Keywords anterior cruciate ligament - mechanoreceptors - proprioception - stabilometry - knee
ligament laxity - knee outcome scores
Introduction
The central nervous system receives a collective neural input from peripheral receptors
found within joints, ligaments, tendons, muscles, and skin.[1 ]
[2 ]
[3 ]
[4 ] The anterior cruciate ligament (ACL) contains mechanoreceptors and free nerve endings.
The latter are more abundant and function as nociceptors, reacting to joint inflammation
and pain stimuli. The mechanoreceptors found in the ACL include Pacinian corpuscles
(quick adapting receptors activated by compression and mediate kinesthesia), Ruffini
endings, and Golgi tendon organs (slow adapting receptors activated by stretch and
mediate joint position sense).[4 ]
[5 ]
[6 ] These receptors signal potentially harmful deformations of the ligaments and knee
joint via proprioceptive feedback which constitutes the afferent arc input. Protective
reflexes intended to resist the injurious movements, such as reflex muscular stabilization,
are initiated via efferent responses (Hilton's law).[6 ]
In addition to its proprioceptive role, the ACL is the primary restraint to anterior
tibial translation and a major secondary restraint to internal rotation, thereby contributing
to the normal kinematics of the knee.[7 ]
[8 ]
[9 ]
[10 ] Rupture of the ACL can lead to mechanical instability resulting in pathological
displacement of the tibia relative to the femur. This may give rise to progressive
instability, which can result in meniscal tears and early arthritis.[11 ]
[12 ]
[13 ] ACL reconstruction can be performed in order to restore mechanical knee stability.
Following reconstruction, there are some patients who have a persistent laxity on
clinical examination but, nonetheless, return to their preinjury level of activities.
There are also some patients who have a clinically stable knee postoperatively but
remain unsatisfied and continue to perceive a feeling of instability in their knee.
Proprioception testing may be a superior end-point of quantifying a successful outcome
following ACL reconstruction than clinically observed ligament laxity testing.
We conducted a prospective longitudinal study analyzing knee proprioception using
dynamic single-leg stance postural stabilometry. The primary aim of the study was
to evaluate if a proprioceptive deficit exists in patients with ACL ruptures, either
compared to their contralateral knee or to normal controls. The secondary aim of the
study was to investigate if there was an improvement following ACL reconstruction
if a preoperative proprioceptive deficit was present. The tertiary aim of the study
was to assess if a correlation existed between proprioceptive function, instrumented
ligament laxity testing, and clinical outcome measures.
Materials and Methods
Full approval was received for the study from the Research Ethics Committee and the
Research Governance Committee. All subjects signed informed consent forms to participate.
This therapeutic study is a prospective longitudinal case-control study which formed
part of the first author's doctorate thesis.
There was a total of 100 subjects recruited to the study. [Table 1 ] shows their demographic details. The mean time from injury to clinic review for
the ACL group was 63 weeks (SD = 59). [Fig. 1 ] shows the mechanism of injury of the ACL group. An ACL rupture was diagnosed by
clinical history and examination as well as magnetic resonance imaging (MRI) scan
of the injured knee for all patients in the ACL group. The diagnosis was confirmed
at the time of knee arthroscopy. The patients in the ACL group had a normal contralateral
knee confirmed by clinical history and examination. [Fig. 2 ] illustrates the flow of the patients in the ACL group through the study. Four patients
with delayed surgical intervention postponed their operation for personal reasons
(i.e., work or university commitments). One patient was recruited to the ACL group
and underwent all the assessments except for the proprioception analysis as the equipment
was unavailable at the time of the patient's attendance. However, the data for the
remaining assessments that they did undergo are still included in the relevant sections.
Of the 34 patients who underwent ACL reconstruction, 25 had an ipsilateral middle
third bone-patella tendon-bone autograft, and 9 had an ipsilateral quadrupled hamstring
autograft. At the time of surgery in the ACL group, 11 patients were found to have
a concomitant medial meniscal tear, 8 patients had a lateral meniscal tear, and 11
subjects had both a medial and a lateral meniscal tear. All patients with concurrent
meniscal tears also underwent a partial meniscectomy. None of the patients had significant
associated articular cartilage lesions. The mean time to follow-up was 14 weeks (SD = 4)
following surgery.
