Articles in PresS. J Appl Physiol (September 26, 2013). doi:10.1152/japplphysiol.00244.2013
1
1
Individuals with Medial Knee Osteoarthritis show Neuromuscular Adaptation when
2
Perturbed during Walking in spite of Functional and Structural Impairments
3
Deepak Kumar1,2; Charles (Buz) Swanik1,2; Darcy S. Reisman1,3; Katherine S Rudolph1,3
4
1
5
Delaware, Newark, DE
6
2
7
3
8
Corresponding Author and Request for Reprints:
9
Katherine Rudolph, PT, PhD
10
Associate Dean for Research,
11
Westbrook College of Health Professions
12
University of New England
13
716 Stevens Avenue, Portland, ME 04103
14
Ph: 207-221-4113, Email: [email protected]
15
Author Contributions:
16
Conception and Design: Kumar, Swanik, Reisman, Rudolph
17
Acquisition of data: Kumar
18
Analysis and Interpretation of Data: Kumar, Swanik, Reisman, Rudolph
19
Drafting and final approval of the article: Kumar, Swanik, Reisman, Rudolph
20
Running Head: Neuromuscular adaptation in medial knee osteoarthritis
Interdisciplinary Program in Biomechanics and Movement Sciences, University of
Kinesiology and Applied Physiology, University of Delaware, Newark, DE
Department of Physical Therapy, University of Delaware, Newark, DE
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
Copyright © 2013 by the American Physiological Society.
Neuromuscular adaptation in knee osteoarthritis
1
ABSTRACT
22
Neuromuscular control relies on sensory feedback that influences responses to changing
23
external demands, and the normal response is for movement and muscle activation patterns to
24
adapt to repeated perturbations. People with knee osteoarthritis (OA) are known to have pain,
25
quadriceps weakness and neuromotor deficits which could affect adaption to external
26
perturbations. The aim of this study was to analyze neuromotor adaptation during walking in
27
people with knee OA (n=38) and controls (n=23). Disability, quadriceps strength, joint space
28
width, malalignment and proprioception were assessed. Kinematic and EMG data were
29
collected during undisturbed walking and during perturbations which caused lateral
30
translation of the foot at initial contact. Knee excursions and EMG magnitudes were
31
analyzed. Subjects with OA walked with less knee motion and higher muscle activation; and
32
had greater pain, limitations in function, quadriceps weakness, and malalignment but no
33
difference was observed in proprioception. Both groups showed increased EMG and
34
decreased knee motion in response to the 1st perturbation followed by progressive decreased
35
EMG activity and increased knee motion during mid-stance over the first 5 perturbations, but
36
no group differences were observed. Over 30 trials, EMG levels returned to those of normal
37
walking.
38
individuals when exposed to challenging perturbations during functional weight-bearing
39
activities, in spite of structural, functional and neuromotor impairments.
40
underlying the adaptive response in people with knee OA need further study.
41
Keywords: Proactive response, motor control, EMG, reactive response, afferent feedback
42
43
44
45
The results illustrate that people with knee OA respond similarly to healthy
Mechanisms
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
21
Neuromuscular adaptation in knee osteoarthritis
2
INTRODUCTION
47
Knee osteoarthritis (OA) affects 16% of adults over 45 years of age (38) with majority of
48
people with knee OA having significant disability (23). The medial compartment of the knee
49
is most commonly affected by OA (12). Clinically, people with knee OA report significant
50
pain, stiffness and functional knee instability (FKI), all of which negatively impact activities
51
of daily living (ADL) and quality of life (QOL) (13, 21, 68). The OA disease process
52
involves morphological and compositional degeneration of all major knee tissues including
53
articular cartilage, meniscus, ligaments, subchondral/trabecular bone and muscles (10, 46, 49,
54
53, 60). It has also been suggested that people with knee OA have deficits in afferent and
55
efferent neural pathways demonstrated by decreases in proprioception, vibratory perception,
56
muscle force control and muscle strength (5, 6, 30, 34, 58, 71). Hence interventions that focus
57
on increasing muscle strength and those that aim at improving proprioception are included in
58
the management of individuals with knee OA (7, 20, 48, 78, 82, 83).
59
Presence of pain, damage to joint structures, and afferent and efferent neural deficits,
60
could impair the ability of the neuromuscular system to sense and execute appropriate
61
commands in response to external challenges to joint stability (31, 43). Interventions that rely
62
on improving proprioception or improving neuromuscular control aim to do so by using error
63
signals generated from external cues and clinician controlled external perturbations to induce
64
corrective reactions (3, 7, 19, 79). However, it is unknown if people with knee OA, who have
65
functional and structural impairments, are able to respond to external perturbations in a
66
manner similar to people without knee symptoms or radiographic evidence of OA.
67
Ability to modify movement and muscle activation patterns is commonly assessed as
68
a response to a series of external perturbations (24, 29, 52, 59, 62). Typical responses to
69
perturbations include feed-back (aka reactive) responses and feed-forward (aka proactive)
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
46
Neuromuscular adaptation in knee osteoarthritis
3
responses (37, 44, 52, 55, 57). Reactive responses occur during or shortly after a disturbance
71
in order to restore balance, whereas proactive responses are those that occur prior to the onset
72
of the disturbance and are thought to minimize the destabilization brought on by a
73
disturbance (52, 55, 57). Proactive responses represent the ability of the nervous system to
74
use sensory input to predict the effect of a disturbance and adjust the response accordingly
75
(76). Nielsen et al (54) suggested that error signals (difference in anticipated and actual
76
movement) generated from external perturbations during gait, when repeated, may constitute
77
a substrate for motor learning. Hence, an analysis of short-term adaptation of muscle
78
activations and movement patterns can provide insight into the ability of the nervous system,
79
in people with knee OA, to integrate sensory input and produce appropriate reactive and
80
proactive responses.
81
The aim of this study was to compare short term adaptation in muscle activation and
82
joint movement in response to repeated lateral perturbations during walking, between people
83
with and without radiographic and symptomatic knee OA. The operational definition of
84
adaptation in the context of this study was an increase in knee motion and /or a decrease in
85
the activation of muscles around the knee joint, over repeated exposure of the perturbation.
86
We hypothesized that people with radiographic and symptomatic knee OA would (1) show a
87
diminished response in movement and muscle activation patterns, as compared to controls,
88
when exposed to the first novel perturbation, and (2) show less adaptation in movement and
89
muscle activation patterns over repeated perturbations, as compared to controls.
90
EXPERIMENTAL PROCEDURES
91
Subjects: Thirty eight individuals with diagnosed medial knee OA and 23 individuals without
92
knee OA (Table 1) were referred from local physicians and recruited from the community
93
through advertisements.
Standing, semi-flexed, posterior-anterior and sunrise view
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
70
Neuromuscular adaptation in knee osteoarthritis
4
radiographs were taken of the more symptomatic knee in the OA subjects and in one knee of
95
the control subject (side chosen at random). Participants in the OA group had Kellgren and
96
Lawrence (K-L) grades of II or greater (39) in the medial tibiofemoral compartment and KL
97
grade in the medial compartment was greater than that of the lateral compartment. If the
98
participant had bilateral knee OA that fit the criteria, the more symptomatic knee was
99
identified by the individual and used in the analysis. Participants were excluded if they had a
100
history of other orthopedic injuries in the lower extremities (e.g., knee ligament injuries) or
101
spine, used an assistive device, had a history of neurologic injury, had a history of rheumatoid
102
arthritis, were pregnant, or had undergone a joint replacement or skeletal realignment
103
procedure in either lower extremity. All participants gave informed consent that was
104
approved by the Institutional Review Board of the University of Delaware.
105
Assessment of Disability:
106
Self-reported disability: The Knee injury and Osteoarthritis Outcome Score (KOOS), which
107
is a self-report measure of function that comprises 5 dimensions of knee function: Pain,
108
Symptoms, Activities of Daily Living (ADL), Sport and Recreation Function (Sport), and
109
Knee-Related Quality of Life (QOL) (47, 64) was used to assess function. Each dimension is
110
scored from 0 to 4, and then scores are transformed to a percentage score of 0 to 100, with 0
111
representing extreme knee problems and 100 representing no knee problems (64). The
112
KOOS has been shown to be a valid, reliable, and responsive measure of overall knee joint
113
function in people with OA (47). For this paper, KOOS subscales of symptoms, pain and
114
ADL were used.
115
Physical performance: A timed stair-climbing test was used where participants were timed
116
with a stopwatch as they ascended and descended a set of 12 stairs (18 cm high). The
117
participants were instructed to perform the task as quickly as they felt safe and comfortable.
