can be tolerated without harmful side effects following
this surgery26.
The purpose of the present study was to evaluate the effects of progressive
eccentric exercise on thigh muscle structure in individuals who had undergone
reconstruction of the anterior cruciate ligament. Our primary hypothesis was
that, compared with standard rehabilitation, eccentrically biased
rehabilitation would result in significantly greater improvements in
quadriceps volume and peak cross-sectional area in the involved thigh.
Furthermore, these structural improvements would lead to superior short-term
results in terms of quadriceps strength and performance while preserving knee
stability. Secondarily, we hypothesized that there would be no difference in
the improvement in hamstring or gracilis muscle volume or peak cross-sectional
area between the rehabilitation groups. We further hypothesized that there
would be significantly greater improvements in quadriceps volume and peak
cross-sectional area in the uninvolved thigh, as it too was incorporated in
the training, but there would be no difference between rehabilitation groups
with regard to the hamstring or gracilis structure in the uninvolved
thigh.
The term standard rehabilitation in this paper does not mean that
the therapy program met some sort of institutional standard. Instead, it
refers to a rehabilitation protocol that we commonly used at our
institution.
Subjects
Patients diagnosed with a rupture of the anterior cruciate ligament at our
University Sports Medicine Center between January 2004 and June 2005 were
considered to be potential subjects. They were included in the study if they
were between eighteen and fifty years of age, moderately active prior to the
injury (a score on the Tegner activity
scale27 of =4
points), and willing to comply with the twelve-week training program (starting
three weeks after surgery). Patients were excluded if they had had a previous
fracture or reconstructive procedure in either lower extremity; abnormal
findings on a radiograph of the knee; or a concurrent injury of the posterior
cruciate ligament or the lateral collateral ligament, a grade-III tear of the
medial collateral ligament, or a substantial articular cartilage lesion.
Patients with a large vertical longitudinal meniscal tear were also excluded
because of concern about allowing aggressive rehabilitation in these cases.
Those who had had a partial meniscectomy or a small meniscal repair were
allowed to participate. The graft selection was based on the patient's desire
and/or request after he or she had been educated about the choice. The
surgeons had a bias toward using bone-patellar tendon-bone grafts in younger
patients and hamstring grafts in older patients. The study received approval
from the institutional review board at the University of Utah, and all
patients provided informed consent before participating.
Surgical Procedures
Two surgeons performed all of the ligament reconstructions in the patients
in this study, and each used an arthroscopically assisted technique with a
semitendinosus-gracilis or bone-patellar tendon-bone autograft. For the
semitendinosus-gracilis procedure, a 3.5-cm incision was made over the medial
aspect of the tibia, directly over the semitendinosus and gracilis tendons.
Sutures were placed in a whip-stitch fashion in the distal 2.5 cm of each of
the tendons. With use of a tendon stripper, the tendons were harvested and
fashioned into two grafts, each 22 cm in length. With the aid of arthroscopy,
the stump of the torn anterior cruciate ligament was débrided and a
lateral notchplasty was performed to ensure that the over-the-top position
could be identified. With use of an anterior-cruciate-ligament aiming guide, a
guidewire was drilled into the anatomic footprint of the anterior cruciate
ligament to position the tibial tunnel. The femoral tunnel was placed at the
10 o'clock position (right knee) or 2 o'clock position (left knee). The graft
was passed through the knee and an EndoButton continuous loop (Smith and
Nephew, Andover, Massachusetts) was used to secure the graft on the femoral
side. The ends of the semitendinosus and gracilis graft were tensioned with
use of the Linvatec Tensioner System (Largo, Florida). Sixty newtons of
tension was placed on the semitendinosus graft, and 40 N was placed on the
gracilis graft. An Intrafix device (DePuy Mitek, Raynham, Massachusetts) or an
Arthrex resorbable interference screw (Naples, Florida) was used to secure the
tibial side of the graft. The suture ends from the graft were then tied over a
bicortical post and washer to provide back-up
fixation28.
For the bone-patellar tendon-bone procedure, an incision was made to
approach the patella, patellar tendon, and proximal part of the tibia. A 10 by
25-mm-long block was harvested from the patella along with a 10-mm-wide strip
of patellar tendon and a 10 by 30-mm tibial bone plug. With use of a tibial
aimer, a guide pin was placed into the tibia and then overdrilled with an
appropriately sized tibial drill bit. After this, a 6-mm over-the-top aimer
was placed at the 10 o'clock position on the femur for a right knee or the 2
o'clock position for a left knee to accurately select the starting point for
the femoral tunnel. This over-the-top aimer allowed for a 1-mm cortical rim on
the back of the femoral tunnel when a 10-mm graft was used. A Beath pin was
drilled up into position and then overdrilled to the exact length of the
bone-tendon-bone graft with the appropriately sized drill bit. At this point,
the cross-pin aimer (RIGIDfix system; (DePuy Mitek) was placed in the knee up
into the femur. The cross-pin sleeves were then drilled percutaneously from
lateral to medial into the lateral cortex. The graft was pulled up into
position. The cross-pins were drilled, and resorbable pins were placed. After
good fixation was obtained, the tibial end was tensioned. An interference
screw was then placed next to the bone block in an interference-fit
fashion29.
Eccentric and Standard Rehabilitation Programs
A randomized matched design was used after the surgery to randomly assign
patients to either an eccentric or a standard-rehabilitation group. Patients
were matched by graft type, sex, and age. For example, after the first
patient, a thirty-five-year-old man who had undergone a reconstruction of the
anterior cruciate ligament with a semitendinosus-gracilis autograft, was
randomized (by coin flip) into one group, the second man who had the same
graft type and was between the ages of thirty-two and thirty-eight was
assigned to the other group. The standard rehabilitation protocol that all
patients followed was a criterion and time-based, three-phase rehabilitation
program from this institution that emphasized closed-chain exercises,
functional training, and gaining an early range of knee motion
(Table I). The exercise
prescription was determined by the individual response to exercise.