Table 1
ACL group
Control group
(n = 50)
(n = 50)
Mean age (yrs) (SD)
30 (9)
25 (5)
Male: female
36:14
35:15
Injured knee (right: left)
24:26
—
Mean height (m) (SD)
1.72 (0.1)
1.75 (0.1)
Mean weight (kg) (SD)
78.1 (14.4)
76.1 (14.4)
Mean BMI* (kg/m2 ) (SD)
26.2 (3.8)
24.6 (3.4)
Fig. 1 Mechanism of injury ACL group (n = 50),
Fig. 2 Flow of subjects through the study.
[Fig. 2 ] illustrates the flow of the subjects in the control group through the study. All
the participants in the control group had normal knees confirmed by clinical history
and examination of both knees as well as an MRI scan of one knee. The control group
data was also used as the normal controls in other published studies.[14 ]
[15 ]
Subjects who were 16 to 45 years of age were included. Participants were excluded
from the study if there was a concomitant posterior cruciate ligament (PCL), medial
collateral ligament (MCL) or lateral collateral ligament (LCL) tear of the knee, significant
history of ankle or hip pathology, lumbar spine symptoms (including radiculopathy
in either limb), neurological or vestibular disease, diabetes, or regular use of opiate
analgesics. In addition, subjects were excluded from the control group if there was
a significant history of any knee pathology.
The Rolimeter knee arthrometer (Aircast Incorporated, Summit, NJ, USA) was used to
measure quantitatively the anterior displacement of the tibia relative to the femur
of both knees in both groups. The maximum manual instrumented test was used to measure
ligament laxity in both the Lachman test (20° knee flexion) and the anterior drawer
test (90° knee flexion) ([Fig. 3 ]). The registered anterior displacement (in mm) was used for statistical analysis.
Fig. 3 The Rolimeter knee arthrometer (A) Lachman test (B) Anterior drawer test.
All subjects of both groups were assessed using the Tegner activity score[16 ] and the Lysholm knee score.[16 ]
The Biodex Balance SD System (Biodex Medical Systems Incorporated, Shirley, NY, USA)
was used to quantitatively measure postural stability ([Fig. 4 ]). It has been validated for its use in assessing dynamic single-leg postural stability.[17 ]
[18 ]
[19 ] Stabilometry is an accepted method of measuring proprioception in the ACL deficient
knee.[20 ]
[21 ] The Biodex Balance SD System consists of a multiaxial moveable platform which computes
an output in the form of an overall stability index (OSI). A low score indicates that
the subject has good postural stability (and, therefore, good proprioception), and
a high score reflects poorer stability and proprioception. Each leg in all the participants
(in bare feet) was assessed 3 times for a duration of 20 seconds for each test period.
The computer output for each leg was calculated from the average of the three tests.
The mean OSI result was used as the quantitative measure of proprioception for the
purpose of statistical analyses.
Fig. 4 Single-leg stance postural stability testing using the Biodex Balance SD System.
Statistical Analysis
A post-hoc power calculation for this study was derived from the results of the longitudinal
within-group analysis of the ACL group injured knee log (OSI) (primary outcome) as
detailed in [Table 4 ]. The sample size of 34 subjects based on a conventional type I error of 5% with
a within-group mean difference of 0.23 and a within-group standard deviation of 0.40
yielded a statistical power calculation of 90.2% for this study. All data variables
for both groups displayed a normal distribution (verified by both plotted histograms
and the Shapiro-Wilks test) except for the OSI measurements (negatively skewed distribution).
Data transformation was implemented using the natural logarithm following which the
log (OSI) data demonstrated a normal distribution and was used for the purposes of
statistical calculations using the appropriate parametric tests. The level of statistical
significance was set at p < 0.05. Statistical analysis was performed using the SPSS for Windows, version 25.0
(IBM Corp., Armonk, NY, USA). The power calculation was performed using the Minitab
statistical software version 19 (Minitab LLC, State College, PA, USA).