118
They were encouraged not to use the handrail, but were not prohibited from doing so for
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
94
Neuromuscular adaptation in knee osteoarthritis
5
safety. A longer time to complete the stair climbing test represents worse functional
120
limitations. Excellent test-retest reliability (Pearson r=.93) was reported for a similar stair-
121
climbing task in people with knee OA (63).
122
Assessment of functional impairments:
123
Functional Knee Instability: FKI was assessed using the Knee Outcome Survey–Activities of
124
Daily Living Scale (36) (KOS-ADLS). One question from the KOS-ADLS relating to
125
functional stability of the knee has been shown to be a reliable measure of self-reported knee
126
instability in patients with knee OA (21). In this question, participants rated the severity of
127
knee instability on a 6-point scale in response to the question, “To what degree does giving
128
way, buckling, or shifting of your knee affect your level of daily activity?”. A score of < 4
129
indicates presence of FKI, a score of 4 indicated FKI that does not impact daily activities and
130
a score > 4 indicated absence of FKI.
131
Quadriceps strength : Quadriceps femoris muscle strength was measured as the magnitude
132
of the force output (in Newton) during a maximal voluntary isometric contraction (MVIC) at
133
90° knee flexion on an isokinetic dynamometer (Kin Com Isokinetic International, Harrison,
134
TN 37341, USA). Each participant practiced producing maximal quadriceps femoris muscle
135
contractions against the dynamometer arm while verbal encouragement and visual feedback
136
were provided to maximize volitional efforts. For the test, participants were asked to produce
137
an MVIC of their quadriceps femoris muscle and the highest trial with the greatest strength
138
(highest force in Newton) was used in the analysis. All strength data were normalized to the
139
subject’s BMI.
140
Proprioception: Threshold to detect passive motion (TTDPM) was measured on a custom
141
build device (Figure 1) with the subjects seated (75). The lower leg was secured in a
142
pneumatic sleeve to minimize cutaneous cues and headphones and blindfold were used to
143
eliminate auditory and visual cues, respectively. TTDPM was tested at 15° and 45° from end
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
119
Neuromuscular adaptation in knee osteoarthritis
6
144
of the subject’s available knee extension range. The subjects were given 3 practice trials. In
145
each recorded trial, the examiner tapped the subject on the shoulder to notify him/her that the
146
device would start moving in the next 10 seconds. At a random interval within the 10 sec, the
147
device passively flexed or extended the lower leg of the subject at a velocity of 0.5°/sec and
148
acceleration of 100°/sec2. When the subject perceived the knee movement they pressed a
149
hand held switch which disengaged the motor and the degree of rotation was recorded.
150
Average of three trials was taken. Previous studies using the proprioception testing device
151
have shown test-retest reproducibility of 0.92 (75).
153
Assessment of Structural Impairments:
154
Medial Joint Space Width: Medial joint space width was measured on a posterior-anterior
155
weight bearing semi-flexed radiograph as the narrowest distance between the femur and tibia
156
(42).
157
Alignment: Alignment was assessed using a standing, anterior- posterior radiograph in which
158
the hip, knee, and ankle joints were visible. Alignment was determined by the angle (varus
159
<180°, valgus >180°) of the mechanical axes of the femur and tibia (32).
160
The coefficient of variation for the radiographic measures for the same rater was < 3%.
161
162
Assessment of Response to Perturbations:
163
Motion Analysis: Subjects walked at their self-selected speed over-ground along a 13-m
164
walkway. Kinematic data were collected at 120Hz using a passive 8-camera system (VICON
165
MX, Oxford Metrics, Oxford, UK). Joint centers of the lower limb were defined using 9.5
166
mm retro-reflective markers placed bilaterally over the iliac crests, greater trochanters, lateral
167
femoral condyles, lateral malleolus, and 5th metatarsal heads. Rigid thermoplastic shells
168
affixed with four markers were attached to an elastic underwrap (SuperWrapTM, Fabrifoam,
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
152
Neuromuscular adaptation in knee osteoarthritis
7
Inc., Exton, PA 19341, USA) surrounding the thigh and shank. Both shank and thigh shells
170
were wrapped with CobanTM self-adherent wraps (3M, St. Paul, MN, USA ) to minimize
171
movement (51). A marker triad placed on the sacrum and two additional markers on the heel
172
counter of the subject’s shoe along with the marker on the 5th metatarsal head were used to
173
track pelvis and foot movement respectively. Inter- and intra-rater reliability was established
174
for marker placement in a 6 young healthy subjects. The inter class-coefficients for sagittal
175
and frontal plane variables were > 0.90.
176
Surface Electromyography: Muscle activity was recorded simultaneously at 1080 Hz using a
177
16-channel system (MA300, Motion Lab Systems, Baton Rouge, LA, USA). Pre-amplified
178
surface electrodes (20 mm inter-electrode distance, 12 mm disk diameter) were placed over
179
the mid-muscle belly of the semitendinosis (MH), biceps femoris (LH), vastus medialis
180
(MQ), vastus lateralis (LQ), and medial (MG) and lateral (LG) heads of the gastrocnemeii
181
(14). EMG signals during a maximum volitional isometric contraction (MVIC) and at rest
182
were recorded for each muscle for use during post-processing.
183
Disturbed Walking Paradigm: A custom-built, moveable platform (NSK Ltd, Tokyo, Japan)
184
imbedded in the walkway, was used to deliver the perturbations that consisted of a lateral
185
translation of 5.8 cm at a speed of 40 cm/s in response to a signal from a switch mat mounted
186
on the platform surface generated at initial contact (delay ≤ 10 msec, Figure 2).
187
perturbation paradigm has been used in earlier studies from our group (44, 67). The paradigm
188
is designed to challenge frontal plane stability in people with medial knee OA who are known
189
to have abnormal frontal plane mechanics (2, 74). Data were collected during 10 trials in
190
which the subject was aware that no movement would occur (“normal”). For safety, subjects
191
were allowed to observe the perturbation and if requested, they were allowed to perform 1
192
practice trial. No subject requested a practice trial. After 10 normal trials were collected
The
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
169
Neuromuscular adaptation in knee osteoarthritis
8
subjects were asked to continue walking at the same speed and during one of these trials the
194
platform would move causing a perturbation (P). The trial number in which the platform first
195
moved (P1) was randomized (between 1 -5 trials). After the first perturbation trial (P1) was
196
presented subjects were informed that the platform would move during all subsequent trials
197
and 5 consecutive perturbation trials were collected. After initial inspection of the data, it
198
appeared that adaptation continued beyond the 5th perturbed trial in some individuals.
199
Therefore, in order to assess if knee motion and muscle activity adapted to the extent that
200
they were no different from level walking values, we collected data from a total of 30
201
consecutive perturbations trials in a subset of subjects (Controls, n = 17 and OA, n = 14).
202
Data Management: Marker trajectories were low-pass filtered (Butterworth 4th order, phase
203
lag) with a cutoff frequency of 6 Hz using Visual 3D (C-Motion, Germantown, MD 20874,
204
USA). Three-dimensional joint kinematics were calculated using rigid body analysis and
205
Euler angles and referenced to the coordinate system from a standing posture. Sagittal plane
206
knee angle variables included – angle at initial contact, and excursions over two intervals:
207
loading response (from initial contact through peak knee flexion) and midstance (from peak
208
knee flexion angle through peak knee extension) (Figure 3).
209
EMG data were high pass filtered using a recursive 4th order Butterworth filter with a
210
cut-off of 20 Hz, full wave rectified and linear envelope created using a low pass 4th order
211
recursive Butterworth filter with a cut-off of 20 Hz (Visual 3D, C-Motion, Germantown, MD
212
20874, USA). The level of resting EMG was subtracted from the linear envelope data from
213
the active trials. The linear enveloped EMG data were then normalized to peak activity
214
collected from a maximum voluntary isometric contraction (MVIC) performed for each
215
muscle group so EMG data are reported as a percentage of the maximum (%Max). Linear
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
193
Neuromuscular adaptation in knee osteoarthritis
9
envelope data were averaged over the following intervals: pre-activation (100 ms prior to
217
initial contact), loading response and midstance (Figure 3).
218
Statistical Analyses:
219
Disability, functional impairments and structural impairments: Independent samples t-tests
220
were used compare subject demographics, KOOS scores, stair climbing test, quadriceps
221
strength, TTDPM, medial joint space width and alignment between the control and knee OA
222
groups. Prevalence of FKI was compared across the groups using a chi-square test.
223
Proactive and reactive responses to first 5 perturbations: A two-way mixed ANOVA was
224
used to compare the kinematic (knee angle at initial contact, flexion excursion, extension
225
excursion) and EMG (MQ, LQ, MH, LH, MG, LG) responses during Pre-activation, loading
226
response and midstance phases. The anlyses were performed using a between-group factor
227
[Group (2)] and a with-in group repeated factor [Trial (6)]. The 2 groups were controls and
228
OA. The 6 trials were level walk (x of 10 trials), and each of the first 5 perturbation trials (P1,
229
P2… P5). Paired t-tests were used for post-hoc comparisons of one trial to the next adjacent
230
trial in each of the groups.