Specifically, if exercises were completed without an increase in knee pain or
effusion, the patient was considered ready to progress. Other exercises were
then added or current exercises were continued at a higher intensity,
frequency, and/or duration.
After ligament reconstruction, all patients completed two to three weeks of
phase-I exercises that focused on controlling pain and effusion, gaining a
full range of motion of the knee, and attaining basic quadriceps function
(Table I). Beginning three
weeks following surgery, patients in the eccentric-exercise group continued
with standard rehabilitation and also began a twelve-week progressive
negative-work exercise program using one of two recumbent eccentric
ergometers, described previously in
detail20,23,26,30.
The first ergometer was similar to a recumbent cycle. It was replaced by a
second, more durable and comfortable ergometer (Eccentron, Denver, Colorado)
similar to a recumbent stepper. The cycle ergometer was used by the first five
patients, and the stepper ergometer was used thereafter. Both ergometers
induced eccentric contractions of the knee and hip extensors and negative work
of similar magnitude (Fig. 1).
During each exercise session, the negative work rate was visible on the
computer monitor, and the total amount of negative work (measured in
kilojoules) was recorded. The pedal speed was self-selected and ranged from 20
to 40 revolutions per minute. Patients were positioned on the ergometer so
that the negative work would occur from approximately 20° to 60° of
knee flexion, effectively minimizing the possibility of a knee hyperextension
injury. The intensity of the exercise was based on the Borg rating of
perceived exertion
scale31. The first
session was five minutes in duration at a "very, very light"
intensity. If a patient had a favorable response to exercise (such as absence
of increased knee pain, effusion, or excessive fatigue), he or she was allowed
to gradually progress to a "hard" intensity and a maximum duration
of thirty minutes (Table II).
Conducting the exercise regimen in this manner has been shown to be safe and
feasible after reconstruction of the anterior cruciate
ligament26.
Patients had to complete a minimum of 80% of the training sessions to continue
in the study. Beginning three weeks postoperatively, the patients in the
standard-rehabilitation group continued with the standard rehabilitation
protocol. In an attempt to equalize the total exercise time between the
groups, these patients were instructed to follow an exercise regimen that was
similar to the one used by the eccentric-exercise group except that the
patients in the standard-rehabilitation group used a concentric ergometer
(gradually progressing to a "hard" intensity and a duration of
thirty minutes).
Determination of Muscle Structure with Magnetic Resonance
Imaging
A 1.5-T Signa LX magnetic resonance imaging instrument and body coil
(General Electric Medical Systems, Milwaukee, Wisconsin) was used to acquire a
coronal scout scan and axial spin-echo T1-weighted images. Both thighs were
scanned from the superior border of the femoral head to the tibiofemoral joint
line while the subject lay supine in the scanner. The scans were acquired with
an image matrix of 256 × 256, a field of view of 40 to 44 cm depending
on the size of the subject, a slice thickness of 8 mm, and an interslice
distance of 15 mm. After electronic data transfer of magnetic resonance
images, cross-sectional areas were measured with use of custom-written
image-analysis software (MATLAB; The MathWorks, Natick, Massachusetts) on a
desktop personal computer. Muscle volumes could be determined by measuring the
muscle cross-sectional area in sequential axial sections across the length of
the muscle32. On
each image, the entire muscle of interest (independent of skin, bone, and fat)
was identified and was manually traced with use of a computer mouse. The
cross-sectional area of each slice was automatically computed with use of the
averaged gray-scale density of the traced muscle. The muscle volume was
calculated by multiplying the average of two consecutive measurements of
cross-sectional area by the slice thickness plus the interslice distance (23
mm) and then summing those values across the length of the muscle.
A pretraining magnetic resonance imaging scan was acquired for each
participant three weeks (mean [and standard deviation], 22.2 ± 3.4
days) after surgery. The follow-up images were acquired fifteen weeks (mean,
107.8 ± 7.5 days) after surgery, following completion of the
twelve-week training program. The main objective of this study was to evaluate
the effect of the eccentric-exercise intervention on the structure, including
the volume (in cubic centimeters) and peak cross-sectional area (in square
centimeters), of the thigh muscles. Depending on the size of the subject, the
volume was calculated from seventeen to twenty axial slices of the quadriceps,
fourteen to seventeen slices of the hamstrings, and thirteen to sixteen slices
of the gracilis. Because the eccentric-exercise intervention was a
quadriceps-dominated exercise, the primary outcome measures were changes in
the volume and peak cross-sectional area of the quadriceps. However, as a
result of the frequency with which patients reported soreness in the gluteal
region due to training, we decided to also evaluate the distal portion of the
gluteus maximus, from the head of the femur distally. Thus volume was
calculated from eight, nine, or ten axial magnetic resonance image slices. The
same investigator, who was blinded to whether the imaging was done before of
after training, performed all structural measurements in a highly reproducible
manner (intraclass correlation coefficients, >0.99).
Assessment of Knee Stability and Functional Status
Routine clinical examinations, which included an assessment of knee
stability with use of the KT-1000 device (MEDmetric, San Diego, California),
were completed prior to reconstruction of the anterior cruciate ligament and
fifteen weeks following the surgery. These examinations also included
isokinetic strength testing and the single-leg hop-for-distance test.
