Factors associated with greater co-contraction during walking and quadriceps exercises in patients with knee osteoarthritis

Abstract

Background

Patients with knee osteoarthritis exhibit greater knee muscle co-contraction, and which in turn is a risk factor for disease progression.

Objective

The aims of this study were to assess the muscle co-contraction during walking and quadriceps exercises in patients with medial knee osteoarthritis, and to identify the factors most associated with the alterations in co-contraction.

Methods

The subjects were 12 women with medial knee osteoarthritis and 13 asymptomatic controls. Kinematic and kinetic parameters during walking, and co-contraction indices during walking, knee extension and straight leg raising exercises were measured. The factors associated with the alteration in co-contraction in the osteoarthritis group were determined by linear regression analyses.

Results

Compared with the control group, the osteoarthritis group showed significantly greater co-contraction of the vastus lateralis and biceps femoris (VLBF) in two quadriceps exercises as well as the VLBF, co-contraction of the vastus lateralis and lateral gastrocnemius (VLLG) in walking. In linear regression analyses, the VLBF and VLLG in walking were associated with knee extension moment and knee pain frequency in daily life. The VLBF in knee extension and straight leg raising exercise were associated with knee flexion angle in a quiet standing position and knee varus peak angle during the stance phase of walking.

Conclusions

Greater muscle co-contractions were observed in not only walking but quadriceps strengthening exercises in patients with knee OA. Besides, the factors of these patterns were different in different tasks. These findings may help the development of more effective rehabilitation strategies for patients with knee osteoarthritis.

Keywords

Knee osteoarthritis muscle co-contraction gait muscle strengthening exercise

Introduction

Muscle co-contraction refers to the simultaneous recruitment of synergistic muscles, agonist and antagonist muscles crossing a joint during dynamic tasks.^1,2 Muscle co-contraction of agonist and antagonist muscles, such as the knee flexors and extensors crossing a joint of the lower limbs, is a common strategy adopted to reduce strain and shear forces at the joint, but it increases compressive forces and joint mechanical load.³

Cumulative mechanical load is a risk factor for knee osteoarthritis (OA), a degenerative joint disease.^4,5 Patients with knee OA exhibit greater muscle co-contraction around the knee joint during walking,^6,7 which may be an attempt to stabilize the knee joint and avoid pain.^6,8 However, this response inhibits the knee’s shock absorption mechanism and increases harmful loads on the joint, which can result in progression of the OA.⁹ Therefore, the reduction of excessive co-contraction is important to reduce OA symptoms and slow the progression of OA.

Various factors have been reported to contribute to the greater muscle co-contraction during walking in patients with knee OA, including knee instability,^10,11 medial compartment joint loading,^12,13 internal knee extension moment,¹⁴ the severity of OA,^15–17 knee muscle strength,¹⁸ gait speed,¹⁹ and knee pain.^14,18,20,21 Studies have examined the associations between greater co-contraction and knee instability,^10,11 medial compartment joint loading,¹³ internal knee extension moment,¹⁴ the severity of OA,¹⁵ and knee pain.^14,20 However, to the best of our knowledge, no study has extensively evaluated multiple factors, so the most associated factor with the greater co-contraction in patients with knee OA remains unclear.

Quadriceps strengthening exercise programs are commonly prescribed for patients with knee OA to improve muscle strength,^22,23 knee pain, physical function, and quality of life.^22,24 However, there is no consensus on whether strengthening exercises reduce muscle co-contraction.^18,25 The basic muscle strengthening exercises most often used for patients with knee OA are open kinetic chain (OKC) exercises, single-joint or single-muscle group exercise.²⁶ In healthy subjects, greater muscle co-contraction around the knee joint has rarely been observed during OKC exercises, whereas it has been reported during closed kinetic chain (CKC) exercises such as the squat and lunge.^27,28 In patients with knee OA, greater muscle co-contraction has been observed while a CKC motion (descending a step),⁶ but there has been no investigation of co-contraction during OKC quadriceps exercises. If muscle co-contraction increases during simple OKC quadriceps exercises, repeating these exercises may exacerbate the co-contraction pattern, with potential progression of the OA.

The aims of this study were (i) to investigate knee muscle co-contraction during walking and OKC quadriceps exercises in patients with knee OA and (ii) to identify the most associated factors with alterations in muscle co-contraction. Understanding the factors associated with alterations in muscle co-contraction in knee OA could lead to the development of more effective rehabilitation strategies.