231
In the subset of individuals who completed 30 perturbation trials, exploratory analyses
232
were done using a Group (2) by Trial (2) mixed ANOVA to compare the knee movement and
233
muscle activity during level walking with the amount of adaptation during the perturbations,
234
for the midstance phase only. The 2 groups were controls and OA. The 2 trial conditions
235
were level walk (x of 10 trials), and the “bin” of 5 trials with lowest muscle activation or
236
greater knee excursion (Figure 4). The 30 trials were divided into bins of 5 trials and mean
237
extension excursion and activity of all muscles were calculated for each bin (Figure 4). The
238
greatest extension excursion and the lowest EMG activity in the bins were defined as the
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
216
Neuromuscular adaptation in knee osteoarthritis
10
level of adaptation. The midstance phase was chosen because the time from initial contact to
240
peak knee extension is within the duration of a long latency reflex when adaptation is
241
expected to occur.
242
RESULTS
243
Disability, functional impairments and structural impairments: The differences between
244
control and OA subjects for age, BMI and gender distribution (Table 1) were not significant
245
(P > 0.05). The OA group had significantly higher reports of pain, knee related symptoms
246
and difficulties with ADL (P < 0.001) (Table 2). The OA group walked slower, took longer
247
to complete the stair climbing test, had lower quadriceps strength and greater prevalence of
248
symptomatic FKI (P <0.001 – 0.037). The differences in proprioception were not significant
249
between OA and controls (P > 0.05). Subjects with knee OA had lesser medial joint space
250
width and greater frontal plane varus (P < 0.001) compared to the control subjects.
251
Proactive and reactive responses to perturbation:
252
Pre-activation : The data for knee angle at initial contact and muscle activity for all
253
musclesare shown in Table 3. During the pre-activation phase, prior to the foot contacting
254
the platform, a main effect for trial type was observed. In P1, both groups demonstrated a
255
similar pattern of greater knee flexion at initial contact and higher levels of muscle activity
256
across all muscles (P ≤ 0.002). From P1 to P2, both groups increased their knee flexion at
257
initial contact and showed an increase in muscle activity for LG (P ≤ 0.008). The activity for
258
all other muscles did not show any further change after P1. Across all trials, the OA subjects
259
maintained their knee in greater flexion at initial contact compared to the control group (P =
260
0.043).
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
239
Neuromuscular adaptation in knee osteoarthritis
11
Loading Response: The data for knee flexion excursion, and muscle activity for all muscles
262
are shown in Table 4. During the loading response phase, as the limb accepts weight, a main
263
effect for trial type was observed. In P1, both groups demonstrated a similar pattern of lesser
264
knee flexion excursion during loading response and higher levels of muscle activity across all
265
muscles (P ≤ 0.006). From P1 to P2, both groups showed a further decrease in their knee
266
flexion excursion and increase in the activity in MH and LH muscles (P ≤ 0.029). There were
267
no changes in the flexion excursion or muscle activity after P2. Across all trials, the OA group
268
had less flexion excursion and higher LH activation during loading response (P ≤ 0.005).
269
Midstance: The data for knee extension excursion, and muscle activity for all muscles are
270
shown in Figure 5. During the midstance phase as the stance knee extends, a main effect for
271
trial type was observed for all variables (P < 0.001). In P1, subjects in both groups showed a
272
reduction in the extension excursion and an increase in activity of all muscles. Thereafter, the
273
extension excursion increased from P1 to P2 (P < 0.001) and activity of MQ, LQ, MH and LH
274
showed a decrease from P1 to P2 and from P2 to P3 (P ≤ 0.023). Activity of MQ further
275
decreased from P3 to P5 (P ≤ 0.034) and activity of MH also decreased from P4 to P5 (P =
276
0.011). Activity of MG decreased from P2 to P3 (P = 0.023) and did not change thereafter.
277
Activity of LG did not change from P1 to P2 but showed a decrease from P3 to P5 (P ≤ 0.048).
278
Across all trials, subjects with knee OA had smaller extension excursion and greater
279
activation in MQ, LQ and LH muscles (P ≤ 0.003).
280
Neuromuscular adaptation : The data for knee extension excursion, and muscle activity for
281
MQ, MH and MG for level walking and the greatest knee excursion or lowest level of EMG
282
are shown in Figure 6. Both groups showed an increase in knee extension excursion and
283
decreased magnitude of muscle activation over the 30 consecutive perturbation trials. No
284
statistical differences were observed between the extension excursion during level walking
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
261
Neuromuscular adaptation in knee osteoarthritis
12
and the greatest extension excursion during the 30 trials, or the activation of MQ, LQ, MH
286
and LH during level walking and the lowest EMG magnitude during the 30 perturbation trials
287
indicating that muscle responses and knee excursions had adapted to baseline levels. The
288
magnitude of MG and LG activity in the 30 trials stayed greater than that of level walking in
289
both groups (P ≤ 0.023).
290
DISCUSSION
291
The aim of this study was to compare short term adaptation in muscle activation and joint
292
movement in response to repeated lateral perturbations during walking, between individuals
293
with medial knee OA who present with significant functional and structural impairments and
294
healthy asymptomatic controls. The hypotheses was that, compared to the control subjects,
295
people with medial knee OA would exhibit a reduced ability to adapt their movement and
296
muscle activation patterns due to structural, functional, and neuromotor impairments related
297
to the OA disease process. However, our hypotheses were not supported by the data with
298
both groups demonstrating similar proactive and reactive responses to perturbations that
299
challenged knee stability. The OA group had significant structural and functional
300
impairments compared to the control group. Furthermore, the OA group also demonstrated
301
patterns of higher muscle activation and less knee motion which have been shown in multiple
302
earlier studies (33, 44, 66, 67) indicating that the OA cohort in this study had neuromuscular
303
impairments, even though we did not observe a difference in joint proprioception. The
304
findings from this study show that people with knee OA use strategies that lead to similar
305
neuromotor responses as that seen in healthy control subjects, when exposed to challenging
306
perturbations. However, mechanisms underlying the adaptive response in people with knee
307
OA need further study. In our paradigm, input was available from multiple lower extremity
308
afferents including muscle spindles, skin and other lower extremity joints in people with
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
285
Neuromuscular adaptation in knee osteoarthritis
13
significant knee OA related impairments. Furthermore, the techniques used in our study may
310
have limited sensitivity to detecting proprioceptive deficits (61). This redundant input may
311
allow the generation of appropriate response to external challenges to stability while walking.
312
Hence, the often reported deficits in knee proprioception in people with knee OA, measured
313
under carefully controlled conditions, may not be critical towards maintaining joint stability
314
during daily activities. However other magnitudes and directions of perturbations than those
315
used in our study, may yield different results. Future studies should also take into
316
consideration the limited sensitivity of commonly used tests of proprioception, and the role of
317
muscle spindles in movement and position sense.
318
Disability, functional and structural impairments, and walking patterns:
319
Subjects in our OA group had significantly greater pain and self-reported and physical
320
limitations compared to the control group as demonstrated by lower KOOS scores, greater
321
time taken to complete the stair climbing test and slower walking speed. The OA group also
322
had greater quadriceps weakness, varus malalignment and FKI. Pain at the knee has been
323
shown to be associated with quadriceps inhibition (4, 70) but none of our subjects reported
324
pain during maximal quadriceps strength assessment. Hence the quadriceps strength deficits
325
in the OA group may be more related to other mechanisms like loss of cross-sectional area
326
(35), and change in muscle fiber type (18). The smaller medial joint space and greater frontal
327
plane varus suggest that there was significant damage to the knee tissues in the OA group. It
328
has been shown that varus malalignment is a reliable marker of OA incidence and
329
progression with greater malalignment associated with greater medial cartilage loss, meniscal
330
damage and extrusion and greater bone marrow edema like lesions (25, 72, 73).
