Radiological and clinical outcomes of concurrent hamstring stretching with quadriceps strengthening in patients with knee osteoarthritis: A randomized clinical trial

Abstract

BACKGROUND:

Hamstring shortening altered joint reaction forces during activities of daily living (ADL), causing knee pain. Moreover, weak quadriceps may negatively distribute the compressive and shear forces at the knee joint.

PURPOSE:

The study examined the effect of adding hamstring stretching to quadriceps strengthening exercises on joint space narrowing (JSN), medial joint space width (mJSW), and physical abilities in patients with knee osteoarthritis (KOA).

METHODS:

A total of 42 osteoarthritis patients, aged from 50 to 65 years, were randomized and assigned into 2 groups: the study and the control groups. Quadriceps strengthening exercises were given to both groups, while static hamstring stretching was applied to only the study group. Patients of both groups were screened with a weight-bearing x-ray beam to investigate the JSN, mJSW, and functional abilities measured in the WOMAC scale. The Outcomes were evaluated at the baseline and immediately after 6 weeks of treatment.

RESULTS:

The mJSW improved in the study group ( $p<$ 0.001) compared to the control group ( $p=$ 0.07). The OARSI JSN was enhanced significantly in both groups, but in favor of the study group ( $p<$ 0.001) over the control group ( $p=$ 0.046). Both MVIC and total score of WOMAC were significantly improved in both groups ( $p<$ 0.001).

CONCLUSION:

Adding static hamstring stretching to quadriceps strengthening exercises provided a substantial effect on mJSW, JSN, and functional abilities in KOA patients.

Keywords

Hamstring stretching quadriceps strengthening exercise joint space narrowing joint space width knee osteoarthritis

1. Introduction

Knee osteoarthritis (KOA) is a debilitating musculoskeletal problem that encumbers more than 250 million persons across the globe [1]. The relevant clinical findings in KOA patients include joint stiffness, decreased range of motion (ROM), quadriceps muscle weakness, and disturbed proprioception awareness [2]. Pain and functional limitations are the most frequent issues of complain in KOA patients, especially in people over 45 years of age (19.2–27.8%). X-ray revealed that around 37% of patients over 60 s years of age had KOA [3]. Joint space narrowing (JSN) is highly correlated with chronic knee osteoarthritis as well as meniscal tears [4]. Quadriceps weakness could increase the load on the knee joint. Moreover, quadriceps weakness may negatively distribute the compressive and shear forces at the knee joint [5, 6].

In a previous cohort study, weakness of quadriceps muscle was found to be highly associated with JSN of tibiofemoral and patellofemoral joints in females [7]. Culvenor et al. stated that the developed risks of cartilage damage in lateral patellofemoral arthritis in women were related to decreased quadriceps strength [8]. On the other hand, although increased quadriceps strength improved knee pain and functional abilities in patients with knee osteoarthritis, high quadriceps strength did correlate with cartilage loss of the tibiofemoral joint, even in malaligned knees [9].

The flexibility status of the hamstring muscles is one of the most important aspects that could influence soft tissues elasticity around the extended knee joint [10]. Hamstring shortening altered the biomechanics substantially, leading to increased joint reaction forces during activities of daily living (ADL), causing knee pain [11]. In comparing healthy subjects and patients suffering from KOA, hamstring flexibility was found higher in KOA compared to that in healthy subjects [12]. Hamstring tightness has an impact on the function and biomechanics of the knee and hip joints, possibly leading to dysfunction. Additionally, hamstring shortening could induce muscle weakness, improper action of the quadriceps muscle, and postural disorders [13]. Reduced hamstring flexibility leading to increased functional limitations in patients with KOA has already been proven. Such patients need to be introduced to hamstring stretching exercises [14].

Impairment of strength and flexibility in muscle around knee OA is one of the significant causes that affect the dynamic stability, functionality, and the ability of the knee joint to absorb the load [15]. Despite debate on whether quadriceps weakness plays an essential role in mJSW and JNS, and cartilage loss, little is known about the relationship between hamstring flexibility and quadriceps strength to maintain or improve knee joint space in KOA. Notably, this study is the first concerning the effect of hamstring stretching combined with quadriceps strengthening exercises on radiological and clinical measures in KOA. This study examined our hypothesis that the addition of hamstring stretching to quadriceps strengthening exercises helps improve the joint space narrowing (JSN) and medial joint space width (mJSW) as the primary outcome of measures, enhance physical abilities in patients with KOA as the secondary outcome.

2. Methods

2.1 Subjects

This study was a randomized controlled, double-blinded two-armed study in which a total of 50 patients, aged 50 to 65 years old, diagnosed with KOA were. All patients were diagnosed and referred by orthopedists and orthopedic surgeons to the physiotherapy outpatient clinic, College of Applied Medical Sciences, Prince Sattam Bin Abdulaziz University, Saudi Arabia. All patients were assigned and completed a consent form, which ensured the acceptance of participation. The ethical approval number of the study was registered to and granted from the ethical research committee (No. RHPT 022018) of the Physical Therapy and Health Rehabilitation Department. The existence or absence of JSN and osteophytes in the medial and lateral compartments of tibiofemoral joints was identified.

Figure 1.

Patient randomization and dropouts.