Methods

Subjects

Women are at higher risk of OA symptoms and of developing OA than men.^29,30 Additionally, the relationship between quadriceps and the prevalence or symptoms of knee OA has been pointed out, especially in women.³¹ Therefore, we limited the subjects to women. Twelve women diagnosed with medial knee OA and 13 age-matched asymptomatic women were recruited for this study (Table 1). The OA group subjects were recruited from local orthopedic clinics and an employment service center and met the following inclusion criteria: aged ≥65 years, had medial knee pain in a prior month,³² and radiographically diagnosed with medial compartment OA by orthopedic surgeons using the Kellgren–Lawrence (K/L) grading system.³³ In the knee OA group, the affected leg was tested for unilateral OA subjects, and the leg with the stronger symptoms was tested for bilateral OA subjects. Asymptomatic control group subjects were recruited from an employment service center; none had symptoms of degenerative joint disease in the lower extremity. The following exclusion criteria were applied for both groups: candidacy for any surgery; a history of central nervous system disease, serious heart or lung disease, or any lower extremity injury or surgery; rheumatoid arthritis; and inability to walk independently without ambulatory aids and assistance.

Table 1.

Characteristics of the knee OA and control groups.

Variables	Knee OA group (n = 12)	Control group (n = 13)	p
Age (years)	70.1 (3.2)	70.8 (2.8)	0.58
Body height (m)	1.54 (0.06)	1.51 (0.05)	0.15
Body weight (kg)	59.0 (8.1)	53.4 (8.6)	0.11
BMI (kg/m²)	24.9 (3.2)	23.8 (3.7)	0.44
JKOM total score	46.6 (9.0)	29.9 (3.7)	<0.001*
Knee varus angle in a quiet standing position^a (deg)	184.1 (3.9)	177.6 (4.1)	<0.001*
K/L grading system (n)	I: 5
	II: 2
	III: 3
	IV: 2

JKOM, Japanese Knee Osteoarthritis Measure; K/L, Kellgren–Lawrence; *, p values of <0.05 were statistically significant. Values are expressed as mean (SD).

^a>180° means varus knee.

The severity of knee OA in the OA group was K/L grade I in 5 patients, grade II in 2 patients, grade III in 3 patients, and grade IV in 2 patients. Their main symptom was knee pain. None reported feelings of knee instability.

Assessment of knee pain

The Japanese Knee Osteoarthritis Measure (JKOM)³⁴ was used to assess the subjects’ knee conditions in their daily lives. Each subject was asked to indicate the intensity and frequency of knee pain in these few days. Pain intensity was valuated using a visual analog scale (VAS) with a range of 0 to 100 mm, 0 indicating no pain and 100 indicating the worst possible pain. Pain frequency was assessed using a 5-point scale (5: always; 4: often; 3: sometimes; 2: rarely; 1: never).³⁵ Knee pain intensity during the walking trials was also assessed using the VAS.

Knee joint range of motion and knee angles

To measure range of motion (RoM), reflective markers were attached to the greater trochanters and lateral epicondyles of the femurs, the heads of the fibulae, and the lateral malleoli of the tibiae; then photographs were taken of the end angles of passive knee extension and flexion in the supine position, and of the knee flexion angle and knee varus angle in a quiet standing position.³⁶ The photographs were taken using a digital camera (IXY DIGITAL 510 IS; Canon, Tokyo, Japan). The knee angles were measured from the photographs using ImageJ 1.43u software (National Institutes of Health; MD, USA).

Measurement of maximum joint torque

The maximum isometric knee extension, knee flexion, and ankle plantar flexion torques were measured using a hand-held dynamometer (µTas MT-1; Anima, Tokyo, Japan) during maximal voluntary isometric contraction (MVIC). The knee extension torque was measured in a seated position with the knee flexed at approximately 45°.¹⁹ The knee flexion torque measured with the subject prone, with the knee flexed at approximately 60°.¹⁹ The ankle plantar flexion torque was measured with the subject supine, with the ankle in the neutral position.²¹ During the measurement, the subject was asked to grip the edge of the bed with both hands. Isometric contraction for 3 s was performed twice, separated by a 1-min rest period. The torques, averaged over two trials, were normalized to the subject’s body weight (Nm/kg). Electromyogram (EMG) data were recorded during the MVIC trial for each muscle (as described later).