331
We also observed less knee motion and higher muscle activation in people with knee
332
OA compared to controls during walking. These findings have also been reported earlier in
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
309
Neuromuscular adaptation in knee osteoarthritis
14
multiple studies (33, 44, 66, 67) and indicate that the cohort of knee OA subjects did have
334
neuromotor impairments. Similar responses to perturbation in both groups, in spite of the
335
profound differences in structure, function and walking patterns, could be due to (a) the
336
redundancy in afferent input from lower extremities, (b) the perturbation being of insufficient
337
magnitude to challenge knee stability, or (c) other compensatory strategies. Since the
338
perturbation was applied at the foot, it is quite likely that afferent information from multiple
339
structures including the sole of the foot, ankle and foot muscles and ankle and foot joint
340
receptors would be available to the nervous system. None of our subjects had pain in other
341
joints of the lower extremity and hence we could assume a normal afferent input from these
342
structures. It is possible that the information from these structures was sufficient for the
343
nervous system to generate adequate responses to these perturbations even in people with
344
significant knee OA. Hence, the deficits in knee proprioception that have been reported in
345
earlier studies may not impair the ability of people with knee OA to respond to external
346
challenges to stability under functional weight-bearing conditions. It is less likely that the
347
perturbation was of insufficient magnitude to challenge knee stability. Using the same
348
perturbation paradigm, we have earlier observed greater medial muscle co-contraction in
349
people with knee OA compared to controls, and in people with knee OA who have FKI
350
compared to those who do not, during standing and walking (44, 67).Hence, further work is
351
needed to understand the strategies underlying the adaptive response in people with knee OA,
352
perhaps with different directions and magnitudes of perturbations.
353
Even though we observed differences in movement and muscle activation patterns
354
we did not see a difference in proprioception as assessed using the TTDPM technique
355
between the OA and control groups. It has been suggested recently that the proprioception
356
tests which are commonly used, including TTDPM, may not be sensitive to detect threshold
357
of movement onset since they only assess that a movement occurred (61). Muscle spindles
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
333
Neuromuscular adaptation in knee osteoarthritis
15
have been shown to be the primary afferent organ for movement and position sense detection,
359
and muscle spindle discharge can vary depending on the length and history of muscle activity
360
prior to propriception testing (61). It has been recommended that in tests of proprioception
361
under relaxed conditions, like used in our study, the participants should be asked to
362
isometrically contract the agonist muscles at the joint angle the test is being performed at, to
363
counter any thixotropic effects that may be present in the muscle or the spindles (61). The
364
subjects in our study did not perform the isometric contraction and hence the findings may be
365
affected by muscle thixotropy. Furthermore, these tests of proprioception also rely on
366
memory, mood, motivation and reaction time of the participants (71, 77). Hence, other tests
367
including vibratory perception have been recommended which partly overcome some of these
368
limitations (71, 77). In fact, a recent review recommended that a new protocol for
369
measurement of knee proprioception in people with knee OA is needed (40). Earlier studies
370
which found differences in TTDPM between subjects with knee OA report large effect sizes
371
between 0.47 and 2.7 (50, 58). Using these effect sizes, and an alpha level of 0.05 and a
372
power of 80%, we had a sufficient sample size to detect differences. However, for one of the
373
comparisons the P value was 0.092 suggesting that issues related to sample size may be
374
present. Lastly, importance of proprioceptive deficits in knee OA has received some scrutiny
375
with large scale longitudinal studies reporting weak or no associations between
376
proprioceptive deficits and onset of symptomatic or radiographic knee OA or development of
377
adverse OA outcomes (17, 69). The findings from our work also suggest that during
378
functional weight-bearing activities, the redundancy in afferent feedback may be sufficient to
379
allow adequate neuromotor responses.
380
Response to 1st Perturbation
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
358
Neuromuscular adaptation in knee osteoarthritis
16
381
The timing of the first perturbation trial was unknown to all the subjects and subjects
382
in both OA and control group exhibited similar responses. Subjects in both groups responded
383
to the first novel perturbation with a decrease in knee motion during loading response and
384
midstance phases accompanied with an increase in muscle activity of all muscles studied.
385
This first response (aka a “startle-like” response) is comparable to the responses elicited by a
386
sudden high amplitude auditory stimulus (55, 56) and is characterized by co-contraction of
387
muscles. The elevated EMG activity in conjunction with truncated knee motion illustrates a
388
knee stiffening or “freezing” strategy (55) that may be an attempt to maintain knee stability.
Increased knee flexion and higher muscle activity observed during the pre-activation
390
phase was unexpected since subjects were unaware of when the first perturbation would take
391
place (8, 26). This unexpected finding could have occurred because, for safety reasons, we
392
allowed the subjects to observe the platform translate and although they did not know when
393
the first perturbation would occur they may have been sufficiently unsure of the experience
394
that their muscles were more active in anticipation of P1. Such a response has been reported
395
previously (22, 45) and could lead to better stability under uncertain and challenging
396
conditions.
397
Response to repeated perturbations:
398
All subjects in the study showed an increase in knee motion and a reduction in muscle
399
activity of quadriceps and hamstring muscles during the midstance phase on repeated
400
exposure to the perturbations. Prior experience of a perturbation leads to the generation of
401
proactive responses that works in conjunction with reactive response to maintain postural
402
stability (52, 57).
403
perturbations (57). Reactive response consists of short and long-latency responses and it has
404
also been shown that the long-latency reflexes show the greatest habituation by a decrease in
Adaptation is characterized by decrease in the reactive response to
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
389
Neuromuscular adaptation in knee osteoarthritis
17
magnitude (24, 56, 65). For our subjects, the midstance phase likely corresponded with the
406
interval of time when the long-latency reflex (> 90 msec) occurs and hence adaptation was
407
primarily observed in this phase. Although changes in reactive responses that occur in the
408
time frame of a long-latency reflex may be too slow to affect dynamic stability directly,
409
adaptation in the long-latency reflexes represents the influence of proactive responses that
410
occur when the motor system predicts future motion based on past experiences (80). Classen
411
et al. (1999) proposed that short term adaptation is the first step in skill acquisition (9) which
412
would bode well for people with OA who may need to learn to stabilize their knees after
413
joint structures become damaged.
414
It was interesting to see that the short-term adaptation was only seen during midstance
415
phase, a point in the gait cycle when the 2nd peak of external knee adduction moment (KAM)
416
occurs. However, higher articular loads at the knee during loading response at 1st peak of
417
KAM (11, 27, 41) that occurs during the loading response phase of gait is the hallmark of
418
walking patterns in people with knee OA. No adaptation was observed during the loading
419
response, we did not observe an adaptive response with all subjects which is most likely due
420
to the loading response being a phase in which only short and medium latecny reflexes are
421
generated, which usually do not show adaptation (24, 56).
422
The attenuation of the EMG during midstance was most pronounced in the quadriceps
423
and hamstring muscles, whereas the gastrocnemius muscles showed less attenuation and the
424
magnitude was higher even after 30 trials. This finding is consistent with those of
425
Nieuwenhuijzen et al. (2007) who found that sensorimotor adaptation is less in muscles with
426
special significance to the perturbation (55). In the current study, the perturbation was applied
427
at the foot-floor interface so a sudden displacement of the foot is likely to elicit activation of
428
muscles around the ankle joint to provide a more stable ankle and adaptation could have
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
405
Neuromuscular adaptation in knee osteoarthritis
18
429
decreased postural stability (28).
The application of the perturbation at the foot floor
430
interface may be considered a limitation to this study since the perturbation may not have
431
resulted in destabilization of the knee, however, the adaptation that was seen in the muscles
432
that cross the knee and not the ankle, suggest that the paradigm was appropriate for
433
determining if neuromuscular adaptation was different in OA subjects compared to controls.
Studies investigating response to postural perturbations in individuals with knee OA
435
are scarce. Earlier work from our group has found that using the same perturbation paradigm
436
as this study, people with medial knee OA generate higher medial muscle co-contraction
437
during standing compared to controls; and people with medial knee OA who have FKI
438
generate higher medial muscle co-contraction during walking, compared to those without FKI
439
(44, 67). However, adaptive response to repeated perturbations was not investigated in these
440
studies. Results from the current work build upon this earlier work and demonstrate that in
441
spite of these differences in movement patterns, people with knee OA show similar decrease
442
in response as controls, if the perturbations are repeated. Using a knee buckling paradigm in
443
unilateral stance, Irwin et al (37) found no difference in the onset latencies of vastus lateralis
444
or biceps femoris between people with knee OA and old or young adults. They recommended
445
future studies to focus on muscle amplitudes instead of latencies as has been done in the
446
current study. Finally, Fallah-Yakhdani et al (16, 81) assessed dynamic stability and
447
variability during treadmill walking in subjects before and after total knee arthroplasty
448
(TKA). They reported less variability in the affected extremity of OA subjects which was
449
associated with reduce fall risk Furthermore, the OA subjects had greater co-contraction and
450
the affected extremity was more stable than the unaffected extremity. Our findings of less
451
motion and greater muscle activation across all trials likely support the phenomenon of less
452
variability However, the changes in variability across repeated perturbations needs further
453
study.