2.2 Inclusion criteria

The patients were recruited for the study if they met the followings criterias: (1) Their age ranged from 50 to 65 years; (2) their body mass index (BMI) is situated between 28 to 31 Kg/m ${}^{2}$ ; (3) the American College Rheumatology of Criteria confirmed knee (tibiofemoral joint) OA with symptoms for $\geqslant$ 6 months [16]; (4) they scored grade 2 or 3 in the Kellgren-Lawrence (K/L) grade system for rating the degree of KOA [17]; (5) for ensuring the same level of activity between the patients in the two groups, the modifiable activity questionnaire (MAQ) was given to all patients and recall survey results were obtained. The MAQ is a valid quantitative retrospective questionnaire that gives a thorough picture of activity levels in various people. Its grades are leisure, occupation, and transport [18]; (6) patients who suffered from medial unicompartmental osteoarthritis of the knee joint and scored one or higher according to Osteoarthritis Research Society International of joint space narrowing (OARSI JSN) and normal lateral knee compartment (OARSI JSN grade 0).

2.3 Exclusion criteria

Patients were excluded if (1) the lateral compartment of the tibiofemoral joint scored in OARSI JSN or had osteophytes, (2) they had practiced routine physical activities during the last six months, (3) any musculoskeletal problems, cardiovascular diseases, or knee surgery substantially interfered with the patients’ performance, (4) the pain score measured on a visual analog scale (VAS) was less than 1 or more than 8, (5) the patient was injected with analgesics or anti-inflammatory drugs throughout the last 12 weeks, and (6) the medications of cartilage repair or maintenance should have been stopped during the last six months but was still taken.

2.4 Randomization and allocation

All participants were randomized and assigned into one of two groups: the study group and the control group. Randomization was conducted using a hidden computer-sequential list of recruited participants. Each participant was assigned a number that was sealed in envelopes. Patients’ dropouts and withdrawals were shown in Fig. 1.

2.4.1 Study plan

All patients were measured for variables of interest at baseline (pre) and immediately after the end of 6 weeks of treatment (post). Unilateral or bilateral knees were analyzed if the knee scored grade 2 or 3 on the Kellgren-Lawrence scale. Those variables of interest were maximum voluntary isometric contraction (MVIC), joint space narrowing (OARSI JSN), medial joint space width (mJSW), and physical abilities measured in Western Ontario and McMaster Universities Osteoarthritis Index (WOMAC). The concentric isokinetic training and hamstring static stretching were applied to the study group, while patients in the control group received concentric isokinetic training only.

2.5 Assessment procedures

Outcome measures were examined at the baseline and after the end of treatment as follow:

2.5.1 Radiographic outcomes

A standard fluoroscopic x-ray beam was used in screening each patient. A bilateral weight-bearing of semi-flexed knee position was used to assess the posteroanterior view of the tibiofemoral compartment of the knee joint. The radiologist who shared in the current study conducted the screening of the knee joint by using a metacarpophalangeal (MTP) knee view. The patient stood with a slight feet-external rotation at 15 ${}^{\circ}$ from the midline sagittal axis. The 1st MTP of each foot was aligned with the tip of the front 17 $\times$ 14-inch film cassette. The central ray of the x-ray beam, which was directed from the x-ray tube, was parallel to the ground and perpendicular to the film cassette. The knees of the patients were positioned (semi-flexion) from 5 ${}^{\circ}$ to 10 ${}^{\circ}$ till the anterior aspect of the knee touched the middle of the film cassette. The contour of each foot was printed to ensure the accurate repetition of procedures during the post-treatment test [19].

These behavioral variables were considered secondary outcomes, given the treatment asymmetry (stretching only applied to the treatment group). The radiological domains were as follows:

2.5.2 Joint space narrowing (OARSI JSN)

The severity and degree of JSN were rated autonomously by 2 radiologists, who did not participate in the study, blinded to both the patient’s radiographic film and the treatment group. Grades from 0 to 3 were available. A rate that gained the agreement of the two readers was analyzed. A third radiologist was also consulted if there was a contradiction between the two readers [20, 21].

2.5.3 Medial joint space width (mJSW)

A digitalized caliper was used to estimate mJSW (mm) of the medial tibiofemoral compartment. The radiologist used calipers for manual measurement. The interbone length was measured between the caliper points on the radiograph [19].

2.5.4 Physical abilities

A WOMAC questionnaire examined the functional abilities, including the three domains of pain, stiffness, and physical function, by answering five, two, and seventeen questions, respectively. Each question was rated from 0 to 4; higher scores meant worsening of symptoms. Available high score for each subscale is 20, 8, and 68, respectively. Finally, a global score was gained by addition of all three subscales [22].

2.5.5 Active knee extension test (AKEt)

The AKEt comprehensively measured the hamstring flexibility before and after 6 weeks of intervention. The test was conducted at a temperature of 23 ${}^{\circ}$ C in a laboratory setting. The knee angle was calculated using a manual goniometer with a long arm. The patient was laid in a supine posture with a 90 ${}^{\circ}$ hip flexion, a horizontal tibia, and a neutral angle joint. A strap was used to secure the contralateral lower limb to the table. Verbal directions for this position was given: “While maintaining contact with the grip on the box, attempt to straighten the knee as much as you can.” The angle of the knee joint was measured when the participant reached maximum knee extension. The test scores were taken twice, each with a one-minute break in between. The mean values were applied for statistical analysis [23].