Quadriceps and hamstring strength (peak torque) were assessed with use of a
Kin Com isokinetic dynamometer (Chattecx, Chattanooga, Tennessee). Patients
were tested concentrically at 60° · s—1 in a
seated position with the hips and knees in 90° of flexion and the thighs,
pelvis, and upper body firmly strapped to the seat of the dynamometer. Prior
to testing, a warm-up consisting of three repetitions (at 50%, 75%, and 100%
intensity) was completed. After a brief rest period of one minute, patients
completed three separate trials at 100% intensity. The peak torques of the
three trials were averaged, and the average was recorded. For the
hop-for-distance test, patients were instructed to hop as far as possible,
always landing on the same leg. Hopping with each leg was tested three times,
and the maximal distance was recorded. The average of the two farthest hops
was recorded. The strength and performance indices (the value for the involved
limb divided by the value for the uninvolved limb) were used for statistical
analysis. Patients also completed the Activities of Daily Living Scale of the
Knee Outcome Survey and the Lysholm questionnaire. Although the focus of this
research was on muscle structure, these measures were included to establish
the short-term functional status of the patients prior to surgery and after
the twelve-week training program.
Statistical Methods
The sample size was based on preliminary data with use of improvement in
quadriceps volume resulting from a twelve-week eccentric resistance training
program as the primary outcome measure. This showed that nine patients in each
group would be sufficient to achieve significance with 80% power and an
a level set at 0.05. In order to analyze the effects of eccentric
exercise independent of graft type, because both a semitendinosus-gracilis and
a bone-patellar tendon-bone graft were used for the surgical reconstructions,
twenty patients treated with each graft type (with ten treated with each
exercise regimen in each graft group)—i.e., a total of forty
individuals—were recruited to participate. Data were analyzed with SPSS
software (version 13.0; SPSS, Chicago, Illinois). Descriptive statistics for
categorical variables and measures of central tendency for continuous
variables were calculated to summarize the data. Tests for outliers and
assumptions of the parametric statistical tests were performed. A two-way
mixed repeated-measures analysis of variance with factors of group and time
was used to analyze mean differences in muscle volume and peak cross-sectional
area between the eccentric and standard-rehabilitation groups. The Pearson
product-moment correlation was used to correlate improvements in muscle volume
and peak cross-sectional area. An independent t test was used to analyze mean
differences in knee laxity, quadriceps and hamstring strength, hopping
distance, and self-reported scores fifteen weeks after surgery between the
eccentric and standard-rehabilitation groups. Significance levels for all
statistical analyses were set at a < 0.05.
All forty patients who enrolled completed the study. Preoperative
demographic and physical characteristics were similar between the intervention
groups; however, those treated with the bone-patellar tendon-bone graft were
significantly younger and more active than those treated with the
semitendinosus-gracilis graft (see Appendix). Thirty-two of the forty patients
had surgery within four months after the injury (at a mean of 45.1 ±
24.5 days in the eccentric-exercise group and at a mean of 41.8 ± 29.3
days in the standard-rehabilitation group). The time between the initial
ligament tear and the surgery was longer than one year for five patients (two
in the eccentric-exercise group and three in the standard-rehabilitation
group). Three individuals in the eccentric-exercise group and four in the
standard-rehabilitation group had small meniscal lesions that were repaired,
and three individuals in both groups had meniscal lesions that were
débrided or resected.
The twenty patients in the eccentric-exercise group completed a mean of
31.1 ergometry sessions (range, twenty-nine to thirty-six sessions), for an
overall compliance rate of 86%. No significant differences in results were
observed between the cycle and stepper ergometers (p = 0.86). Overall, the
participants completed an average of 738 minutes of eccentric ergometry. The
patients reported that they performed lower-extremity weight-lifting,
excluding the eccentric ergometry, on a mean of 15.3 days during the
twelve-week training period. In comparison, the twenty patients in the
standard-rehabilitation group averaged 709 minutes of concentric ergometry.
Those patients reported that they performed lower-extremity weight-lifting on
a mean of 25.4 days during the twelve-week training period. The number of
reported days on which weight-lifting was performed was significantly greater
in the standard-rehabilitation group (p < 0.01).
Volume and Peak Cross-Sectional Area
Quadriceps
Compared with the pretraining measurements, the posttraining quadriceps
volume and peak cross-sectional area in the involved thigh increased
significantly in both the eccentric and the standard-rehabilitation group (p
< 0.001). However, these increases in the quadriceps volume and peak
cross-sectional area were significantly greater (p < 0.001), by more than
two-fold, in the eccentric-exercise group (mean improvement, 23.1% ±
12.9% and 24.2% ± 12.6%, respectively) than in the
standard-rehabilitation group (mean improvement, 8.8% ± 9.3% and 9.3%
± 9.4%). There was a significant correlation between improvement in
quadriceps volume and improvement in peak cross-sectional area in the involved
thigh (r = 0.98, p = 0.01). The greater than twofold increase in quadriceps
hypertrophy in the eccentric-exercise group was observed in both the
semitendinosus-gracilis and the bone-patellar tendon-bone cohort, although the
overall magnitude of improvement was smaller (nonsignificantly so) in the
bone-patellar tendon-bone cohort (Figs.
2 and
3 and Appendix).
Nine of the ten patients in the eccentric-exercise group who had been
treated with a semitendinosus-gracilis graft demonstrated a quadriceps volume
increase of >20%, whereas nine of the ten patients in the
standard-rehabilitation group who had been treated with a
semitendinosus-gracilis graft demonstrated a volume increase of <15%. In
contrast, five of the ten patients in the eccentric-exercise group who had
been treated with a bone-patellar tendon-bone graft demonstrated a quadriceps
volume increase of >20%, whereas eight of the ten patients in the
standard-rehabilitation group who had been treated with a bone-patellar
tendon-bone graft demonstrated a volume increase of <10% (see
Appendix).