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
434
Neuromuscular adaptation in knee osteoarthritis
454
19
Conclusions and Clinical Implications
455
The results from this study show that individuals with knee OA demonstrate similar
456
responses to perturbations during walking as those without knee OA. Exercise programs
457
focusing on joint stability and proprioception are becoming more popular in the rehabilitation
458
of people with knee injuries (1, 15, 19).
459
“neuromuscular training” are purported to address knee control or alter walking patterns to
460
lower knee contact loads and they often involve activities that challenge knee stability in a
461
safe and controlled manner (3, 7, 79). The role of diminished knee proprioception, if present
462
in people with knee OA, towards maintaining knee stability during weight-bearing activities
463
is questionable due to redundancy of afferent input. However, if these perturbation training
464
based programs are successful at altering movement patterns that can reduce articular loading
465
during walking, they may have utility towards slowing structural progression of knee OA (7).
466
Results from this study show that people with medial knee OA demonstrate changes in
467
muscle activation and movement patterns when exposed to perturbations, but future studies
468
would need to be done to investigate if specific changes can be targeted and retained over a
469
long period of time.
So called “proprioceptive training” or
The results from this study need to be interpreted in light of certain limitations. The
471
techniques used to assess proprioception may have had limited sensitivity as discussed
472
earlier. However, these techniques have been used in earlier studies in subjects with knee OA
473
allowing us to compare our findings to published literature. The perturbation paradigm used
474
allowed subjects to continue walking after experiencing the perturbation to the end of the
475
walkway and then back to the starting position. This period could have induced some
476
“washout” of the adaptive response resulting from the perturbation. However, had subjects
477
been able to experience the perturbation in consecutive strides we speculate that the
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
470
Neuromuscular adaptation in knee osteoarthritis
20
478
magnitude and rate of habituation may actually have been higher than observed here. Also, it
479
is likely that the perturbation used, though appropriate to analyze reactive and proactive
480
responses, was not of sufficient magnitude to elicit differential responses between groups.
481
Finally, we did not adjust for multiple comparisons in the between-group analyses and hence
482
P values close to 0.05 should be interpreted with caution.
In conclusion, the results from this study provide indirect evidence that the manner in
484
which the nervous systems processes sensory information in people with knee OA is similar
485
to that in healthy control subjects. To our knowledge, this is the first study to demonstrate
486
similar responses to repeated perturbations in people with symptomatic and radiographic
487
knee OA and controls. The subjects with knee OA had significantly worse structure and
488
function, and differences in walking patterns, compared to the control subjects but still
489
showed similar adaptive response. Hence, compensatory strategies may be sufficient to allow
490
people with knee OA to maintain stability when challenged during walking. However, the
491
mechanisms underlying these responses will need further study.
492
ACKNOWLEDGEMENTS
493
Funding was provided by International Society of Biomechanics Doctoral
494
Dissertation Grant, American College of Rheumatology-Research and Education Foundation
495
Health Professional Graduate Student Preceptorship, University of Delaware Graduate
496
Fellowship and NIH 1P20RR016458-01 and 1P20RR016458-06. Currently. Dr. Deepak
497
Kumar is affiliated with the Muscoloskeletal Quantitative Imaging Research Group, Dept. of
498
Radiology, University of California, San Francisco, CA, USA. Currently Dr. Katherine
499
Rudolph is affiliated with the Dept. of Physical Therapy, University of New England,
500
Portland, ME, USA.
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
483
Neuromuscular adaptation in knee osteoarthritis
1
REFERENCES
502
503
504
505
506
507
508
509
510
511
512
513
514
515
516
517
518
519
520
521
522
523
524
525
526
527
528
529
530
531
532
533
534
535
536
537
538
539
540
541
542
543
544
545
546
547
548
1.
Ageberg E, Link A, and Roos EM. Feasibility of neuromuscular training in
patients with severe hip or knee OA: the individualized goal-based NEMEX-TJR
training program. BMC Musculoskelet Disord 11: 126, 2010.
2.
Andriacchi TP, and Mundermann A. The role of ambulatory mechanics in the
initiation and progression of knee osteoarthritis. Curr Opin Rheumatol 18: 514-518,
2006.
3.
Arampatzis A, Peper A, and Bierbaum S. Exercise of mechanisms for dynamic
stability control increases stability performance in the elderly. J Biomech 44: 52-58,
2011.
4.
Arvidsson I, Eriksson E, Knutsson E, and Arner S. Reduction of pain inhibition
on voluntary muscle activation by epidural analgesia. Orthopedics 9: 1415-1419, 1986.
5.
Barrack RL, Skinner HB, Cook SD, and Haddad RJ, Jr. Effect of articular
disease and total knee arthroplasty on knee joint-position sense. J Neurophysiol 50: 684687, 1983.
6.
Barrett DS, Cobb AG, and Bentley G. Joint proprioception in normal,
osteoarthritic and replaced knees. J Bone Joint Surg Br 73: 53-56, 1991.
7.
Bennell KL, Egerton T, Wrigley TV, Hodges PW, Hunt M, Roos EM, Kyriakides
M, Metcalf B, Forbes A, Ageberg E, and Hinman RS. Comparison of neuromuscular
and quadriceps strengthening exercise in the treatment of varus malaligned knees with
medial knee osteoarthritis: a randomised controlled trial protocol. BMC Musculoskelet
Disord 12: 276, 2011.
8.
Bhatt T, and Pai YC. Immediate and latent interlimb transfer of gait stability
adaptation following repeated exposure to slips. J Mot Behav 40: 380-390, 2008.
9.
Classen J, Liepert J, Hallett M, and Cohen L. Plasticity of movement
representation in the human motor cortex. Electroencephalogr Clin Neurophysiol Suppl
51: 162-173, 1999.
10.
Conaghan PG, Felson D, Gold G, Lohmander S, Totterman S, and Altman R.
MRI and non-cartilaginous structures in knee osteoarthritis. Osteoarthritis Cartilage 14
Suppl A: A87-94, 2006.
11.
D'Lima DD, Patil S, Steklov N, Slamin JE, and Colwell CW, Jr. The Chitranjan
Ranawat Award: in vivo knee forces after total knee arthroplasty. Clin Orthop Relat Res
440: 45-49, 2005.
12.
Dearborn JT, Eakin CL, and Skinner HB. Medial compartment arthrosis of the
knee. Am J Orthop 25: 18-26, 1996.
13.
Dekker J, van Dijk GM, and Veenhof C. Risk factors for functional decline in
osteoarthritis of the hip or knee. Curr Opin Rheumatol 21: 520-524, 2009.
14.
Delagi E IJ, Perotto A,. Anatomic guide for the electromyographer, the limbs.
Springfield,IL: 1981.
15.
Diracoglu D, Aydin R, Baskent A, and Celik A. Effects of kinesthesia and
balance exercises in knee osteoarthritis. Jcr-Journal of Clinical Rheumatology 11: 303310, 2005.
16.
Fallah-Yakhdani HR, Abbasi-Bafghi H, Meijer OG, Bruijn SM, van den
Dikkenberg N, Benedetti MG, and van Dieen JH. Determinants of co-contraction
during walking before and after arthroplasty for knee osteoarthritis. Clin Biomech
(Bristol, Avon) 27: 485-494, 2012.
17.
Felson DT, Gross KD, Nevitt MC, Yang M, Lane NE, Torner JC, Lewis CE, and
Hurley MV. The effects of impaired joint position sense on the development and
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
501
Neuromuscular adaptation in knee osteoarthritis
progression of pain and structural damage in knee osteoarthritis. Arthritis Rheum 61:
1070-1076, 2009.
18.
Fink B, Egl M, Singer J, Fuerst M, Bubenheim M, and Neuen-Jacob E.
Morphologic changes in the vastus medialis muscle in patients with osteoarthritis of the
knee. Arthritis Rheum 56: 3626-3633, 2007.
19.
Fitzgerald GK, Childs JD, Ridge TM, and Irrgang JJ. Agility and perturbation
training for a physically active individual with knee osteoarthritis. Phys Ther 82: 372382, 2002.
20.
Fitzgerald GK, Piva SR, Gil AB, Wisniewski SR, Oddis CV, and Irrgang JJ.
Agility and perturbation training techniques in exercise therapy for reducing pain and
improving function in people with knee osteoarthritis: a randomized clinical trial. Phys
Ther 91: 452-469, 2011.
21.
Fitzgerald GK, Piva SR, and Irrgang JJ. Reports of joint instability in knee
osteoarthritis: its prevalence and relationship to physical function. Arthritis Rheum 51:
941-946, 2004.
22.
Gruneberg C, Nieuwenhuijzen PH, and Duysens J. Reflex responses in the lower
leg following landing impact on an inverting and non-inverting platform. J Physiol 550:
985-993, 2003.
23.