2.5.6 Strength of quadriceps muscle

The maximum voluntary isometric contraction (MVIC) in N.m is considered a valid measure for muscle strength. The MVIC of the quadriceps muscle was measured at 60 ${}^{\circ}$ knee flexion using an isokinetic dynamometer (CSMI Humac 2009, Cybex II, II $+$ , version 129, USA). The patient performed three continuous, maximal isometric contractions. Each contraction remained for 2 seconds with a one-minute rest-pause between the contractions. The mean of 3 maximal quadriceps contraction moments was than analyzed [24].

2.6 Treatment procedures

2.6.1 Quadriceps strength training

The patient strengthened the quadriceps muscle by using an isokinetic dynamometer (CSMI Humac 2009, Cybex II, II $+$ , version 129, USA) to increase the power of the quadriceps muscle by concentric isokinetic training. Treatment consisted of five repetitions of concentric isokinetic contraction for one set at the first session. The patient proceeded to perform sessions until he or she reached 12 sets of five repetitions at the last session [25]. Patients were gradually trained from lower velocity (60 ${}^{\circ}$ /s) in the first half of the sessions to higher velocity (180 ${}^{\circ}$ /s) for the rest of the sessions. Eighteen sessions of concentric isokinetic training (3 sessions per week) from flexion to extension direction with maximal effort of the targeted knee were conducted in the study group as well as the control group.

2.6.2 Static stretching of hamstring

The participants laid supine with 90 ${}^{\circ}$ hip flexion, followed by the therapist straightening the patient’s knee passively until a feel of stretching sensation without pain was perceived. That position was then held for 30 seconds. The entire procedure was repeated three times with 10-second intervals in between. The static stretching was applied three days per week for six weeks in the study group only [26].

2.7 Sample size calculation

The sample size was estimated using effect size ( $d=$ 0.20) and a probability of 0.05 with the operation of G*power 3.0.10 software (University of Dusseldorf, Dusseldorf, Germany). For rejecting the null hypothesis, the power of analysis was set at 80%, and 36 patients were recruited. We raised the sample size to 42 patients, anticipating the withdrawals or dropouts of about 20% of the patients.

2.8 Statistical analysis

All statistical analyses were carried out through the SPSS software package version 23. Mean and standard deviation described the variables of interest: OARSI JSN, mJSW, MVIC, AKE, and WOMAC. The Shapiro-Wilk test ensured the normality of data. Independent $t$ -test, Mann-Whitney U test, and chi-square test were used to confirm the homogeneity of basic characteristics of parametric, nonparametric, and categorical data, respectively, between the two groups. A two-way repeated-measures ANOVA (2 $\times$ 2, group x time, repeated measures) was used to explore the differences before and after treatment in variables of interest between the experimental and the control groups. A paired-samples $t$ -test was utilized to ascertain within-group changes across Group x Time if a significant interaction was presented. Pearson correlation coefficient determined the strength and direction of the relationship between AKE, mJSW, and WOMAC scores. The adjusted p value was set at $P<$ 0.008.

3. Results

3.1 Basic and demographic characteristics

Thirty-nine patients were analyzed; however, a total of 67 knees were investigated (study group: 31 knees; control group: 36 knees). The basic and demographic characteristics revealed homogeneity between the two groups since there were no significant differences (Table 1).

Table 1
Basic and demographic characteristics of two groups

	Study group ( $n=$ 19)	Control group ( $n=$ 20)	$p$
Mean $\pm$ SD (CI 95%)
Age, years ${}^{\ast}$	59.15 $\pm$ 4.66 (56.90–61.40)	57.65 $\pm$ 4.13 (55.41–59.31)	0.292
Height, cm ${}^{\ast}$	173.84 $\pm$ 5.06 (171.39–176.28)	174.65 $\pm$ 5.52 (171.70–177.03)	0.638
Weight, Kg ${}^{\ast}$	78.78 $\pm$ 4.03 (76.84–80.73)	79.65 $\pm$ 4.95 (77.42–82.25)	0.557
BMI, (Kg/m ${}^{2}$ ) ${}^{\ast}$	27.30 $\pm$ 0.62 (26.99–27.60)	27.17 $\pm$ 0.77 (26.15–27.53)	0.569
Median (Q1–Q3)
Severity of knee O.A, (K/L) grade ${}^{{\dagger}}$	2 (2–3)	2 (2–3)	0.916
Duration of symptoms, weeks ${}^{{\dagger}}$	30 (24–40)	36 (30–41)	0.363
Q angle, ( ${}^{0}$ ) ${}^{{\dagger}}$	17.5 (15.5–18.75)	18.5 (15.5–20)	0.427
No. (%)
Gender ${}^{{\ddagger}}$
Male	13 (68.4%)	11 (55%)	0.389
Female	6 (31.6%)	9 (45%)
Physical activity ${}^{{\ddagger}}$
Leisure	7 (36.8%)	8 (40%)	0.810
Occupation	10 (52.6%)	11 (55%)
Transport	2 (10.5%)	1 (5%)
Distribution of unilateral/bilateral knee O.A ${}^{{\ddagger}}$
Unilateral	12 (63.2%)	16 (80%)	0.243
Bilateral	7 (36.8)	4 (20%)

BMI: Body mass index; CI: Confidence interval; Q1: $25^{\text{th}}$ quartile; Q3: $75^{\text{th}}$ quartile; K/L: Kellgren-Lawrence scale; O.A: Osteoarthritis; ${}^{\ast}$ : Nonsignificant difference between groups (Independent samples $t$ -test); ${}^{{\dagger}}$ : Nonsignificant difference between groups (Mann-Whitney U test); ${}^{{\ddagger}}$ : Nonsignificant difference between groups (Chi-Square test).