The quadriceps volume and peak cross-sectional area in the uninvolved thigh
increased significantly in both the eccentric and the standard-rehabilitation
group (p = 0.001), although these structural increases were significantly
greater (p < 0.001) in the eccentric-exercise group (mean improvement,
11.2% ± 5.1% and 11.0% ± 4.9%, respectively) than in the
standard-rehabilitation group (mean improvement, 3.0% ± 3.3% and 3.1%
± 3.7%). The improvement in the uninvolved thigh was significantly
greater in the individuals who had been treated with the bone-patellar
tendon-bone graft (p < 0.001) than it was in those who had been treated
with the semitendinosus-gracilis graft (Figs.
2 and
3 and Appendix). There was a
significant correlation between improvement in quadriceps volume and
improvement in peak cross-sectional area in the uninvolved thigh (r = 0.92, p
= 0.01).
Gluteus Maximus
The distal portion of the gluteus maximus, beginning from the superior
border of the femoral head, was analyzed. Compared with the pretraining
values, the posttraining volume and peak cross-sectional area of the gluteus
maximus of the involved lower extremity increased significantly in both the
eccentric and the standard-rehabilitation group (p < 0.001). The magnitude
of these structural increases was significantly greater (p < 0.001), by
more than twofold, in the eccentric-exercise group (mean improvement, 25.3%
± 12.9% and 26.5% ± 10.5%, respectively) than in the
standard-rehabilitation group (mean improvement, 9.8% ± 9.3% and 9.6%
± 10.5%) (Fig. 3 and
Appendix). There was a significant correlation between improvement in the
volume and improvement in the peak cross-sectional area of the gluteus maximus
of the involved lower extremity (r = 0.94, p = 0.01). The greater than twofold
increase in gluteus maximus hypertrophy in the eccentric-exercise group was
observed in both the semitendinosus-gracilis and the bone-patellar tendon-bone
cohort, although the overall magnitude of improvement was smaller
(nonsignificantly so) in the semitendinosus-gracilis cohort.
The volume and peak cross-sectional area of the gluteus maximus of the
uninvolved thigh increased significantly in the eccentric-exercise group (mean
improvement, 11.1% ± 5.1% and 10.2% ± 6.4%, respectively; p <
0.001) but not the standard-rehabilitation group (mean improvement, 2.5%
± 6.1% and 3.8% ± 6.8%; p = 0.19)
(Fig. 3 and Appendix). There
was a significant correlation between improvement in the volume and
improvement in the peak cross-sectional area of the gluteus maximus of the
uninvolved lower extremity (r = 0.83, p = 0.01).
Hamstrings
Comparison of the pretraining and posttraining values revealed no
significant differences in the improvements in hamstring volume or peak
cross-sectional area in either the involved or the uninvolved thigh between
the eccentric and standard-rehabilitation groups (p range, 0.23 to 0.90).
However, there was a significant difference between graft types, as the
hamstring volume and peak cross-sectional area in the involved thigh increased
significantly, compared with the pretraining values, in the bone-patellar
tendon-bone cohort (p = 0.006) but not in the semitendinosus-gracilis
cohort (p range, 0.13 to 0.53; Appendix and
Fig. 4). There was a
significant correlation between improvement in the hamstring volume and
improvement in the hamstring peak cross-sectional area in the involved (r =
0.89, p = 0.01) and uninvolved (r = 0.62, p = 0.01) thighs.
Gracilis
Comparison of the pretraining and posttraining measurements also showed no
significant differences in the improvements in the gracilis volume or peak
cross-sectional area in either the involved or the uninvolved thigh between
the eccentric and standard-rehabilitation groups (p range, 0.35 to 0.92).
However, whereas the gracilis volume and peak cross-sectional area in the
involved thigh decreased significantly, compared with the pretraining values,
in the semitendinosus-gracilis cohort (p < 0.001), no significant changes
were observed in the bone-patellar tendon-bone cohort (p range, 0.16 to 0.78).
The gracilis volume and peak cross-sectional area in those who had undergone
the semitendinosus-gracilis graft procedure decreased 18.6% ± 7.0% and
13.0% ± 10.1% in the eccentric-exercise group and 16.7% ± 12.4%
and 10.0% ± 11.9% in the standard-rehabilitation group (Figs.
2 and
4 and Appendix). There was a
significant correlation between improvement in the gracilis volume and
improvement in the peak cross-sectional area in the involved (r = 0.91, p =
0.01) and uninvolved (r = 0.69, p = 0.01) thighs.
Assessment of Knee Stability and Functional Status
The functional status measures are presented in a table in the Appendix.
With the numbers studied, there were no significant differences in the knee
laxity measured with the KT-1000 device (with manual maximum force) between
the eccentric (mean, 1.6 ± 1.8 mm) and standard (mean, 1.7 ± 1.0
mm) rehabilitation groups fifteen weeks after reconstruction of the anterior
cruciate ligament (p = 0.83). The overall quadriceps strength index was
significantly greater in the eccentric-exercise group than in the
standard-rehabilitation group (p = 0.03). There were no significant
differences between groups with regard to the hamstring strength index (p =
0.49) or hop index (p = 0.09); however, the hop index was significantly
greater in the eccentric-exercise group of the bone-patellar tendon-bone
cohort (p = 0.04). Scores on the Activities of Daily Living Scale of the Knee
Outcome Survey and on the Lysholm scale improved significantly fifteen weeks
after surgery, compared with preoperative values, in all groups (p <
0.001), but with the numbers studied no significant differences between groups
were observed (p = 0.66 and 0.93, respectively).
In support of our primary hypothesis, this investigation demonstrated that
the addition of progressive eccentric exercise, implemented three weeks after
reconstruction of the anterior cruciate ligament, safely induced gains in size
and strength in key muscle groups that exceeded the gains following a standard
rehabilitation program while preserving knee stability. The increases in the
sizes of the quadriceps and gluteus maximus muscles were twofold greater than
those observed following the standard rehabilitation program. Because muscle
atrophy is ubiquitous and profound in the early period following surgery,
these structural increases (observed in both the involved and the uninvolved
lower extremities and in both the semitendinosus-gracilis and the
bone-patellar tendonbone cohort) are unprecedented, to our knowledge.