Results
[Figs. 5 ] and [6 ] illustrate the findings of the instrumented ligament laxity measurements of both
the Lachman test and the anterior drawer test respectively, and [Table 2 ] shows the results of their statistical analyses. There was no significant difference
between the right and left knees of the control group for either the Lachman test
(p = 0.53; 95% CI -0.50, 0.26) or the anterior drawer test (p = 0.32; 95% CI -0.10, 0.30). There was a significant difference of both tests when
comparing the injured knee of the ACL group preoperatively to their uninjured knee
and that of the control group. Following surgery, the injured knee of the ACL group
showed a significant improvement compared to preoperative findings but still had a
significant difference compared to their uninjured knee and the control group.
Fig. 5 Instrumented ligament laxity measurement for the Lachman test displaying means and
standard errors.
Fig. 6 Instrumented ligament laxity measurement for the anterior drawer test displaying
means and standard errors.
Table 2
Uninjured knee[a ]
Control group[b ]
Injured knee postop[a ]
p -value (95%CI)
p -value (95%CI)
p -value (95%CI)
Lachman
Injured knee preop.
< 0.001* (4.6, 6.2)
< 0.001* (5.2, 7.3)
< 0.001* (1.0, 2.5)
Injured knee postop.
< 0.001* (1.4, 3.1)
< 0.001* (3.7, 5.4)
—
Anterior Drawer
Injured knee preop.
< 0.001* (4.3, 5.8)
< 0.001* (5.4, 7.8)
0.001* (0.9, 3.3)
Injured knee postop.
< 0.001* (1.5, 3.1)
< 0.001* (3.4, 5.2)
—
[Table 3 ] shows the results of the knee outcome scores for the ACL group. There was a significant
improvement postoperatively of both the Tegner activity score and the Lysholm score.
A significant difference persisted between the preinjury and postoperative Tegner
activity scores.
Table 3
Preoperative
Postoperative
p -value[a ] (95% CI)
Mean (SD)
Mean (SD)
Lysholm
71.7 (12.8)
85.3 (10.5)
< 0.001 (8,18–19,18)
Tegner
3.3 (1.2)
4.1 (0.2)
0.006 (0,23–1,28)
Preinjury
Postoperative
Tegner
6.7 (1.3)
4.1 (0.2)
< 0.001 (2,11–3,31)
[Table 4 ] shows the proprioception measurements for the ACL and the control groups. The results
of their statistical analyses are shown in [Table 5 ]. There was no significant difference found between the right and left knees of the
control group (p = 0.42; 95% CI -0.04, 0.10). There was no significant difference found of the uninjured
knee in the ACL group between preoperative and postoperative results (p = 0.28; 95% CI -0.05, 0.19). There was a statistically significant difference between
the injured knee of the ACL group preoperatively when compared to their uninjured
knee and also to the control group. There was no significant difference found between
the uninjured knees of the ACL and the control groups. There was a statistically significant
improvement in proprioception of the injured knee in the ACL group compared to preoperative
findings following ACL reconstruction, to the extent that no significant difference
was found between their operated knee and either their uninjured knee or the control
group.
Table 4
Group
Mean (SD)
ACL group preoperatively (n = 49)
Injured knee
0.70 (0.45)
Uninjured knee
0.46 (0.35)
ACL Group postoperatively (n = 34)
Injured knee
0.47 (0.40)
Uninjured knee
0.42 (0.39)
Control group (n = 50)
Right knee
0.49 (0.35)
Left knee
0.52 (0.34)
Table 5
Uninjured knee[a ]
Control group[b ]
Injured knee postop[a ]
p -value (95%CI)
p -value (95%CI)
p -value (95%CI)
Injured knee preop.
< 0.001* (0.14, 0.34)
0.01* (0.05, 0.38)
0.003* (0.10, 0.42)
Uninjured knee
—
0.73 (-0.16, 0.12)
—
Injured knee postop.