Table 2

Differences of radiological and clinical outcomes between the two groups

	Study group ( $n=$ 19, 31 knees) Mean $\pm$ SD (CI 95%)		Control group ( $n=$ 20, 36 knees) Mean $\pm$ SD (CI 95%)		Group x time interaction
	Pre	Post	Pre	Post	$P$	$\eta^{2}_{\text{partial}}$
Medial JSW, mm	3.29 $\pm$ 0.30 (3.18–3.40)	4.42 $\pm$ 0.23 ${}^{{\ddagger}}$ (4.33–4.51)	3.35 $\pm$ 0.32 (3.24–3.49)	3.47 $\pm$ 0.27 ${}^{{\dagger}{\dagger}}$ (3.37–3.56)	$<$ 0.001 ${}^{*}$	0.644
OARSI JSN, median (Q1–Q3)	3 (2–3)	2 (2–2.5) ${}^{{\dagger}}$	2 (2–3)	2 (2–3) ${}^{{\dagger}{\dagger}}$	0.261 ${}^{{\dagger}{\dagger}}$	–
MVIC, (N.m)	77.76 $\pm$ 6.29 (75.45–80.07)	119.91 $\pm$ 9.85 ${}^{{\ddagger}}$ (116.29–123.52)	79.90 $\pm$ 6.13 (78.90–83)	101.41 $\pm$ 10.33 (96.58–104.12)	$<$ 0.001 ${}^{*}$	0.383
AKEt, ( ${}^{0}$ )	23.96 $\pm$ 3.53 (22.67–25.26)	36.83 $\pm$ 3.99 ${}^{{\ddagger}}$ (35.37–38.30)	25.11 $\pm$ 3.61 (23.8–26.58)	25.58 $\pm$ 3.17 ${}^{{\dagger}{\dagger}}$ (24.50–26.65)	$<$ 0.001 ${}^{*}$	0.571
WOMAC
Pain domain (0–20)	13.03 $\pm$ 2.79 (12–14.05)	6.93 $\pm$ 2.26 ${}^{{\ddagger}}$ (6.1–7.76)	13.75 $\pm$ 2.23 (13.05–14.68)	9.88 $\pm$ 1.92 (9.08–10.53)	0.001 ${}^{*}$	0.171
Stiffness domain (0–8)	5.51 $\pm$ 1.36 (5.01–6.01)	3.64 $\pm$ 0.95 ${}^{{\ddagger}}$ (3.29–3.99)	5.72 $\pm$ 1.11 (5.22–6.06)	4.75 $\pm$ 1.33 (4.30–5.31)	0.024 ${}^{*}$	0.076
Physical function domain (0–68)	36.8 $\pm$ 7.65 (33.99–39.61)	21.67 $\pm$ 4.42 ${}^{{\ddagger}}$ (20.05–23.29)	38.16 $\pm$ 7.39 (35.57–41.19)	29.02 $\pm$ 6.12 (26.36–30.92)	$<$ 0.001 ${}^{*}$	0.229
Total score (0–96)	55.35 $\pm$ 8.32 (52.30–58.40)	32.25 $\pm$ 5.57 ${}^{{\ddagger}}$ (30.21–34.30)	57.51 $\pm$ 7.51 (55.07–60.72)	43.66 $\pm$ 6.24 (40.91–45.59)	$<$ 0.001 ${}^{*}$	0.354

JSW: Joint space width; AKEt: Active knee extension test; WOMAC: Western Ontario and McMaster Universities Osteoarthritis; JSN: Joint space narrowing; MVIC: Maximum voluntary isometric contraction; CI: Confidence interval; $\eta^{2}_{\text{Partial}}$ : Effect size of the difference; ${}^{*}$ : Changes from pre- to post-treatment among study and control groups are significant at $P<$ 0.05; ${}^{{\ddagger}}$ : Significant changes of post-tests between the two groups; ${}^{{\dagger}}$ : Significant changes within-group; ${}^{{\dagger}{\dagger}}$ : Non-significant changes within-group.

Differences of radiological and clinical measures from pre- to post-treatment between the study and control groups are depicted in Table 2. There was a significant interaction in mJSW (F [1, 65] $=$ 117.34, mean square $=$ 8.34, $p<$ 0.001, $\eta^{2}$ $=$ 0.64) and for MVIC of quadriceps (F [1, 65] $=$ 40.29, mean square $=$ 3546, $p<$ 0.001, $\eta^{2}$ $=$ 0.383), as shown in Table 2. The mJSW improved significantly in the study group from pre- to post-treatment ( $p<$ 0.001) but not in the control group ( $p=$ 0.07); whereas the MVIC of quadriceps improved significantly in both groups pre- to post treatment ( $p<$ 0.001). Additionally, a significant interaction was found between the time and group on the hamstring flexibility measured in the AKE test (F [1, 65] $=$ 86.49, mean square $=$ 853.11, $p<$ 0.001, $\eta^{2}$ $=$ 0.571). Patients in the study group showed significant improvement in AKEt between pre- to post treatment ( $p<$ 0.001) than the control group ( $p=$ 0.20).

Figure 2.

Relationship between active knee extension test scores (AKEt) and medial joint space width (mJSW).

Figure 3.

Relationship between active knee extension test scores (AKEt) and total score of WOMAC.