Since the potential to overload muscle is greater with eccentric training
(compared with the potential with concentric training), as a result of its
high force-producing abilities, greater increases in muscle size and strength
should not be surprising. High eccentric muscle forces, however, are closely
associated with a muscle damage response in individuals not adapted to these
forces. In fact, the patients in this study reached negative work levels
consistent with those used to induce muscle damage. Another concern with high
eccentric muscle forces is the amount of force that such an intervention would
place through the healing graft, particularly after a bone-patellar
tendon-bone procedure. Yet, as a result of the repeated, gradual, and
progressive exposure to negative work, the patients in this study had great
improvement in the quadriceps (and gluteal) muscle size without experiencing
any deleterious effects. These results suggest that this mode of resistance
training may be ideal for safely mitigating the persistent muscle impairments
commonly observed following reconstruction of the anterior cruciate ligament,
and they support the findings of other investigators who have reported the
safe achievement of substantial gains in muscle size and strength by means of
progressive eccentric exercise in healthy and clinical
populations20-25.
Exercising a muscle eccentrically is certainly not unusual following
reconstruction of the anterior cruciate ligament. There is an intrinsic
eccentric muscular component in almost all standard rehabilitation exercises.
However, a key point to consider in this study was that the resultant muscular
response of hypertrophy most likely corresponds to the magnitude of overload
experienced by the muscle. Standard exercises proved beneficial, as evidenced
by improvements in quadriceps volume of approximately 10% after twelve weeks
of rehabilitation. While this muscular response was favorable, overloading the
quadriceps progressively through focused eccentric training safely induced
hypertrophic changes that were more than two-fold greater than those following
the standard rehabilitation.
Although originally we had no intention of evaluating gluteus maximus
structure, it is interesting to compare and contrast the responses of the
quadriceps and gluteus maximus to eccentric training between surgical graft
types. Subject characteristics differed between the grafts, with the
semitendinosus-gracilis cohort consisting of patients who were slightly less
active (average Tegner score, 6.2 points compared with 7.3 points in the other
graft cohort) and older (35.3 compared with 23.2 years of age). However,
despite these differences, progressive eccentric exercise produced
substantially greater increases in the sizes of the quadriceps and gluteal
muscles of both lower extremities when compared with the increases found after
standard rehabilitation. The amount of improvement, however, appeared somewhat
graft-specific. In the eccentric-exercise group, the quadriceps and gluteus
maximus volumes improved 26.7% and 21.6%, respectively, in the
semitendinosus-gracilis cohort compared with 19.8% and 29.1%, respectively, in
the bone-patellar tendonbone cohort.
Whichever graft was used, the gluteus maximus appeared to have recovered
more completely than the quadriceps by fifteen weeks after surgery when the
uninjured extremity was used for comparison. The size increase in the gluteus
maximus may coincide with the increase in hip extensor strength reported after
hamstring reconstruction of the anterior cruciate
ligament33. These
structural results also lend anatomic support to the findings of kinetic
studies, which have often demonstrated greater hip extension moments and
reduced knee extension moments following reconstruction of the anterior
cruciate
ligament34,35.
While the eccentric-exercise paradigm used in this study appears excellent for
inducing hypertrophy of the quadriceps and gluteus maximus muscles, it does
not appear to prevent imbalances from developing between the knee and hip
extensor muscles following reconstruction of the anterior cruciate
ligament.
Our secondary hypothesis was that there would be no difference in the
improvement in the hamstring or gracilis volume in the involved thigh between
rehabilitation groups. Our results supported this hypothesis. Because the
eccentric intervention was largely a quadriceps-dominated exercise, it was not
surprising that the two rehabilitation groups would be similar with regard to
hamstring or gracilis structural changes. There were differences, however, in
hamstring and gracilis changes between graft types, most likely as a result of
graft site morbidity. In a detailed morphological study, Williams et
al.17 found an
overall reduction in hamstring volume of 11% approximately six months
following reconstruction of the anterior cruciate ligament with an autologous
semitendinosus-gracilis graft but reported a >30% reduction in
semitendinosus volume. We did not analyze each hamstring muscle separately;
however, on the basis of visual inspection
(Fig. 2) we believe that our
results would have been similar.
Structural changes in the gracilis also appeared to be graft-dependent.
Gracilis volume improved marginally in the bone-patellar tendon-bone cohort,
but it decreased substantially in the semitendinosus-gracilis cohort. A
reduction in muscle volume of nearly 20% was already evident three weeks after
surgery and it increased to a deficit of 35% just twelve weeks later.
Intriguingly, only a 4% reduction in the peak cross-sectional area was
observed three weeks after surgery; this increased to 15% by the time of the
posttraining follow-up assessment. These structural findings were consistent
with those reported by Williams et
al.17. Also, this
large deficit in gracilis muscle structure seems to coincide with deficits in
hip adductor strength reported after this surgical
procedure33.
Short-term studies have consistently demonstrated substantial reductions in
the hamstring and gracilis muscles following reconstruction of the anterior
cruciate ligament with an autologous semitendinosus-gracilis
graft11,17,18,36,
but long-term studies have not been conducted to determine the extent of
recovery of hamstring or gracilis structure, to our knowledge. Because several
investigators have observed persistent hamstring strength deficits after this
type of
surgery12,36,37,
one might anticipate discovering parallel hamstring structural deficits as
well. It would also be interesting to determine whether targeted eccentric
training for the hamstrings (and possibly the gracilis) would result in
positive structural adaptations similar to those observed in the quadriceps
and the gluteus maximus in our study.