Tasks

The subjects performed three tasks: a walking task and then two OKC quadriceps exercise tasks. Prior to the measurements, the subjects practiced each task to become familiar with the motion and movements. For the walking task, the subjects were instructed to walk along a flat 10-m walkway at a self-selected gait speed. The task was performed three times, and the mean values were used in the analysis. The two OKC quadriceps exercise tasks were a knee extension task and a straight leg raising (SLR) task. For the knee extension task, the subjects sat on a height-adjustable chair without a backrest and armrests, with their lower legs vertical and their arms folded across their chest. After an oral cue, the subjects extended the knee joint from the starting position to its maximum angle over 3 s, held it there for 3 s, and then returned to the starting position over 3 s. For the SLR task, the subjects lay supine on a bed with both legs extended straight and their arms folded across their chest. After an oral cue, the subjects flexed the hip joint of one leg over 3 s until their toe touched a bar that was 10 cm above the toe at the starting position, held their leg there for 3 s, and then returned to the starting position for 3 s. A metronome set at 60 beat/min was used to time the motion speed. The quadriceps exercise tasks were performed twice, and the mean values were used in the analysis.

Motion data acquisition and analysis

Infrared-reflective markers were attached to 45 landmarks: the temples, lateral ends of the superior nuchal line, tragi, acromia, olecranon processes, styloid processes of the ulnae, superior edges of the iliac crests, anterior superior iliac spines, posterior superior iliac spines, greater trochanters, lateral and medial epicondyles of the left and right femurs, lateral and medial joint spaces of the left and right knee joints, lateral and medial condyles of the left and right tibiae, bilateral lateral and medial malleoli, bilateral first and fifth metatarsal heads, and bilateral calcaneal tuberosities. Kinematic data were collecting using a three-dimensional motion analysis system (Vicon MX; Vicon Motion Systems, Oxford, UK) with six infrared cameras at a sampling rate of 100 Hz. At the same time, three-dimensional ground reaction forces were collected using eight force plates (TF-400-A; Tec Gihan, Kyoto, Japan) at a sampling frequency of 1000 Hz. The stance phase during walking (from initial contact to toe-off of ipsilateral leg) was defined by a vertical ground reaction force >10 N.³⁷ For the quadriceps exercises, joint movement from initiation to termination was defined by the joint angle being greater than the mean plus three standard deviations of the joint angle for the baseline period prior to the oral cue.

The data processing and analysis were performed using BodyBuilder software (Vicon Motion Systems, Oxford, UK). The coordinates of the joint center, joint excursion, peak angle from initial contact to mid-stance of ipsilateral leg during walking, and the maximum, mean, and impulse of the knee joint moment in the stance phase were calculated as described previously^38,39 (Supplemental Table). The joint moments were normalized to the subject’s body weight.

EMG acquisition and analysis

Surface EMG data were acquired using an EMG Master (Mediarea Support Business Union, Okayama, Japan), with a pass-band of 15–500 Hz and a sampling frequency of 1000 Hz. The skin surface was prepared by shaving and then cleaning with the skin preprocessing agent Skin Pure (Nihon Kohden, Tokyo, Japan). Bipolar surface circular Ag/AgCl electrodes (Blue-sensor M-00-S; Ambu, Ballerup, Denmark) were placed 30-mm apart, center to center, in line with the muscle fibers over the vastus medialis, vastus lateralis, semitendinosus, biceps femoris, lateral gastrocnemius, and medial gastrocnemius muscles. The electrodes were placed according to the SENIAM guidelines,⁴⁰ with a reference electrode placed over the radial styloid process. To analyze the co-contraction of muscle pairs, co-contraction indices (CCIs) were calculated from 100 ms prior to the initial contact to the toe-off of ipsilateral leg during walking, and from 100 ms prior to movement initiation to movement termination during the quadriceps exercises,^41,42 for the following muscle pairs: vastus medialis and semitendinosus (VMST), vastus medialis and medial gastrocnemius (VMMG), vastus lateralis and biceps femoris (VLBF), and vastus lateralis and lateral gastrocnemius (VLLG) (Figure 1). The highest root mean square signals during each MVIC trial, averaged over a moving 50-ms window, were used for normalization of the values for each muscle.⁴³ The raw EMG data for each trial were subjected to full-wave rectification and then expressed as a percentage of the EMG value obtained during MVIC (%MVIC). Each CCI was determined as follows, using the method described by Lewek et al.¹⁰

CCI = \frac{1}{100} \int_{i = 1}^{100} {\frac{{l o w e r E M G}_{i}}{{h i g h e r E M G}_{i}} ({l o w e r E M G}_{i} + {h i g h e r E M G}_{i})}

Figure 1.