There was a significant interaction in the total score of WOMAC as F (1, 65) $=$ 35.66, mean square $=$ 693.4, $p<$ 0.001, $\eta^{2}$ $=$ 0.354. The total score of WOMAC was improved significantly in both groups but in favor of the study group (32.25 $\pm$ 5.57, $p<$ 0.001) over the control group (43.66 $\pm$ 6.24, $p<$ 0.001), as shown in Table 2. The main effects of time and group in the global score of WOMAC were statistically found ( $p<$ 0.001).

A Wilcoxon signed-rank test investigated the difference of medians in the OARSI JSN scores and revealed that the sum of ranks between pre- to post-treatment in each group was statistically significant (study group: sum of ranks $=$ 105, $p<$ 0.001; control group: sum of ranks $=$ 10, $p=$ 0.046). However, when comparing the scores of OARSI JSN after treatment intervention (post-test scores) between the two groups, the Mann-Whitney test reported no statistical difference between study and control groups ( $p=$ 0.261), as shown in Table 2.

A Pearson correlation coefficient was conducted to investigate the relationship between the AKEt scores and mJSW and WOMAC total score in the study group, as illustrated in Figs 2 and 3. There was a strong positive relationship between AKEt scores and mJSW ( $r=$ 0.63, $p<$ 0.001), but there was a moderately negative association between AKEt and total scores of the WOMAC questionnaire ( $r=-$ 0.37, $p=$ 0.041).

4. Discussion

To our knowledge, this study was the first to examine the effect of adding hamstring stretching to quadriceps strengthening on the mJSW, OARSI JSN, and functional abilities in osteoarthritis patients. It is well-known that strengthening thigh muscles provides a considerable effect on attenuating risk factors for KOA. Andriacchi et al. mentioned in their study that one of the quadriceps’ roles is to protect the articular surface of the knee joint from excessive loads. Authors have mentioned quadriceps weakness as one of the main causes of degeneration in the knee joint [27].

However, the novelty and importance of this study lay in exploring and clarifying the effect of adding hamstring stretching to a strengthening program for treating KOA. We hypothesized that increased hamstring flexibility plays an important role in improving the joint space, enhancing functional abilities, and decreasing pain level.

Our results showed that the effects of hamstring stretching applied with concentric strengthening exercises of the quadriceps muscle improved the joint space as measured in mJSW. To be noted, the mJSW is the length measurement between of highest point of the femoral condyle and the hindmost point of the tibia [28]. Moreover, there was a strong correlation ( $p<$ 0.001) between the AKEt and the mJSW in the study group. The joint space was increased significantly in the study group (34.3%) while no significant change was observed in the control group (3.5%). Patients in the study group showed more significant improvement in OARSI JSN ( $p<$ 0.001) than patients in the control group ( $p=$ 0.046). Thus, adding hamstring stretching to quadriceps strengthening program had an obvious effect on improving the mJSW and OARSI JSN of knee osteoarthritis patients in the study group, more so than the control group in which only the quadriceps strengthening exercise was applied.

Our speculation for that big discrepancy of improvement in mJSW and OARSI JSN between the control group and the study group lay in the lack of hamstring flexibility within the control group, which increased the knee joint compressive load. It was stated that a less flexible hamstring in such patients pulls the pelvis posteriorly and decreases the lordotic curve of the lumbar spine. As a form of compensation, the quadriceps is probably activated intensely to overcome the reduced hamstring flexibility, consequently applies more compressive loads on the knee joint components [29]. Park and Jung reported a significant improvement in pelvic displacement especially the anterior pelvic tilt after the hamstring stretching [30]. To sum up, the decreased anterior pelvic tilt, leading to stretching, hence increased force of the rectus femoris [31]. This mechanical hypothesis supports our finding that the patients in the control groups did not improve in quadriceps strength like the treatment group.

Furthermore, it is well-known that increased knee stiffness is due to increased tightness of the muscles surrounding the knee, including the hamstring, which operates by decreasing the anterior tibial translation and is accompanied by increased knee joint compressive load, which may protect the anterior cruciate ligament (ACL) [32].

So, increasing the hamstring flexibility in the study group and based on the aforementioned explanations should decrease the knee joint compressive load on the knee joint, which should improve the mJSW and score of OARSI JSN. Meanwhile, it was mentioned in a previous study that stretching exercises for the hamstring do not impose any danger to the ACL, which agrees with our findings in the current study [33]. For these reasons, stretching the hamstring might explain the significantly noticeable improvement of mJSW and OARSI JSN in the study group compared to that of the control group.

Rehabilitation programs for decreasing the knee joint compressive forces in KOA always include strengthening exercises to attenuate the compressive load, which could occur at the tibiofemoral joint. However, a previous study reported that the high-intensity strength exercise for the quadriceps did not significantly reduce the knee joint compressive forces after 18 months compared to other kinds of strength training exercises [34]. This result predicted our findings that the mJSW in the control group did not change significantly after quadriceps strengthening training only.

The addition of hamstring stretching exercise to the quadriceps strength program in the present study which yielded increased strength of quadriceps muscle in the study group compared with that of the control group (119.91 N.m; $+$ 54%, 101.41 N.m; $+$ 26.9%, respectively) provided an added clinical value for osteoarthritis patients. This result might be attributed to the enhancement of biomechanics of the knee joint after hamstring stretching. Hanada et al. stated that patients with KOA exhibit reduced screw-home mechanism and abnormality of external leg rotation during knee extension [35]. Therefore, increasing the flexibility of the hamstring muscles would be an effective tool to restore the proper biomechanical alignment of leg rotation in a well-designed therapeutic regimen aiming to improve the strength of knee extensors in knee osteoarthritis patients [36]. Also, Sandberg et al. reported a marked increase in knee extension strength after static stretching of the hamstring muscles [37].