0.25 (-0.03, 0.13)
0.85 (-0.18, 0.15)
—
[Table 6 ] shows the results of the Pearson correlation analyses between knee outcome scores,
stabilometry and ligament laxity measurements of the injured knee of the ACL group.
Preoperatively, proprioception measurements had a significant (inversely proportional)
correlation with both knee outcome scores. A higher knee outcome score (i.e., better
function) was associated with a lower log (OSI) score (i.e., good proprioception).
There was no significant correlation between ligament laxity measurements and proprioception.
Postoperatively, there were no statistically significant correlations between any
of these variables.
Table 6
Pre operative
Post operative
Log (OSI)
Lachman
Anterior drawer
log (OSI)
Lachman
Anterior drawer
r / p -value[a ]
r / p -value[a ]
r / p -value[a ]
r / p -value[a ]
r / p -value[a ]
r / p -value[a ]
95% CI
95% CI
95% CI
95% CI
95% CI
95% CI
Lachman
0.07 / 0.630
——-
——-
-0.24 / 0.180
——-
——-
(-0.22, 0.34)
(-0.53, 0.11)
Anterior drawer
-0.07 / 0.640
——-
——-
0.09 / 0.620
——-
——-
(-0.34, 0.22)
(-0.26, 0.42)
Tegner
-0.42 / 0.003*
0.02 / 0.890
0.13 / 0.370
-0.12 / 0.500
-0.19 / 0.2900
-0.15 / 0.4200
(-0.63, -0.16)
(-0.27, 0.30)
(-0.16, 0.40)
(-0.44, 0.23)
(-0.50, 0.16)
(-0.46, 0.20)
Lysholm
-0.35 / 0.016*
-0.25 / 0.090
-0.20 / 0.180
-0.09 / 0.610
-0.22 / 0.230
-0.02 / 0.920
(-0.58, -0.07)
(-0.50, 0.04)
(-0.46, 0.09)
(-0.42, 0.26)
(-0.52, 0.13)
(-0.36, 0.32)
[Fig. 7 ] illustrates the scatterplot of the Pearson correlation analyses comparing pre and
postoperative proprioception measurements of the injured knee of the ACL group. A
significant (directly proportional) correlation was found demonstrating that low preoperative
log (OSI) scores were associated with low postoperative log (OSI) scores.
Fig. 7 Pearson product moment correlation analysis of proprioception measurements of the
injured knee of the ACL group before and after reconstruction.
Discussion
The results of this study found that there is a significant proprioceptive deficit
as measured by dynamic single-leg postural stabilometry in patients with an ACL rupture
as compared to their contralateral uninjured knee and to normal controls. ACL reconstruction
significantly improved proprioception to the level of normal controls. We found no
significant difference in proprioception between the uninjured knee of the ACL group
and that of the control group. Clinical outcome measures were found to have a better
correlation with proprioception than with instrumented ligament laxity testing.
Beard et al.[22 ] defined proprioception into three components; joint position sense (static awareness
of joint position in space), kinesthesia (detection of joint movement and acceleration),
and the efferent closed-loop reflex which regulates muscle stiffness. The complex
interactions between the afferent sensory and the efferent motor pathways are collectively
referred to as the sensorimotor system.[20 ] The present study measured proprioception using dynamic single-leg postural stabilometry,
which assesses both the afferent and the efferent neuromuscular pathways.[23 ] This has the advantage of assessing proprioception whilst the subjects are balancing
upright and is a more dynamic technique than the joint position sense (JPS) or threshold
to detection of passive movement (TDPM) testing methods, in which the subjects are
in the seated position.
The present study found a significant improvement of proprioceptive function at an
average of 14 weeks (approximately 3 months) following surgery. In other studies,
Iwasa et al.[24 ] showed that proprioception did not recover fully until 18 months after reconstruction,
Fremerey et al.[2 ] showed that proprioceptive recovery occurred 6 months after surgery while Reider
et al.[4 ] demonstrated an improvement of TDPM as compared to preoperative values as early
as 6 weeks following reconstruction. Graft reinnervation alone is unlikely to explain
a proprioceptive improvement as soon as 3 months after surgery in the present study.