The definition of analytical range of the muscle co-contractions. The muscle co-contractions were determined using the equation described by Lewek et al.⁷ The sample waveforms of vastus lateralis (VL) (dashed), biceps femoris (BF) (dotted), and co-contraction for VL and BF (VLBF) (solid) in a subject with OA. The upper panel (a) displays the waveforms during walking. Dashed vertical lines show the timing of initial contact, 100 ms prior to initial contact, and toe-off. The middle panel (b) displays the waveforms during knee extension exercise. Dashed dotted line shows the knee joint angle in the sagittal plane (full extension is 0° and the positive values indicate the knee joint flexion angle). Dashed vertical lines show the timing of knee motion initiation, 100 ms prior to knee motion initiation, and knee motion termination. The lower panel (c) displays the waveforms during straight leg raising exercise. Dashed dotted line shows the hip joint angle in the sagittal plane (the positive values indicate the hip joint flexion angle). Dashed vertical lines show the timing of hip motion initiation, 100 ms prior to hip motion initiation, and hip motion termination.

Here, the terms lower EMGi and higher EMGi refer to the muscle activity in the less active and more active muscle, respectively, in each muscle pair.⁶

Statistical analyses

Statistical analyses were performed using IBM SPSS Statistics 26 (IBM Japan, Tokyo, Japan). The Shapiro–Wilk test was applied to assess variables for normality of their distributions. For normally distributed data, two-sample t-test (for homoscedastic data) or Welch’s test (for heteroscedastic data) were used. The Mann–Whitney U test was used if the data were not normally distributed.

In the OA group, Pearson’s correlation analysis (or Kendall’s correlation analysis if the data were not normally distributed) was used to evaluate the relationships between the CCIs and the following parameters: gait speed, knee pain intensity and frequency, maximum joint torques, RoM of passive knee extension, knee flexion angle in a quiet standing position, K/L grading system, knee varus peak angle during the stance phase of walking, and external knee varus and internal knee extension moments. Stepwise linear regression analyses were used to determine the most associated factors with alterations in CCIs in OA group. The independent variables were the parameters significantly correlated with CCIs in the correlation analyses. To avoid multicollinearity, if any two independent variables showed a correlation with a correlation coefficient was ≥0.70, the more statistically significant of the two variables was entered into the regression model. The significance level for all tests was <0.05.

Results

Subject characteristics

The subject’s characteristics, knee varus angle in a quiet standing position, JKOM total scores, and radiographic scores are shown in Table 1. The knee varus angle was significantly larger in the OA group than in the control group (p < 0.001). There were no significant differences between the two groups in age, height, body weight, or body mass index.

Knee pain, maximum joint torque, RoM, and knee angle

Table 2 compares knee pain, maximum joint torques, knee joint RoMs, and knee flexion angle in a quiet standing position between the two groups. Knee pain intensity and frequency were significantly higher in the OA group than in the control group (p < 0.001). Knee pain intensity during the walking trial was higher in the OA group than in the control group, but this difference was not statistically significant.

Table 2.

Knee pain, maximum joint torque, knee joint range of motion, and walking parameters.

Variables	Knee OA group (n = 12)	Control group (n = 13)	p
Knee pain
Intensity in daily life (VAS, mm)	28.1 [24.7]	0 [0]	<0.001*
Frequency in daily life (5-point scale, 1–5)	4 [1.5]	1 [0]	<0.001*
Intensity during walking trial (VAS, mm)	0 [4.9]	0 [0]	0.077
Maximum joint torque (Nm/kg)
Knee extension	0.71 (0.10)	0.76 (0.14)	0.35
Knee flexion	0.38 (0.11)	0.40 (0.08)	0.67
Ankle plantar flexion	0.79 (0.29)	0.78 (0.33)	0.95
Knee range of motion (deg)
Passive knee extension^a	−5.8 [3.5]	−2.3 [3.2]	0.003*
Passive knee flexion^b	139.4 (15.0)	152.5 (5.3)	0.013*
Knee flexion angle in a quiet standing position^b (deg)	16.2 (6.8)	7.2 (5.3)	0.001*
Gait speed (m/s)	0.87 (0.15)	1.1 (0.16)	0.004*
Knee excursion (deg)
Flexion from IC to Mst	9.6 (3.9)	12.2 (2.5)	0.054
Extension from IC to Mst	3.5 [3.9]	8.0 [6.2]	0.016*
Total from IC to Mst^c	13.9 (6.5)	20.1 (4.9)	0.013*
Knee varus peak angle during the stance phase of walking (deg)	191.2 (3.3)	188.9 (3.8)	0.079
Internal knee extension moment
Maximum joint moment (Nm/kg)	0.60 (0.15)	0.63 (0.23)	0.72
Mean joint moment (Nm/kg)	0.30 (0.11)	0.23 (0.08)	0.06
Joint moment impulse (Nm•s/kg)	0.23 (0.07)	0.15 (0.05)	0.001*
External knee varus moment
The first peak (Nm/kg)	0.57 (0.17)	0.45 (0.16)	0.069
The second peak (Nm/kg)	0.56 (0.15)	0.40 (0.17)	0.028*
Mean joint moment (Nm/kg)	0.38 (0.11)	0.28 (0.12)	0.040*
Joint moment impulse (Nm•s/kg)	0.28 (0.08)	0.18 (0.08)	0.008*