It was observed that with the decrease in quadriceps strength came an increase in knee pain [38] and in difficulty of stair-climbing activities [39]. Hence, increasing the strength of the quadriceps muscle will lead to a significant reduction of knee pain for KOA patients. Additionally, hamstring stretching seems to induce an increase in the strength of the quadriceps muscle. A previous study confirmed that the improvement of knee extension range of motion due to stretching exercises was likewise accompanied by enhanced quadriceps peak torque (49%) at the end-range of knee extension [40]. Moreover, Lee et al. stated that the dynamic stretching of the hamstring muscle improved the quadriceps strength by $+$ 78.43% and decreased the quadriceps activation time by $-$ 39.7%. While the static stretching of the hamstring muscle promoted only the quadriceps strength by $+$ 61.9% in patients with patellofemoral pain syndrome with hamstrings tightness [41]. Also, a previous study revealed that the EMG activities of the rectus femoris muscle increased significantly during the 2nd and 3rd sets of barbell squats after the hamstring stretching [42].

The results of the present study showed a significant alleviation of the pain in the study group (6.93 $\pm$ 2.26, $+$ 46.81%) compared to the control group (9.88 $\pm$ 1.92, $+$ 28.14%). This pain reduction might be attributed to the increased quadriceps strength in both groups, but it favored the study group for its concurrent application of hamstring stretching exercises (MVIC of the study group: $\uparrow$ 54.2%, MVIC of the control group: $\uparrow$ 26.9%). A previous study reported that quadriceps strength training improved the pain level in knee osteoarthritis significantly ( $p<$ 0.001) [43]. Hence, quadriceps strength is very essential for controlling pain levels in arthritic cases such as tibiofemoral and patellofemoral osteoarthritis.

Clearly, adding a hamstring stretching program to quadriceps strengthening exercises provided significant benefits in decreasing knee pain. It could be attributed to enhanced blood perfusion of the muscle, which may consequently decrease pain level. In a previous study, Caliskan et al. examined the acute effects of 30-second static stretching of the rectus femoris muscle applied for a total of either 2 or 5 minutes. The results of that study revealed that both stretching durations induced vascular changes, and the blood flow increased significantly [44]. The stretching exercise improves vascular dilatation [45] by washing out substance P, which leads to a decrease in the pain level [46], improvement of knee range of movement [47], and physical performance [48].

In line with our results, a previous study suggested that the presence of functional limitations caused by hamstring tightness in patients with KOA could be treated by a flexibility exercise [14]. The results of the current study showed a significant improvement in functional abilities in the study group compared to the control group as the total WOMAC scores improved significantly (by 53.7%) in the study group. The study group also showed a moderately significant relationship ( $p=$ 0.04) between the AKEt and the WOMAC scale. This improvement of functional abilities in the study group of the current study occurred after the application of static stretching of the hamstring muscles. This agrees with a study conducted by Cronin et al. who investigated the effects of stretching and vibration of the hamstring or a combination of both on dynamic knee range of motion after a single session. Their study reported that hamstring stretching induced a small, temporary change in dynamic knee range of motion [49]. However, in the present study, we applied hamstring stretching three times per week for six weeks as this period of time promoted changes in hamstring flexibility and improved the knee range of motion and the patient’s functional abilities.

The slight improvement of functional abilities measured in WOMAC and OARSI JSN in the control group could be attributed to the increased strength of quadriceps muscle. This is consistent with an earlier study that reported the increase of quadriceps strength resulting in decrease of the knee pain, which in turn led to improvement of the knee joint flexibility and, subsequently the achievement of a good level of physical activities [50].

4.1 Limitations

The study was limited to factors which could be controlled to enhance the generalization. First, the study was conducted with only grades 2 and 3 of the Kellgren-Lawrence scale for KOA; the effect of hamstring stretching on grade 4, i.e., more severe cases of knee osteoarthritis, may be different. Second, the study is limited to investigating only the static stretching of the hamstring. There are other techniques of stretching such as dynamic, PNF, and ballistic hamstring stretching which should be examined before the generalization of results. Third, the treatments were unbalanced between groups (quadriceps strengthening, only in the control groups) so that clinical, patient-centered outcomes, with particular reference to pain reports, could be biased in favor of the stretching group. Fourth, the study lacks follow-up, so it cannot give an accurate picture of the long-lasting effects of applying hamstring stretching on radiological and clinical measures in KOA.

5. Conclusion

Based on our results, static stretching of the hamstring alongside quadriceps strengthening added clinical value in improving mJSW, JSN, and functional abilities of osteoarthritis patients. This paper recommends the inclusion of static stretching of hamstring muscles in therapeutic programs for KOA treatment.

Author contributions

CONCEPTION: Waleed S. Mahmoud and Ahmed Osailan.

PERFORMANCE OF WORK: Waleed S. Mahmoud, Ahmed Osailan and Ragab K. Elnaggar.

INTERPRETATION OR ANALYSIS OF DATA: Waleed S. Mahmoud, Ahmed Osailan, Ragab K. Elnaggar and Ali B Alhailiy.