Guccione AA, Felson DT, Anderson JJ, Anthony JM, Zhang Y, Wilson PW,
Kelly-Hayes M, Wolf PA, Kreger BE, and Kannel WB. The effects of specific medical
conditions on the functional limitations of elders in the Framingham Study. Am J Public
Health 84: 351-358, 1994.
24.
Hansen PD, Woollacott MH, and Debu B. Postural responses to changing task
conditions. Exp Brain Res 73: 627-636, 1988.
25.
Hayashi D, Englund M, Roemer FW, Niu J, Sharma L, Felson DT, Crema MD,
Marra MD, Segal NA, Lewis CE, Nevitt MC, and Guermazi A. Knee malalignment is
associated with an increased risk for incident and enlarging bone marrow lesions in the
more loaded compartments: the MOST study. Osteoarthritis Cartilage 20: 1227-1233,
2012.
26.
Heiden TL, Sanderson DJ, Inglis JT, and Siegmund GP. Adaptations to normal
human gait on potentially slippery surfaces: the effects of awareness and prior slip
experience. Gait Posture 24: 237-246, 2006.
27.
Heinlein B, Kutzner I, Graichen F, Bender A, Rohlmann A, Halder AM, Beier A,
and Bergmann G. ESB Clinical Biomechanics Award 2008: Complete data of total knee
replacement loading for level walking and stair climbing measured in vivo with a
follow-up of 6-10 months. Clin Biomech (Bristol, Avon) 24: 315-326, 2009.
28.
Hof AL, Elzinga H, Grimmius W, and Halbertsma JP. Detection of non-standard
EMG profiles in walking. Gait Posture 21: 171-177, 2005.
29.
Horstmann GA, Gollhofer A, and Dietz V. Reproducibility and adaptation of the
EMG responses of the lower leg following perturbations of upright stance.
Electroencephalogr Clin Neurophysiol 70: 447-452, 1988.
30.
Hortobagyi T, Garry J, Holbert D, and Devita P. Aberrations in the control of
quadriceps muscle force in patients with knee osteoarthritis. Arthritis Rheum 51: 562569, 2004.
31.
Hsieh RL, Lee WC, Lo MT, and Liao WC. Postural stability in patients with
knee osteoarthritis: comparison with controls and evaluation of relationships between
postural stability scores and international classification of functioning, disability and
health components. Arch Phys Med Rehabil 94: 340-346 e341, 2013.
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
549
550
551
552
553
554
555
556
557
558
559
560
561
562
563
564
565
566
567
568
569
570
571
572
573
574
575
576
577
578
579
580
581
582
583
584
585
586
587
588
589
590
591
592
593
594
595
596
2
Neuromuscular adaptation in knee osteoarthritis
32.
Hsu RW, Himeno S, Coventry MB, and Chao EY. Normal axial alignment of the
lower extremity and load-bearing distribution at the knee. Clin Orthop Relat Res 215227, 1990.
33.
Hubley-Kozey C, Deluzio K, and Dunbar M. Muscle co-activation patterns
during walking in those with severe knee osteoarthritis. Clin Biomech (Bristol, Avon) 23:
71-80, 2008.
34.
Hurley MV, Scott DL, Rees J, and Newham DJ. Sensorimotor changes and
functional performance in patients with knee osteoarthritis. Ann Rheum Dis 56: 641648, 1997.
35.
Ikeda S, Tsumura H, and Torisu T. Age-related quadriceps-dominant muscle
atrophy and incident radiographic knee osteoarthritis. J Orthop Sci 10: 121-126, 2005.
36.
Irrgang JJ, Snyder-Mackler L, Wainner RS, Fu FH, and Harner CD.
Development of a patient-reported measure of function of the knee. J Bone Joint Surg
Am 80: 1132-1145, 1998.
37.
Irwin KE, Wening JD, Bhatt T, and Pai YC. Does knee osteoarthritis alter the
neuromuscular responses to a perturbation during single lower limb stance? J Geriatr
Phys Ther 28: 93-101, 2005.
38.
Jordan JM, Helmick CG, Renner JB, Luta G, Dragomir AD, Woodard J, Fang
F, Schwartz TA, Abbate LM, Callahan LF, Kalsbeek WD, and Hochberg MC.
Prevalence of knee symptoms and radiographic and symptomatic knee osteoarthritis in
African Americans and Caucasians: the Johnston County Osteoarthritis Project. J
Rheumatol 34: 172-180, 2007.
39.
Kellgren JH, and Lawrence JS. Radiological assessment of osteo-arthrosis. Ann
Rheum Dis 16: 494-502, 1957.
40.
Knoop J, Steultjens MP, van der Leeden M, van der Esch M, Thorstensson CA,
Roorda LD, Lems WF, and Dekker J. Proprioception in knee osteoarthritis: a narrative
review. Osteoarthritis Cartilage 19: 381-388, 2011.
41.
Kumar D, Manal KT, and Rudolph KS. Knee joint loading during gait in healthy
controls and individuals with knee osteoarthritis. Osteoarthritis Cartilage 21: 298-305,
2013.
42.
Lequesne M editor. Quantitative measurements of joint space during progression
of osteoarthritis: “chondrometry”. Rosemont, IL: American Academy of Orthopaedic
Surgeons, 1995, p. 427-444.
43.
Lewek MD, Chmielewski TL, Risberg MA, and Snyder-Mackler L. Dynamic
knee stability after anterior cruciate ligament rupture. Exerc Sport Sci Rev 31: 195-200,
2003.
44.
Lewek MD, Ramsey DK, Snyder-Mackler L, and Rudolph KS. Knee
stabilization in patients with medial compartment knee osteoarthritis. Arthritis Rheum
52: 2845-2853, 2005.
45.
Lewek MD, Rudolph KS, and Snyder-Mackler L. Control of frontal plane knee
laxity during gait in patients with medial compartment knee osteoarthritis.
Osteoarthritis Cartilage 12: 745-751, 2004.
46.
Li X, Benjamin Ma C, Link TM, Castillo DD, Blumenkrantz G, Lozano J,
Carballido-Gamio J, Ries M, and Majumdar S. In vivo T(1rho) and T(2) mapping of
articular cartilage in osteoarthritis of the knee using 3 T MRI. Osteoarthritis Cartilage
15: 789-797, 2007.
47.
Liang MH, Larson MG, Cullen KE, and Schwartz JA. Comparative
measurement efficiency and sensitivity of five health status instruments for arthritis
research. Arthritis Rheum 28: 542-547, 1985.
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
597
598
599
600
601
602
603
604
605
606
607
608
609
610
611
612
613
614
615
616
617
618
619
620
621
622
623
624
625
626
627
628
629
630
631
632
633
634
635
636
637
638
639
640
641
642
643
644
645
3
Neuromuscular adaptation in knee osteoarthritis
48.
Lin DH, Lin CH, Lin YF, and Jan MH. Efficacy of 2 non-weight-bearing
interventions, proprioception training versus strength training, for patients with knee
osteoarthritis: a randomized clinical trial. J Orthop Sports Phys Ther 39: 450-457, 2009.
49.
Lohmander LS. Articular cartilage and osteoarthrosis. The role of molecular
markers to monitor breakdown, repair and disease. J Anat 184 ( Pt 3): 477-492, 1994.
50.
Lund H, Juul-Kristensen B, Hansen K, Christensen R, Christensen H,
Danneskiold-Samsoe B, and Bliddal H. Movement detection impaired in patients with
knee osteoarthritis compared to healthy controls: a cross-sectional case-control study. J
Musculoskelet Neuronal Interact 8: 391-400, 2008.
51.
Manal K, McClay I, Stanhope S, Richards J, and Galinat B. Comparison of
surface mounted markers and attachment methods in estimating tibial rotations during
walking: an in vivo study. Gait Posture 11: 38-45, 2000.
52.
Marigold DS, and Patla AE. Strategies for dynamic stability during locomotion
on a slippery surface: effects of prior experience and knowledge. J Neurophysiol 88:
339-353, 2002.
53.
Mosher TJ, and Dardzinski BJ. Cartilage MRI T2 relaxation time mapping:
overview and applications. Semin Musculoskelet Radiol 8: 355-368, 2004.
54.
Nielsen JB, and Sinkjaer T. Afferent feedback in the control of human gait. J
Electromyogr Kinesiol 12: 213-217, 2002.
55.
Nieuwenhuijzen PH, and Duysens J. Proactive and reactive mechanisms play a
role in stepping on inverting surfaces during gait. J Neurophysiol 98: 2266-2273, 2007.
56.
Nieuwenhuijzen PH, Schillings AM, Van Galen GP, and Duysens J. Modulation
of the startle response during human gait. J Neurophysiol 84: 65-74, 2000.
57.