VAS, visual analog scale; IC, initial contact; Mst, mid-stance; *, p-values of <0.05 were statistically significant. Values are expressed as mean (SD) or median [IQR].

^aFull extension angle of the knee joint is 0° and the negative values indicate the limited knee extension.

^bFull extension angle of the knee joint is 0° and the positive values indicate the knee joint flexion angle.

^cSum of flexion and extension excursion.

The RoMs of passive knee extension and flexion were significantly smaller in the OA group than in the control group (p < 0.01; p < 0.05). The knee flexion angle in a quiet standing position showed significantly greater flexion in the OA group than in the control group (p = 0.001).

There were no significant differences in any of the maximum joint torques between the two groups.

Walking parameters

Table 2 summarizes the walking parameters in the stance phase. The gait speed was slower in the OA group than in the control group (p < 0.01). Knee extension excursion and total excursion (the sum of flexion and extension excursion, Supplemental Table) were significantly less in the OA group than in the control group (p < 0.05). Knee flexion excursion was also less in the OA group, but the difference was not statistically significant (p = 0.054). The knee varus peak angle during the stance phase was greater in the OA group than in the control group, but the difference was not statistically significant (p = 0.079).

The internal knee extension moment impulse was significantly greater in the OA group than in the control group (p = 0.001). The graph of the external knee varus moment in the stance phase showed a bimodal shape⁴⁴; we therefore compared the two peaks between the groups (Supplemental Table). The second peak, mean, and impulse of the external knee varus moment were significantly greater in the OA group (p < 0.05). No differences were found between the two groups for the maximum and mean internal knee extension moment and for the first peak of the external knee varus moment.

CCIs

Table 3 compares the four CCIs for the stance phase during walking and for the quadriceps exercises. VLBF and VLLG during walking were significantly greater in the OA group than in the control group (p < 0.05). However, no differences were observed between the two groups for VMST and VMMG in walking. VLBF during knee extension and SLR exercises were significantly greater in the OA group than in the control group (p = 0.001; p < 0.05), but no differences were observed for other CCIs in the quadriceps exercises.

Table 3.

CCIs for the stance phase of walking and quadriceps strengthening exercises.

Variables	Knee OA group^a	Control group^b	p
Stance phase of walking
VMST	6.9 (2.9)	6.7 (2.8)	0.87
VMMG	9.9 (4.4)	6.8 (3.0)	0.055
VLBF	10.0 (4.2)	6.4 (2.4)	0.016*
VLLG	10.9 [7.3]	7.6 [2.1]	0.014*
Knee extension exercise
VMST	2.5 (0.97)	2.4 (0.73)	0.70
VMMG	2.4 [1.4]	1.6 [2.0]	0.53
VLBF	5.7 (2.1)	2.9 (1.2)	0.001*
VLLG	2.6 [1.2]	2.2 [1.3]	0.72
Straight leg raising exercise
VMST	1.6 [0.69]	1.6 [0.63]	0.90
VMMG	1.3 (0.60)	1.3 (1.8)	0.92
VLBF	3.02 [1.5]	1.9 [1.0]	0.044*
VLLG	1.5 (1.7)	1.3 (1.7)	0.72

CCIs, Co-contraction indices calculated from surface EMG data using the method described by Lewek et al.⁷; VMST, vastus medialis and semitendinosus; VMMG, vastus medialis and medial gastrocnemius; VLBF, vastus lateralis and biceps femoris; VLLG, vastus lateralis and lateral gastrocnemius; *, p-values of <0.05 were statistically significant. Values are expressed as mean (SD) or median [IQR].