Our final hypothesis was that there would be significantly greater
improvement in the quadriceps volume and peak cross-sectional area in the
uninvolved thigh in the eccentric-exercise group but there would be no
difference between groups with regard to the hamstring or gracilis structure
in the uninvolved thigh. Our results support this hypothesis. While eccentric
ergometry did not significantly affect the hamstring or gracilis muscle of the
uninvolved thigh, the intervention did induce an 11% increase in the
quadriceps and gluteus maximus volumes. Williams et
al.17 reported
minimal differences between any muscle volumes or peak cross-sectional areas
in the uninvolved lower extremity before and after surgery.
It should be considered beneficial to increase muscle size and strength in
the uninvolved thigh after surgery. However, when the uninvolved side
improves, outcome measures based on a comparison of the involved and
uninvolved sides are negatively affected. In this study, for example, without
the 11% improvement in the size of the quadriceps in the uninvolved thigh, the
volume index would have been 92.4 instead of 83.1. Researchers assessing
outcomes often focus on comparing the muscle size, strength, and performance
ability of the injured extremity with those of the "normal,"
uninjured extremity. The assumption seems to be that the uninjured extremity
is "normal," thereby providing a valid comparison for the injured
extremity. We believe that this assumption is not necessarily true after an
injury and reconstruction of the anterior cruciate ligament and that in many
cases, including the subject in our recent case
report20, the
"normal" limb is also deconditioned and atrophied (albeit to a
lesser extent) as a result of a large decrease in the person's typical
activity.
In this study, there was considerable variability in the improvement in the
quadriceps volume among patients. Several potential confounding factors that
ultimately could have influenced a muscle's ability to hypertrophy were also
identified (for example, knee pain, lack of range of motion, effusion,
compliance, and the amount of pretraining atrophy). In the
semitendinosus-gracilis graft cohort, it is difficult to ascertain why the
quadriceps mass of the outlier in the eccentric-exercise group did not improve
like the others. This individual complied with the exercise program and
produced exceptional negative work values during training. However, because he
did not have a great amount of atrophy after the surgery (a pretraining volume
index of 91.3), he consequently had less potential for improvement. This
relationship was reflected by the negative correlation between improvement in
quadriceps volume and the pretraining volume index (r = —0.47;
r2 = 0.22). Essentially, those who began training with a higher
quadriceps volume index (less atrophy) had less improvement at the time of
follow-up. Another person in the eccentric-exercise group, with demographic
characteristics and negative work output values that were nearly identical to
those of the outlier, had a pretraining volume index of 91.1. That person
demonstrated improvement in the quadriceps volume of nearly 21%. Therefore, we
are uncertain why these two individuals in the eccentric-exercise group
differed. The outlier in the standard-rehabilitation group was one of the
youngest and most active patients (as indicated by the preinjury Tegner score)
in the study. She had substantial quadriceps atrophy three weeks after the
surgery (a volume index of 71.2) so one might have predicted an above-average
increase in quadriceps volume after twelve weeks of rehabilitation. However,
the improvement in quadriceps volume (39.3%) was more than twice that of any
other patient in the standard-rehabilitation group and the improvement in
hamstring volume (22.5%) was more than ten times greater than the average in
the semitendinosus-gracilis graft cohort. Standard rehabilitation exercise
typically requires the muscle to work both concentrically (pushing and
overcoming a resistance) and eccentrically (pushing but yielding to the same
resistance)38. This
subject, however, reported doing the concentric portion (i.e., of the leg
press) bilaterally and the eccentric portion unilaterally. She stated that the
applied resistance was "more than I could do with one leg alone."
It would be compelling to credit her extraordinary results to eccentric
training, but we cannot draw such conclusions from this study. Other factors
such as pretraining atrophy, age, or preinjury activity level may have
contributed considerably.
In the bone-patellar tendon-bone cohort, the worst result in the
standard-rehabilitation group and second worst in the eccentric-exercise group
occurred in individuals who struggled to gain full passive knee extension
(ultimately falling 3° to 5° short) and who experienced
mild-to-moderate anterior knee pain throughout training. The person with the
second worst result in the standard-rehabilitation group was not highly
compliant with the weight-lifting regimen during the training period. The
worst result in the eccentric-exercise group was in an individual who
sustained two blunt injuries to the knee (from slipping on ice and landing on
the knee) three weeks apart during the study period. Thus, rehabilitation
following reconstruction of the anterior cruciate ligament is multifaceted,
with outcomes being affected by a myriad of factors.
The current study had several limitations. Rehabilitation guidelines were
provided for both groups, but postoperative activity levels were not
documented even though differences in total activity between individuals can
be confounding. A more detailed description of weight-lifting-specific
activities would have been useful. While attempts were made to treat both
groups equally, there was no way to completely blind patients to their
treatment-group assignment. Although the study was appropriately powered, the
sample size was small, and there were substantial differences between the
graft types that limit generalizability. Finally, perhaps the greatest
limitation of the study is that the outcomes that we reported were short-term.
It is unknown whether the positive structural changes observed in this study
will result in long-term benefits in terms of muscle size, strength, or
performance. However, the considerable clinical attention and effort toward
mitigating quadriceps atrophy and weakness during the first three months
following reconstruction of the anterior cruciate ligament suggest that this
is an essential time period for restoring muscle structure and function. At
the time of writing, we were collecting data on this cohort one year after
surgery to further understand the effects of eccentric training after
reconstruction of the anterior cruciate ligament.
In conclusion, this study demonstrated that progressive eccentric
resistance exercise implemented three weeks after reconstruction of the
anterior cruciate ligament can induce changes in the structure of the
quadriceps and gluteus maximus that greatly exceed (by more than twofold)
those changes following an institutional standard rehabilitation program.