PREPARATION OF THE MANUSCRIPT: Waleed S. Mahmoud, Ahmed Osailan and Ragab K. Elnaggar.

REVISION FOR IMPORTANT INTELLECTUAL CONTENT: Ragab K. Elnaggar and Ali B Alhailiy.

Ethical considerations

All patients assigned and completed a given consent form, ensuring the acceptance of participation. The ethical approval number of the study was registered and granted from the ethical research committee (No. RHPT 022018) of the Physical Therapy and Health Rehabilitation Department. All procedures tracked instructions defined and expressed by the (Declaration of Helsinki, 1964).

Funding

The authors are grateful to the Deanship of scientific research at Prince Sattam Bin Abdulaziz University, Saudi Arabia, for financial support to accomplish this work. Project No. 2021/03/18445.

Footnotes

Acknowledgments

The authors are thankful to the Deanship of scientific research at Prince Sattam Bin Abdulaziz University, Saudi Arabia, for completing this work.

Conflict of interest

All authors state that they have no conflicts of interest.

References

Cunha

Barbosa

Castro

PAT de S

Luiz

BLF

Silva

ACA

Russo

, et al. Knee osteoarthritis induces atrophy and neuromuscular junction remodeling in the quadriceps and tibialis anterior muscles of rats. Sci Rep [Internet]. 2019 Dec 24; 9(1): 6366. Available from: http://www.nature.com/articles/s41598-019-42546-7.

Purba

TSP

Moeliono

Sastradimadja

. Effect of quadriceps muscle strengthening exercise on quadriceps and hamstring muscle strength ratio in patients with osteoarthritis grade 2 and 3. Int J Integr Heal Sci. 2017; 5(2): 64-9.

Alkhawajah

Alshami

. The effect of mobilization with movement on pain and function in patients with knee osteoarthritis: A randomized double-blind controlled trial. BMC Musculoskelet Disord. 2019; 20(1): 1-9.

Chan

Huang

Hsu

Chang

. Radiographic joint space narrowing in osteoarthritis of the knee: Relationship to meniscal tears and duration of pain. Skeletal Radiol. 2008; 37(10): 917-22.

Jefferson

Collins

Whittle

Radin

O’Connor

. The role of the quadriceps in controlling impulsive forces around heel strike. Proc Inst Mech Eng Part H, J Eng Med. 1990; 204(1): 21-8.

Radin

Burr

Caterson

Fyhrie

Brown

Boyd

. Mechanical determinants of osteoarthrosis. Semin Arthritis Rheum. 1991 Dec; 21(3 Suppl 2): 12-21.

Segal

Glass

Torner

Yang

Felson

Sharma

, et al. Quadriceps weakness predicts risk for knee joint space narrowing in women in the MOST cohort. Osteoarthr Cartil. 2010 Jun; 18(6): 769-75.

Culvenor

Segal

Guermazi

Roemer

Felson

Nevitt

, et al. Sex-specific influence of quadriceps weakness on worsening patellofemoral and tibiofemoral cartilage damage: A prospective cohort study. Arthritis Care Res. 2019; 71(10): 1360-5.

Amin

Baker

Niu

Clancy

Goggins

Guermazi

, et al. Quadriceps strength and the risk of cartilage loss and symptom progression in knee osteoarthritis. Arthritis Rheum. 2009; 60(1): 189-98.

10.

Cho

Kwon

Lee

Park

Yang

Lee

. The effect of hamstring tightness on intraoperative extension gap in posterior stabilized total knee arthroplasty. Sci Rep [Internet]. 2021; 11(1): 1-8. Available from: doi: 10.1038/s41598-021-83221-0.

11.

Shoukat

Arshad

Sharif

Fatima

Shoukat

. Effects of different stretching times on range of motion in patients with hamstring tightness: A randomised control trial. Ann King Edward Med Univ. 2018; 23(4): 554-9.

12.

Onigbinde

. An assessment of hamstring flexibility of subjects with knee osteoarthritis and their age matched control. Clin Med Res. 2013; 2(6): 121.

13.

Shamsi

Mirzaei

Shahsavari

Safari

Saeb

. Modeling the effect of static stretching and strengthening exercise in lengthened position on balance in low back pain subject with shortened hamstring: A randomized controlled clinical trial. BMC Musculoskelet Disord. 2020; 21(1): 1-9.

14.

Sailor

Limbani

Dhola

. Association between hamstring flexibility and functional performance of patients with knee osteoarthritis. J Integr Heal Sci [Internet]. 2020 Nov 4; 8(2): 57. Available from: https://link.gale.com/apps/doc/A648295065/AONE?u=anon∼9649c444&sid=googleScholar&xid=f2236c8b.

15.

Aguiar

Rocha

Rezende

GA da S

Nascimento

MR do

Scalzo

. Effects of resistance training in individuals with knee osteoarthritis. Fisioter em Mov. 2016; 29(3): 589-96.

16.

Kolasinski

Neogi

Hochberg

Oatis

Guyatt

Block

, et al. 2019 american college of rheumatology/arthritis foundation guideline for the management of osteoarthritis of the hand, hip, and knee. Arthritis Rheumatol. 2020; 72(2): 220-33.

17.

Tuna

Çelik

Balcı

. The effect of physical therapy and exercise on pain and functional capacity according to the radiological grade of knee osteoarthritis. J Back Musculoskelet Rehabil [Internet]. 2021 Aug 20; 1-6. Available from: https://www.medra.org/servlet/aliasResolver?alias=iospress&doi=10.3233/BMR-200287.