^an = 12 for co-contraction indices for the stance phase of walking and n = 11 for co-contraction indices for quadriceps strengthening exercises (data of quadriceps exercises could not be collected from a subject due to the experimental problems).

^bn = 13 for co-contraction indices for the stance phase of walking and n = 11 for co-contraction indices for quadriceps strengthening exercises (data of quadriceps exercises could not be collected from two subjects due to the experimental problems).

Correlation analyses for the OA group

Correlation analyses for each of the CCIs were performed for the parameters that differed significantly between the groups (Table 4). VLBF during walking showed significant correlations with knee pain frequency in daily life (r = 0.48, p < 0.05), knee pain intensity during the walking trial (r = −0.50, p < 0.05), maximum internal knee extension moment (r = 0.81, p = 0.001), mean internal knee extension moment (r = 0.61, p < 0.05), and impulse of internal knee extension moment (r = 0.64, p < 0.05). VLBF during the knee extension exercise showed a significantly correlation only with the knee flexion angle in a quiet standing position (r = 0.69, p < 0.05), and VLBF during SLR was significantly correlated only with the knee varus peak angle during the stance phase (r = 0.71, p = 0.001). The only significant correlation observed for VLLG during walking was knee pain frequency in daily life (r = 0.65, p < 0.01).

Table 4.

The results of correlation analyses in the knee OA group.

Variables	VLBF during stance phase of walking		VLBF during ext ex.		VLBF during SLR ex.		VLLG during stance phase of walking
Variables	r	p	r	p	r	p	r	p
Gait speed	0.030	0.93	−0.076	0.82	0.055	0.82	0.30	0.17
Knee pain
Frequency in daily life	0.48	0.039*	0.098	0.69	0.020	0.94	0.65	0.006*
Intensity in daily life	0.22	0.34	−0.093	0.70	−0.06	0.81	0.31	0.17
Intensity during walking trial	−0.50	0.037*	−0.046	0.86	0.19	0.47	−0.13	0.59
Maximum joint torque of knee extension	−0.17	0.60	−0.054	0.88	−0.16	0.48	−0.33	0.13
Passive RoM of Knee extension	0.030	0.89	0.091	0.70	0.16	0.48	−0.33	0.13
Knee flexion angle in a quiet standing position	0.37	0.24	0.69	0.019*	0.27	0.24	0.36	0.10
K/L grading system	0.40	0.095	0.42	0.097	0.00	1.00	0.36	0.13
Knee varus peak angle during the stance phase of walking	0.21	0.51	0.58	0.06	0.71	0.001*	−0.12	0.64
External knee varus moment during walking
The first peak	−0.031	0.92	−0.25	0.47	−0.24	0.31	−0.061	0.78
The second peak	−0.062	0.85	−0.25	0.45	−0.20	0.39	−0.091	0.68
Mean	−0.030	0.93	−0.17	0.62	−0.27	0.24	−0.12	0.58
Impulse	−0.16	0.62	−0.23	0.50	−0.24	0.31	−0.15	0.49
Internal knee extension moment during walking
Maximum	0.81	0.001*	0.52	0.10	0.42	0.073	0.24	0.27
Mean	0.61	0.034*	0.43	0.19	0.27	0.24	0.33	0.13
Impulse	0.64	0.027*	0.37	0.26	0.35	0.14	0.21	0.34

VLBF, vastus lateralis and biceps femoris; VLBF during ext ex., vastus lateralis and biceps femoris during knee extension exercise; VLBF during SLR ex., vastus lateralis and biceps femoris during straight leg raising exercise; VLLG, vastus lateralis and lateral gastrocnemius; K/L, Kellgren–Lawrence; r, correlation coefficient; *, p-values of <0.05 were statistically significant.