A more probable explanation would be that ACL reconstruction provides a static restraint
and, thereby, improves the abnormal relationship between the femur and the tibia (i.e.,
abnormal knee kinematics) that exists in the ACL deficient knee. This, in turn, reduces
the abnormal neural output from the joint capsule and the remaining ligaments and
intraarticular structures of the knee.[4 ]
[24 ]
There was a significant improvement in ligament laxity measurements following ACL
reconstruction, but a significant difference remained as compared to their contralateral
uninjured knee and to normal controls. The present study found a significant improvement
of both validated knee outcome scores when the ACL group were reassessed 3 months
following surgery. Preoperatively, proprioception measurements were found to have
a significant correlation with both knees' outcome scores. There was no significant
correlation between the proprioception results and the instrumented ligament laxity
measurements. Ligament laxity had no correlation with either of the knee outcome scores.
This shows that proprioception is a better objective measure of knee impairment and
perceived functional stability than ligament laxity testing. Barrett[11 ] demonstrated that proprioception measured using JPS testing methods correlated well
with functional outcome and patient satisfaction and poorly with clinical ligament
testing.
However, postoperatively, proprioception had no significant correlation with any of
the outcome scores or ligament laxity measurements. An explanation for this is that
the outcome scores ask questions relating not only to activities of daily living,
which the patients may return to relatively early after surgery (such as walking and
returning to work), but also to running, sprinting, activities which involve cutting
movements, and return to competitive sport. Following an ACL reconstruction, patients
undergo a structured rehabilitation program which involves a gradual increase in activity
levels. Indeed, returning to full contact sport is prohibited until 9 months after
surgery, in the study's host. These aspects will have a bearing on the answers that
subjects can give to certain items in the outcome scores. Furthermore, a significant
difference between the preinjury and postoperative Tegner activity score was noted.
Therefore, a correlation may indeed exist between postoperative proprioception and
the knee outcome scores, but the analyses may have been obscured by the activity limiting
restrictions which were imposed on the patients at the early stages following their
surgery. A correlation analysis performed 9 months or later after surgery may have
yielded a different result.
There was a significant correlation between pre and postoperative proprioception measurements.
This relationship can help inform the surgeon that patients with an ACL rupture and
a good level of proprioceptive function prior to surgery are likely to have a good
functional outcome following an ACL reconstruction. Conversely, a patient with a poor
level of proprioceptive function prior to surgery is less likely to have as good a
postoperative functional outcome. The contrary can also be argued, that patients who
have a good level of proprioception following an ACL rupture maybe better candidates
for conservative treatment. The secondary stabilizers in their knee maybe sufficient
to allow satisfactory progress with a structured rehabilitation program back to a
premorbid level of sporting activity. Similarly, patients who have poor preoperative
proprioceptive acuity may require reconstructive surgery in order to protect the remaining
intact structures of the knee which are providing a degree of proprioceptive input
and prevent any further decline in this respect. [Fig. 8 ] summarizes the concept of proprioceptive deficits leading to further knee injuries
and the impact that an ACL reconstruction has in preventing further functional decline.
Fig. 8 The knee injury cycle. ACL reconstruction aims to improve proprioception and thereby
interrupt the cycle.
The weaknesses of this study include the length of time for the follow-up review following
surgery (approximately 3 months) and the number of subjects (16 patients) in the ACL
group that did not return for their postoperative assessment. There is also the possibility
that the structured rehabilitation program undertaken by the subjects postoperatively
may have played a significant role in the proprioceptive improvement.
Conclusion
The present study showed a significant proprioceptive deficit as measured by dynamic
single-leg postural stabilometry in patients with an ACL rupture that improved following
ligament reconstruction. The proprioceptive acuity of the uninjured contralateral
knee was similar to that of normal controls and is, therefore, an adequate comparator
for proprioception. Knee outcome scores had a better correlation with proprioception
analysis than instrumented ligament laxity measurements.