These structural increases were observed in both the involved and the
uninvolved thighs and with both the semitendinosus-gracilis and the
bone-patellar tendon-bone grafts. The gradual and progressive exposure to
negative work allowed the patients in this study to safely increase the
intensity of eccentric training and greatly enhance structural changes of the
quadriceps and gluteus maximus. Because the forces produced across a muscle
during negative work are of the greatest magnitude of any muscle action, an
eccentric intervention may be ideal for mitigating the persistent muscle
impairments commonly observed after reconstruction of the anterior cruciate
ligament.
Tables showing preoperative patient characteristics, muscle volume data,
and patient functional status measures are available with the electronic
versions of this article, on our web site at
(go to
the article citation and click on "Supplementary Material") and on
our quarterly CD-ROM (call our subscription department, at 781-449-9780, to
order the CD-ROM). ?
Note: The authors thank Glenn Williams for reviewing the
manuscript and Barry Shultz for statistical consultation.
Elmqvist LG, Lorentzon R, Johansson C,
Langstrom M, Fagerlund M, Fugl-Meyer AR. Knee extensor muscle function before
and after reconstruction of anterior cruciate ligament tear. Scand J
Rehabil Med. 1989;21:
131-9.21131
1989
[PubMed]
Feller JA, Webster KE. A randomized
comparison of patellar tendon and hamstring tendon anterior cruciate ligament
reconstruction. Am J Sports Med.
2003;31:
564-73.31564
2003
[PubMed]
Meighan AA, Keating JF, Will E. Outcome
after reconstruction of the anterior cruciate ligament in athletic patients. A
comparison of early versus delayed surgery. J Bone Joint Surg
Br. 2003;85:
521-4.85521
2003
[CrossRef]
Snyder-Mackler L, Ladin Z, Schepsis AA,
Young JC. Electrical stimulation of the thigh muscles after reconstruction of
the anterior cruciate ligament. Effects of electrically elicited contraction
of the quadriceps femoris and hamstring muscles on gait and on strength of the
thigh muscles. J Bone Joint Surg Am.
1991;73:
1025-36.731025
1991
[PubMed]
Grant JA, Mohtadi NG, Maitland ME,
Zernicke RF. Comparison of home versus physical therapy-supervised
rehabilitation programs after anterior cruciate ligament reconstruction: a
randomized clinical trial. Am J Sports Med.
2005;33:
1288-97.331288
2005
[PubMed][CrossRef]
Risberg MA, Holm I, Steen H, Eriksson J,
Ekeland A. The effect of knee bracing after anterior cruciate ligament
reconstruction. A prospective, randomized study with two years' follow-up.
Am J Sports Med. 1999;27:
76-83.2776
1999
[PubMed]
Anderson JL, Lamb SE, Barker KL, Davies
S, Dodd CA, Beard DJ. Changes in muscle torque following anterior cruciate
ligament reconstruction: a comparison between hamstrings and patella tendon
graft procedures on 45 patients. Acta Orthop Scand.
2002;73:
546-52.73546
2002
[PubMed][CrossRef]
Arangio GA, Chen C, Kalady M, Reed JF
3rd. Thigh muscle size and strength after anterior cruciate ligament
reconstruction and rehabilitation. J Orthop Sports Phys Ther.
1997;26:
238-43.26238
1997
[PubMed]
Bach BR Jr, Jones GT, Sweet FA, Hager
CA. Arthroscopy-assisted anterior cruciate ligament reconstruction using
patellar tendon substitution. Two- to four-year follow-up results. Am J
Sports Med. 1994;22:
758-67.22758
1994
[CrossRef]
Ejerhed L, Kartus J, Sernert N, Kohler
K, Karlsson J. Patellar tendon or semitendinosus tendon autografts for
anterior cruciate ligament reconstruction? A prospective randomized study with
a two-year follow-up. Am J Sports Med.
2003;31:
19-25.3119
2003
[PubMed]
Eriksson K, Hamberg P, Jansson E,
Larsson H, Shalabi A, Wredmark T. Semitendinosus muscle in anterior cruciate
ligament surgery: morphology and function. Arthroscopy.
2001;17:
808-17.17808
2001
[PubMed][CrossRef]
Hamada M, Shino K, Horibe S, Mitsuoka T,
Miyama T, Shiozaki Y, Mae T. Single-versus bi-socket anterior cruciate
ligament reconstruction using autogenous multiple-stranded hamstring tendons
with EndoButton femoral fixation: a prospective study.
Arthroscopy. 2001;17:
801-7.17801
2001
[PubMed][CrossRef]
Jansson KA, Linko E, Sandelin J,
Harilainen A. A prospective randomized study of patellar versus hamstring
tendon autografts for anterior cruciate ligament reconstruction. Am J
Sports Med. 2003;31:
12-8.3112
2003
Jarvela T, Kannus P, Latvala K, Jarvinen
M. Simple measurements in assessing muscle performance after an ACL
reconstruction. Int J Sports Med.
2002;23:
196-201.23196
2002
[PubMed][CrossRef]
Mattacola CG, Perrin DH, Gansneder BM,
Gieck JH, Saliba EN, McCue FC 3rd. Strength, functional outcome, and postural
stability after anterior cruciate ligament reconstruction. J Athl
Train. 2002;37:
262-8.37262
2002
Rosenberg TD, Franklin JL, Baldwin GN,
Nelson KA. Extensor mechanism function after patellar tendon graft harvest for
anterior cruciate ligament reconstruction. Am J Sports Med.
1992;20:
519-26.20519
1992
[PubMed][CrossRef]
Williams GN, Snyder-Mackler L, Barrance
PJ, Axe MJ, Buchanan TS. Muscle and tendon morphology after reconstruction of
the anterior cruciate ligament with autologous s6emitendinosus-gracilis graft.
J Bone Joint Surg Am.
2004;86:
1936-46.861936
2004
[PubMed]
Irie K, Tomatsu T. Atrophy of
semitendinosus and gracilis and flexor mechanism function after hamstring
tendon harvest for anterior cruciate ligament reconstruction.