Linear regression analyses for the OA group

Multiple or simple linear regression analyses, as appropriate, were performed for VLBF during walking, VLBF during knee extension exercise, VLBF during SLR, and VLLG during walking, using the variables indicating statistically significant correlation reported in the previous section (Table 4) as the independent variables (Table 5). For the internal knee extension moment to VLBF during walking, the only maximum internal knee extension moment was entered into the regression model as the independent variable to avoid multicollinearity (maximum internal knee extension moment showed correlations with mean internal knee extension moment, r = 0.81; maximum internal knee extension moment showed correlations with impulse of internal knee extension moment, r = 0.77). The statistically significant predictors for the CCIs were follows: for VLBF during walking, the maximum internal knee extension moment (R² = 0.62, p = 0.001); for VLBF during the knee extension exercise, the knee flexion angle in a quiet standing position (R² = 0.42, p = 0.05); for VLBF during SLR, the knee varus peak angle during the stance phase (R² = 0.70, p < 0.001); and for VLLG during walking, the knee pain frequency in daily life (R² = 0.39, p < 0.05). In all the regression analyses, effect size showed large (Cohen’s f² > 0.35)⁴⁵ and the residuals were normally distributed and residual versus fitted values were not heteroscedastic.

Table 5.

The results of simple and multiple regression analyses in the knee OA group.

Dependent variables	Independent variables	R²	B	95% CI		β	p	ES
Dependent variables	Independent variables	R²	B	Low	High	β	p	ES
VLBF during stance phase of walking	Maximum internal knee extension moment	0.62	22.6	10.1	34.1	0.81	0.001*	1.63
VLBF during knee extension ex.	Knee flexion angle in a quiet standing position	0.42	0.21	0.04	0.38	0.69	0.019*	0.72
VLBF during SLR ex.	Knee varus peak angle during the stance phase of walking	0.70	0.37	0.20	0.54	0.86	<0.001*	2.36
VLLG during stance phase of walking	Knee pain Frequency in daily life	0.39	3.1	0.68	5.5	0.67	0.017*	0.65

95% CI, 95% confidence interval; VLBF, vastus lateralis and biceps femoris; VLBF during knee extension ex., vastus lateralis and biceps femoris during knee extension exercise; VLBF during SLR ex., vastus lateralis and biceps femoris during straight leg raising exercise; VLLG, vastus lateralis and lateral gastrocnemius; R², adjusted R²; B, unstandardized regression coefficients; β, standardized regression coefficients; *, p-values of <0.05 were statistically significant; ES, effect sizes with Cohen’s f² (R²/1-R²).³⁹

Discussion

This study demonstrated relationships between greater VLBF and a higher maximum internal knee extension moment in walking, greater VLBF in knee extension exercises and a greater knee flexion angle in a quiet standing position, greater VLBF in SLR and a greater knee varus peak angle in stance phase of walking, and greater VLLG in walking and a higher knee pain frequency in daily life. To the best of our knowledge, this is the first study to establish the major factor among many factors associated with greater co-contraction in patients with knee OA.

In this study, most of subjects in the OA group (83%) had K/L grading systems I–III, indicating mild to moderate joint changes.^12,21 The OA group showed gait characteristics typical of patients with knee OA, including reduced gait speed, decreased knee excursion in the sagittal plane, increased knee varus peak angle during the stance phase, and increased knee external varus and internal extension moment,^46–51 as well as greater muscle co-contraction in the lateral knee muscles. This finding was consistent with previous reports that patients with relatively early stage of knee OA have greater co-contraction in the lateral knee muscles to protect medial joint.^16,21 We observed associations between greater both VLLG and VLBF in walking and higher knee pain frequency in daily life. Chronic pain and fear of pain can induce the modulation of muscle activity, including increases in the activity of antagonist muscle.^52–54 The association between knee pain and greater activity of the lateral gastrocnemius has also been reported.²⁰ The greater lateral muscle activities of knee may help to redistribute the medial load laterally.⁵⁵ These reports and the findings of this study suggest that greater VLLG and VLBF in walking may be muscle-guarding activity to reduce the medial knee pain that experienced by patients with knee OA in daily life. Patients with knee OA are typically asked about knee pain intensity; these findings suggest it may also be necessary to ask about pain frequency in the clinical interviews with patients with knee OA. VLBF in walking was significantly correlated with not only knee pain frequency in daily life (positive correlation) but also knee pain intensity during the walking trial (negative correlation) and the internal knee extension moments (positive correlation). These results may indicate that patients with OA increase muscle-guarding activity against the knee pain and stress experienced in daily life were attempting to reduce knee pain during the walking trial. However, alterations in antagonist muscle recruitment negatively affect tibiofemoral kinematics^56,57 and increase the load on knee joint structures such as the surfaces of the tibiofemoral joint, muscles, and ligaments.^12,58–60 The OA group walked with greater flexion in the knee joint in the stance phase than the control group. Greater VLBF and VLLG in walking may have interfered with the normal motion of knee extension. The tibiofemoral joint contact area decreases as the knee flexion angle increases.⁶¹ Thus, increased knee flexion in walking increase the contact pressure on the tibiofemoral joint. The OA group also showed increased external varus and internal extension knee moments, indicating mechanical stress on the knee joint. In summary, our results suggest that the knee joints of the subjects in OA group were subjected to higher load arising from kinematic, kinetic, and muscular factors. Greater co-contraction may help stabilize the knee joint and relieve pain in the short term, but it may lead to abnormal knee motion and harmful loads on the knee joint, potentially resulting in OA progression in the long term.