Pai YC, and Bhatt TS. Repeated-slip training: an emerging paradigm for
prevention of slip-related falls among older adults. Phys Ther 87: 1478-1491, 2007.
58.
Pai YC, Rymer WZ, Chang RW, and Sharma L. Effect of age and osteoarthritis
on knee proprioception. Arthritis Rheum 40: 2260-2265, 1997.
59.
Pai YC, Wening JD, Runtz EF, Iqbal K, and Pavol MJ. Role of feedforward
control of movement stability in reducing slip-related balance loss and falls among older
adults. J Neurophysiol 90: 755-762, 2003.
60.
Peterfy CG, Gold G, Eckstein F, Cicuttini F, Dardzinski B, and Stevens R. MRI
protocols for whole-organ assessment of the knee in osteoarthritis. Osteoarthritis
Cartilage 14 Suppl A: A95-111, 2006.
61.
Proske U, and Gandevia SC. The proprioceptive senses: their roles in signaling
body shape, body position and movement, and muscle force. Physiol Rev 92: 1651-1697,
2011.
62.
Quintern J, Berger W, and Dietz V. Compensatory reactions to gait
perturbations in man: short- and long-term effects of neuronal adaptation. Neurosci
Lett 62: 371-376, 1985.
63.
Rejeski WJ, Ettinger WH, Jr., Schumaker S, James P, Burns R, and Elam JT.
Assessing performance-related disability in patients with knee osteoarthritis.
Osteoarthritis Cartilage 3: 157-167, 1995.
64.
Roos EM, Roos HP, Lohmander LS, Ekdahl C, and Beynnon BD. Knee Injury
and Osteoarthritis Outcome Score (KOOS)--development of a self-administered
outcome measure. J Orthop Sports Phys Ther 28: 88-96, 1998.
65.
Rothwell JC, Day BL, Berardelli A, and Marsden CD. Habituation and
conditioning of the human long latency stretch reflex. Exp Brain Res 63: 197-204, 1986.
66.
Rutherford DJ, Hubley-Kozey CL, and Stanish WD. Changes in knee joint
muscle activation patterns during walking associated with increased structural severity
in knee osteoarthritis. J Electromyogr Kinesiol 23: 704-711, 2013.
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
646
647
648
649
650
651
652
653
654
655
656
657
658
659
660
661
662
663
664
665
666
667
668
669
670
671
672
673
674
675
676
677
678
679
680
681
682
683
684
685
686
687
688
689
690
691
692
693
694
695
4
Neuromuscular adaptation in knee osteoarthritis
67.
Schmitt LC. Knee stabilization and medial knee osteoarthritis. In: Biomechanics
and Movement Sciences. Newark,DE: University of Delaware, 2007.
68.
Schmitt LC, Fitzgerald GK, Reisman AS, and Rudolph KS. Instability, Laxity,
and Physical Function in Patients With Medial Knee Osteoarthritis. Phys Ther 2008.
69.
Segal NA, Glass NA, Felson DT, Hurley M, Yang M, Nevitt M, Lewis CE, and
Torner JC. Effect of quadriceps strength and proprioception on risk for knee
osteoarthritis. Med Sci Sports Exerc 42: 2081-2088, 2010.
70.
Shakespeare DT, Stokes M, Sherman KP, and Young A. Reflex inhibition of the
quadriceps after meniscectomy: lack of association with pain. Clin Physiol 5: 137-144,
1985.
71.
Shakoor N, Agrawal A, and Block JA. Reduced lower extremity vibratory
perception in osteoarthritis of the knee. Arthritis Rheum 59: 117-121, 2008.
72.
Sharma L, Chmiel JS, Almagor O, Felson D, Guermazi A, Roemer F, Lewis CE,
Segal N, Torner J, Cooke TD, Hietpas J, Lynch J, and Nevitt M. The role of varus and
valgus alignment in the initial development of knee cartilage damage by MRI: the
MOST study. Ann Rheum Dis 72: 235-240, 2013.
73.
Sharma L, Eckstein F, Song J, Guermazi A, Prasad P, Kapoor D, Cahue S,
Marshall M, Hudelmaier M, and Dunlop D. Relationship of meniscal damage, meniscal
extrusion, malalignment, and joint laxity to subsequent cartilage loss in osteoarthritic
knees. Arthritis Rheum 58: 1716-1726, 2008.
74.
Sharma L, Hurwitz DE, Thonar EJ, Sum JA, Lenz ME, Dunlop DD, Schnitzer
TJ, Kirwan-Mellis G, and Andriacchi TP. Knee adduction moment, serum hyaluronan
level, and disease severity in medial tibiofemoral osteoarthritis. Arthritis Rheum 41:
1233-1240, 1998.
75.
Swanik CB, Lephart SM, and Rubash HE. Proprioception, kinesthesia, and
balance after total knee arthroplasty with cruciate-retaining and posterior stabilized
prostheses. J Bone Joint Surg Am 86-A: 328-334, 2004.
76.
Tang PF, Woollacott MH, and Chong RK. Control of reactive balance
adjustments in perturbed human walking: roles of proximal and distal postural muscle
activity. Exp Brain Res 119: 141-152, 1998.
77.
Thorlund JB, Shakoor N, Ageberg E, Sandal LF, Block JA, and Roos EM.
Vibratory perception threshold in young and middle-aged patients at high risk of knee
osteoarthritis compared to controls. Arthritis Care Res (Hoboken) 64: 144-148, 2012.
78.
Tsauo JY, Cheng PF, and Yang RS. The effects of sensorimotor training on knee
proprioception and function for patients with knee osteoarthritis: a preliminary report.
Clin Rehabil 22: 448-457, 2008.
79.
Tunay VB, Baltaci G, and Atay AO. Hospital-based versus home-based
proprioceptive and strengthening exercise programs in knee osteoarthritis. Acta Orthop
Traumatol Turc 44: 270-277, 2010.
80.
Wagner MJ, and Smith MA. Shared internal models for feedforward and
feedback control. J Neurosci 28: 10663-10673, 2008.
81.
Yakhdani HR, Bafghi HA, Meijer OG, Bruijn SM, van den Dikkenberg N,
Stibbe AB, van Royen BJ, and van Dieen JH. Stability and variability of knee
kinematics during gait in knee osteoarthritis before and after replacement surgery. Clin
Biomech (Bristol, Avon) 25: 230-236, 2010.
82.
Zhang W, Moskowitz RW, Nuki G, Abramson S, Altman RD, Arden N, BiermaZeinstra S, Brandt KD, Croft P, Doherty M, Dougados M, Hochberg M, Hunter DJ,
Kwoh K, Lohmander LS, and Tugwell P. OARSI recommendations for the
management of hip and knee osteoarthritis, Part II: OARSI evidence-based, expert
consensus guidelines. Osteoarthritis Cartilage 16: 137-162, 2008.
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
696
697
698
699
700
701
702
703
704
705
706
707
708
709
710
711
712
713
714
715
716
717
718
719
720
721
722
723
724
725
726
727
728
729
730
731
732
733
734
735
736
737
738
739
740
741
742
743
744
745
5
Neuromuscular adaptation in knee osteoarthritis
746
747
748
749
750
751
752
6
83.
Zhang W, Nuki G, Moskowitz RW, Abramson S, Altman RD, Arden NK,
Bierma-Zeinstra S, Brandt KD, Croft P, Doherty M, Dougados M, Hochberg M, Hunter
DJ, Kwoh K, Lohmander LS, and Tugwell P. OARSI recommendations for the
management of hip and knee osteoarthritis: part III: Changes in evidence following
systematic cumulative update of research published through January 2009.
Osteoarthritis Cartilage 18: 476-499, 2010.
753
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
Neuromuscular adaptation in knee osteoarthritis
FIGURE CAPTIONS
Figure 1 Device to measure proprioception
Figure 2 Displacement and acceleration of the perturbation platform
Figure 3 Intervals of the stance phase used in the analysis. Knee flexion angle (top) and
quadriceps EMG activity (bottom). IC-Initial Contact; PKF-Peak Knee Flexion; PKE-Peak
Knee Extension
Figure 4 Binning of average medial hamstring EMG data during the Midstance Interval.
from one subject to assess adaptation. Individual trials are shown in top graph, and the
average of every 5 trials is shown in bottom graph. Unperturbed Trials 1-10 are shown in
black and perturbed trials 1-30 are shown in Gray. The trial that is circled is that in which the
maximum adaptation had occurred.
Figure 5 Knee Flexion (top) and muscle activation (bottom 3 graphs) during the Midstance.
Average of 10 unperturbed trial (LEVEL) and 1st 5 perturbation trials (P1- P5). Asterisks
indicate statistically significant difference (P < 0.05).