Orthopedics. 2002;25:
491-5.25491
2002
[PubMed]
Lindstedt SL, LaStayo PC, Reich TE. When
active muscles lengthen: properties and consequences of eccentric
contractions. News Physiol Sci.
2001;16:
256-61.16256
2001
[PubMed]
Gerber JP, Marcus RL, Dibble LE, Greis
PE, LaStayo PC. Early application of negative work via eccentric ergometry
following anterior cruciate ligament reconstruction: a case report. J
Orthop Sports Phys Ther. 2006;36:
298-307.36298
2006
Hortobagyi T, Dempsey L, Fraser D, Zheng
D, Hamilton G, Lambert J, Dohm L. Changes in muscle strength, muscle fibre
size and myofibrillar gene expression after immobilization and retraining in
humans. J Physiol.
2000;524:
293-304.524293
2000
[PubMed][CrossRef]
LaStayo PC, Ewy GA, Pierotti DD, Johns
RK, Lindstedt S. The positive effects of negative work: increased muscle
strength and decreased fall risk in a frail elderly population. J
Gerontol A Biol Sci Med Sci.
2003;58:
M419-24.58M419
2003
LaStayo PC, Pierotti DJ, Pifer J,
Hoppeler H, Lindstedt SL. Eccentric ergometry: increases in locomotor muscle
size and strength at low training intensities. Am J Physiol Regul
Integr Comp Physiol. 2000;278:
R1282-8.278R1282
2000
Hortobagyi T, Hill JP, Houmard JA,
Fraser DD, Lambert NJ, Israel RG. Adaptive responses to muscle lengthening and
shortening in humans. J Appl Physiol.
1996;80:
765-72.80765
1996
[PubMed]
Hortobagyi T, Barrier J, Beard D,
Braspennincx J, Koens P, Devita P, Dempsey L, Lambert J. Greater initial
adaptations to submaximal muscle lengthening than maximal shortening. J
Appl Physiol. 1996;81:
1677-82.811677
1996
Gerber JP, Marcus RL, Dibble LE, Greis
PE, Burks RT, LaStayo PC. Safety, feasibility and efficacy of negative work
exercise via eccentric muscle activity following anterior cruciate ligament
reconstruction. J Orthop Sports Phys Ther.
2007;37:
10-18.3710
2007
[PubMed][CrossRef]
Tegner Y, Lysholm J. Rating systems in
the evaluation of knee ligament injuries. Clin Orthop Relat
Res. 1985;198:
43-9.19843
1985
Swenson TM. Endoscopic anterior cruciate
ligament reconstruction using a double looped hamstring tendon graft. In:
Harner CD, Vince KG, Fu FH, editors. Techniques in knee
surgery. Philadelphia: Lippincott Williams and Wilkins;
2001. p 57-72.57
2001
Bach BB. Endoscopic ACL reconstruction
with patellar tendon substitution. In: Harner CD, Vince KG, Fu FH, editors.
Techniques in knee surgery. Philadelphia: Lippincott Williams
and Wilkins; 2001. p 41-56.41
2001
Lastayo PC, Reich TE, Urquhart M,
Hoppeler H, Lindstedt SL. Chronic eccentric exercise: improvements in muscle
strength can occur with little demand for oxygen. Am J Physiol.
1999;276:
R611-5.276R611
1999
[PubMed]
Noble BJ, Borg GA, Jacobs I, Ceci R,
Kaiser P. A category-ratio perceived exertion scale: relationship to blood and
muscle lactates and heart rate. Med Sci Sports Exerc.
1983;15:
523-8.15523
1983
[PubMed]
Tracy BL, Ivey FM, Jeffrey Metter E,
Fleg JL, Siegel EL, Hurley BF. A more efficient magnetic resonance
imaging-based strategy for measuring quadriceps muscle volume. Med Sci
Sports Exerc. 2003;35:
425-33.35425
2003
[CrossRef]
Hiemstra LA, Gofton WT, Kriellaars DJ.
Hip strength following hamstring tendon anterior cruciate ligament
reconstruction. Clin J Sport Med.
2005;15:
180-2.15180
2005
[PubMed][CrossRef]
Ferber R, Osternig LR, Woollacott MH,
Wasielewski NJ, Lee JH. Gait mechanics in chronic ACL deficiency and
subsequent repair. Clin Biomech (Bristol, Avon).
2002;17:
274-85.17274
2002
[PubMed][CrossRef]
Salem GJ, Salinas R, Harding FV.
Bilateral kinematic and kinetic analysis of the squat exercise after anterior
cruciate ligament reconstruction. Arch Phys Med Rehabil.
2003;84:
1211-6.841211
2003
[PubMed][CrossRef]
Aune AK, Holm I, Risberg MA, Jensen HK,
Steen H. Four-strand hamstring tendon autograft compared with patellar
tendon-bone autograft for anterior cruciate ligament reconstruction. A
randomized study with two-year follow-up. Am J Sports Med.
2001;29:
722-8.29722
2001
[PubMed]
Marder RA, Raskind JR, Carroll M.
Prospective evaluation of arthroscopically assisted anterior cruciate ligament
reconstruction. Patellar tendon versus semitendinosus and gracilis tendons.
Am J Sports Med. 1991;19:
478-84.19478
1991
[PubMed][CrossRef]
Kraemer WJ, Adams K, Cafarelli E, Dudley
GA, Dooly C, Feigenbaum MS, Fleck SJ, Franklin B, Fry AC, Hoffman JR, Newton
RU, Potteiger J, Stone MH, Ratamess NA, Triplett-McBride T; American College
of Sports Medicine. American College of Sports Medicine position stand.
Progression models in resistance training for healthy adults. Med Sci
Sports Exerc. 2002;34:
364-80.34364
2002
[CrossRef]