The subjects with knee OA showed greater VLBF even in the OKC quadriceps exercises. This suggests that they may have become accustomed to controlling their knees with antagonist muscles, even though the quadriceps muscle is the prime mover muscle in these exercises. The linear regression analyses indicated that greater VLBF in knee extension exercise in the OA group was associated with a greater knee flexion angle in a quiet standing position. This malposture could result in alterations in muscle activity or flexibility.^62,63 A standing posture with knee full extension needs little activity of the quadriceps and hamstring muscles because the stability of the knee joint depends on the passive stability system provided by, for example, the bones and ligaments.^64,65 However, the activity of these muscles increases as the knee flexion angle increases.^66,67 Appropriate joint stability and movement requires harmony between the passive (bones and ligaments), active (muscles), and neural systems.⁶⁸ A habitual standing posture with knee flexion, indicating a greater dependence on muscle activity in standing, might affect neuromuscular adaptation and result in alterations in muscle activity during knee extension exercises. Furthermore, the association between greater VLBF in SLR and a greater knee varus peak angle during the stance phase of walking may also be an indication of neuromuscular adaptation around the knee joint. Patients with knee OA who exhibit greater knee varus thrust may exert greater muscle co-contraction to keep the knee joint as straight as possible during walking.¹³ Thus, habitual abnormal knee varus movement during walking might affect muscle activity in SLR exercise, the task of which keeps their knee straight. These results provide evidence in support of not recommending aggressive quadriceps strengthening exercises for patients with knee OA who have excessive malalignment or laxity of the knee.⁶⁹ More effective rehabilitation strategies may require different exercises to be prescribed according to the specific characteristics of patients with knee OA, such as their knee flexion angle in a quiet standing posture or the knee varus peak angle during the stance phase of walking. Our findings may also prompt further studies to develop more effective rehabilitation strategies for patients with knee OA.

This study had several limitations. First, after correlation analyses, additional regression analyses were performed to find a more direct relationship with CCIs. However, the number of subjects was small for regression analyses; further research is needed with a larger number of subjects. However, the results of the regression analyses showed large effect sizes (Cohen’s f² > 0.35),⁴⁵ suggesting the results are meaningful. Nevertheless, further studies are needed with a larger number of subjects. Second, our sample population was limited to patients with medial knee OA who could walk without ambulatory aids. Finally, we did not confirm whether treatment for these factors reduced the co-contraction pattern. Future research is required to address these limitations.

Greater muscle co-contractions were observed in not only walking but also OKC quadriceps strengthening exercises in patients with knee OA. These patterns may be due to cumulative daily factors, including maximum internal knee extension moment and knee varus peak angle during the stance phase of walking, knee pain frequency, and knee flexion angle in a quiet standing position. Besides, the factor of these greater co-contractions may be different in different tasks. These findings could help the development of more effective rehabilitation strategies for patients with knee OA.

Supplemental Material

Supplemental Material - Factors associated with greater co-contraction during walking and quadriceps exercises in patients with knee osteoarthritis

Supplemental Material for Factors associated with greater co-contraction during walking and quadriceps exercises in patients with knee osteoarthritis by Yoshio Wakimoto, Masaya Anan, Kenji Tanimoto, Hiroka Hattori and Koichi Shinkoda in Physiotherapy Practice and Research

Footnotes

Author note

This work was performed at Hiroshima University, Hiroshima, Japan

Acknowledgements

The authors thank Dr. Masahide Yagi of Kyoto University for his valuable advices on data analysis.

ORCID iDs

Masaya Anan

Koichi Shinkoda

Ethical approval

The study was undertaken with the approval of the Ethics Committee of Division of Physical Therapy and Occupational Therapy Sciences, Graduate School of Health Sciences, Hiroshima University (No. 1201).

Informed consent

Prior to the study, the purpose of study was explained to all subjects, who all signed informed consent.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Supplemental material

Supplemental material for this article is available online.

Appendix

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