Figure 6 Knee Flexion and muscle activation during the Midstance during level walking and
after maximum adaptation had occurred. Asterisks indicate statistically significant difference
(P < 0.05).
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
754
755
756
757
758
759
760
761
762
763
764
765
766
767
768
769
770
771
772
773
774
775
776
1
Neuromuscular adaptation in knee osteoarthritis
777
Table 1. Age, Gender, BMI, KL grade in controls and OA subjects. Values are Mean
778
(SD). P values are from independent samples t-tests for age and BMI, and from chi-
779
square tests for Gender and KL distribution.
1
780
Control
Osteoarthritis
P
Age
62. 0 (10.5)
66.6 (8.4)
0.066
BMI
27.4 (5.3)
29.7 (4.8)
0.080
12:11
16:21
χ2=0.455, P = 0.500
Male: Female
KL 3
NA
KL 4
781
NA = Not Applicable
782
BMI = Body Mass index
783
KL = Kellgren –Lawrence grade
12 (33%)
10 (27%)
χ2=1.03, P=0.60
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
15 (40%)
KL 2
Neuromuscular adaptation in knee osteoarthritis
784
785
Table 2. Function, proprioception, structure and strength variables in controls and OA
subjects.
Control
Osteoarthritis
P
Symptoms
98.9 (2.5)
62.4 (14.6)
< 0.001
Pain
99.5 (1.8)
64.4 (14.9)
< 0.001
ADL
99.7 (1.3)
70.3 (17.0)
< 0.001
<4
1 (4.3)
15 (40%)
=4
0 (0)
7 (18%)
=5
22 (95.7)
16 (42%)
1.1 (1.1)
1.1 (0.8)
0.915
0.8 (0.4)
0.9 (0.5)
0.355
0.9 (0.5)
1.2 (0.7)
0.107
1.4 (0.9)
1.8 (1.0)
0.092
Medial Joint Space Width (mm)
4.3 (0.7)
0.9 (1.5)
< 0.001
Alignment (Degrees)
178.5 (2.5)
174.4 (3.8)
< 0.001
Stair Climbing Test (sec)
10.0 (1.5)
13.7 (5.1)
0.001
Walking speed (m/sec)
1.6 (0.2)
1.3 (0.2)
< 0.001
Quadriceps Strength (N/BMI)
25. 4(10.1)
20.9 (7.2)
0.037
KOOS
KOS-I*
< 0.001
flexion)
At 15° Flexion (into
TTDPM
extension)
(Degrees)
At 45° Flexion (into
flexion)
At 45° Flexion (into
extension)
All values are Mean (Standard Deviation) except for KOS-I.
*Number of participants (%)
KOOS = Knee injury and osteoarthritis Outcome Score
ADL = Activities of Daily Living
KOS-I = Knee Outcome Survey- Instability item score
TTDPM = Threshold to Detect Passive Motion
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
At 15° Flexion (into
786
787
788
789
790
791
1
Neuromuscular adaptation in knee osteoarthritis
792
Table 3. Knee Angle at Initial Contact and muscle activation for all muscles during the preactivation phase. Average of 10 unperturbed trial
793
(LEVEL) and 1st 5 perturbation trials (P1- P5). Grey shading indicates statistically significant difference between adjacent trials (P < 0.05).
794
Variable
Knee Flexion at Initial
Contact (Degrees)
Control
OA
Level
6.1 (4.3)
9.9 (6.8)
P1
7.7 (6.2)
11.6 (7.1)
P2
8.7 (5.9)
12.6 (6.9)
P3
8.4 (6.3)
11.6 (7.3)
P4
8.0 (6.0)
11.9 (7.1)
P5
7.7 (6.0)
11.6 (7.4)
Medial Quadriceps
(%Max)
Control
12.8 (8.2)
14.6 (11.6)
16.4 (10.7)
14.6 (9.5)
11.4 (8.1)
12.6 (8.0)
OA
14.6 (8.7)
18.3 (10.1)
18.5 (11.1)
17.8 (9.3)
18.5 (11.3)
17.8 (10.5)
Lateral Quadriceps
(%Max)
Control
15.0 (6.4)
17.6 (3.5)
18.6 (8.8)
17.8 (10.6)
16.3 (10.4)
14.9 (9.7)
OA
16.1 (8.3)
20.2 (10.8)
20.3 (11.7)
21.9 (13.0)
21.8 (12.0)
20.0 (10.6)
Medial Hamstrings
(%Max)
Control
16.3 (9.5)
21.4 (14.4)
23.2 (14.1)
25.1 (14.6)
23.9 (14.9)
21.8 (12.2)
OA
18.1 (12.2)
25.7 (22.5)
25.1 (15.1)
27.1 (19.7)
14.1 (14.7)
25.0 (14.7)
Lateral Hamstrings
(%Max)
Control
16.6 (6.7)
19.4 (10.8)
23.7 (14.6)
23.9 (13.1)
23.0 (12.0)
20.7 (10.5)
OA
Control
OA
21.5 (8.7)
2.4 (2.2)
4.8 (5.9)
28.2 (14.9)
4.2 (6.1)
9.2 (11.5)
27.5 (11.1)
6.0 (7.4)
10.1 (10.4)
28.1 (104)
7.3 (6.7)
9.9 (9.8)
26.8 (11.)
6.6 (6.3)
10.0 (9.9)
26.6 (10.4)
6.4 (6.8)
9.2 (9.8)
Control
6.8 (12.3)
9.6 (18.5)
13.0 (17.6)
14.8 (19.0)
12.2 (15.0)
12.5 (14.5)
OA
6.4 (8.0)
11.3 (13.3)
13.7 (12.8)
13.3 (15.3)
13.0 (12.8)
11.3 (11.5)
Medial Gastrocnemius
(%Max)
Lateral Gastrocnemius
(%Max)
795
796
797
798
799
800
801
1
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
Neuromuscular adaptation in knee osteoarthritis
2
st
802
Table 4. Flexion Excursion and muscle activation for all muscles during the Loading Response. Average of 10 unperturbed trial (LEVEL) and 1
803
5 perturbation trials (P1- P5). Grey shading indicates statistically significant difference between adjacent trials (P < 0.05).
804
Variable
Flexion Excursion
(Degrees)
Medial Quadriceps
(%Max)
Control
OA
Control
OA
Level
15.0 (2.7)
10.0 (3.8)
26.7 (15.8)
30.4 (16.2)
P1
12.3 (4.1)
7.8 (3.8)
27.9 (19.6)
37.7 (21.4)
P2
11.2 (3.9)
6.9 (3.5)
28.8 (17.1)
39.3 (21.3)
P3
11.4 (4.4)
7.9 (3.9)
30.4 (21.3)
39.9 (26.6)
P4
12.2 (3.9)
8.0 (4.0)
28.4 (17.6)
37.5 (22.2)
P5
11.8 (3.6)
8.3 (3.4)
28.0 (19.6)
35.7 (21.9)
Lateral Quadriceps
(%Max)
Control
26.7 (11.3)
32.7 (26.2)
28.3 (14.5)
30.9 (18.2)
30.8 (18.6)
29.0 (17.5)
OA
32.7 (14.0)
38.9 (19.4)
40.0 (23.3)
40.4 (25.4)
41.2 (22.3)
40.7 (22.6)
Medial Hamstrings
(%Max)
Control
6.8 (5.7)
12.2 (10.0)
17.9 (15.2)
20.9 (17.5)
19.4 (15.0)
18.2 (14.7)
OA
11.0 (11.4)
18.8 (24.7)
22.0 (19.5)
23.7 (30.1)
23.6 (28.1)
22.0 (20.5)
Lateral Hamstrings
(%Max)
Control
10.2 (7.9)
13.6 (12.0)
16.7 (12.6)
18.2 (12.4)
18.7 (12.2)
18.9 (14.2)
OA
Control
OA
20.0 (12.1)
4.4 (3.7)
9.4 (13.0)
23.9 (15.2)
6.1 (5.7)
10.7 (17.4)
28.6 (14.9)
6.5 (5.9)
11.9 (15.7)
28.0 (13.9)
7.5 (6.4)
10.9 (13.7)
28.7 (12.6)
6.3 (5.4)
11.0 (12.7)
27.5 (15.4)
4.7 (4.1)
9.5 (13.5)
Control
8.2 (7.2)
10.4 (9.8)
11.1 (11.0)
11.8 (12.2)
11.8 (12.4)
10.6 (11.2)
OA
11.4 (10.2)
12.5 (12.1)
14.8 (12.4)
14.8 (15.2)
14.4 (14.2)
12.4 (9.7)
Medial Gastrocnemius
(%Max)
Lateral Gastrocnemius
(%Max)
805
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
ed from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
une 18, 2017
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on June 18, 2017