18.

Sylvia

Bernstein

Hubbard

Keating

Anderson

. Practical guide to measuring physical activity. J Acad Nutr Diet. 2014; 114(2): 199-208.

19.

Mazzuca

Brandt

Buckwalter

. Detection of radiographic joint space narrowing in subjects with knee osteoarthritis: Longitudinal comparison of the metatarsophalangeal and semiflexed anteroposterior views. Arthritis Rheum. 2003; 48(2): 385-90.

20.

Mikesky

Mazzuca

Brandt

Perkins

Damush

Lane

. Effects of strength training on the incidence and progression of knee osteoarthritis. Arthritis Care Res. 2006; 55(5): 690-9.

21.

Sheehy

Culham

McLean

Niu

Lynch

Segal

, et al. Validity and sensitivity to change of three scales for the radiographic assessment of knee osteoarthritis using images from the Multicenter Osteoarthritis Study (MOST). Osteoarthr Cartil [Internet]. 2015; 23(9): 1491-8. Available from: doi: 10.1016/j.joca.2015.05.003.

22.

McConnell

Kolopack

Davis

. The Western Ontario and McMaster Universities Osteoarthritis Index (WOMAC): A review of its utility and measurement properties. Arthritis Care Res Off J Am Coll Rheumatol. 2001; 45(5): 453-61.

23.

Espejo-Antúnez

López-Miñarro

Garrido-Ardila

Castillo-Lozano

Domínguez-Vera

Maya-Martín

, et al. A comparison of acute effects between Kinesio tape and electrical muscle elongation in hamstring extensibility. J Back Musculoskelet Rehabil. 2015; 28(1): 93-100.

24.

Mahmoud

Osailan

Ahmed

Elnaggar

Radwan

. Optimal parameters of blood flow restriction and resistance training on quadriceps strength and cross-sectional area and pain in knee osteoarthritis. Isokinet Exerc Sci. 2021; 29(4): 393-402.

25.

Jegu

Pereira

Andant

Coudeyre

. Effect of eccentric isokinetic strengthening in the rehabilitation of patients with knee osteoarthritis: Isogo, a randomized trial. Trials. 2014; 15(1): 1-6.

26.

Meena

Shanthi

Madhavi

. Effectiveness of pnf stretching versus static stretching on pain and hamstring flexibility following moist heat in individuals with knee osteoarthritis. Int J Physiother. 2016; 3(5): 529-34.

27.

Andriacchi

Mündermann

Smith

Alexander

Dyrby

Koo

. A framework for the in vivo pathomechanics of osteoarthritis at the knee. Ann Biomed Eng. 2004 Mar; 32(3): 447-57.

28.

Kan

Arai

Kobayashi

Nakagawa

Inoue

Hino

, et al. Radiographic measurement of joint space width using the fixed flexion view in 1,102 knees of japanese patients with osteoarthritis in comparison with the standing extended view. Knee Surg Relat Res. 2017; 29(1): 63-8.

29.

Davis Hammonds

Laudner

McCaw

McLoda

. Acute lower extremity running kinematics after a hamstring stretch. J Athl Train. 2012; 47(1): 5-14.

30.

Park

Jung

. Effects of hamstring self-stretches on pelvic mobility in persons with low back pain. Phys Ther Rehabil Sci. 2020; 9(3): 140-8.

31.

Neumann

. Kinesiology of the hip: A focus on muscular actions. J Orthop Sports Phys Ther. 2010; 40(2): 82-94.

32.

Fleming

Ohlén

Renström

Peura

Beynnon

Badger

. The effects of compressive load and knee joint torque on peak anterior cruciate ligament strains. Am J Sports Med. 2003; 31(5): 701-7.

33.

Ruan

Zhang

. Acute effects of static stretching of hamstring on performance and anterior cruciate ligament injury risk during stop-jump and cutting tasks in female athletes. J strength Cond Res. 2017; 31(5): 1241.

34.

Messier

Mihalko

Beavers

Nicklas

Devita

Carr

, et al. Effect of high-intensity strength training on knee pain and knee joint compressive forces among adults with knee osteoarthritis: The START randomized clinical trial. JAMA – J Am Med Assoc. 2021; 325(7): 646-57.

35.

Hanada

Hara

Hirakawa

Hoshi

Ito

Gamada

. Immediate effects of leg-press exercises with tibial internal rotation on individuals with medial knee osteoarthritis. Physiother Res Int. 2018; 23(4): 1-6.

36.

Kimura

. The effects of hamstring stretching on leg rotation during knee extension. J Phys Ther Sci. 2013; 25(6): 697-703.

37.

Sandberg

Wagner

Willardson

Smith

. Acute effects of antagonist stretching on jump height, torque, and electromyography of agonist musculature. J Strength Cond Res. 2012; 26(5): 1249-56.

38.

O’Reilly

Jones

Muir

Doherty

. Quadriceps weakness in knee osteoarthritis: The effect on pain and disability. Ann Rheum Dis. 1998; 57(10): 588-94.

39.

Casaña

Calatayud

Silvestre

Sánchez-Frutos

Andersen

Jakobsen

, et al. Knee extensor muscle strength is more important than postural balance for stair-climbing ability in elderly patients with severe knee osteoarthritis. Int J Environ Res Public Health [Internet]. 2021 Mar 31; 18(7): 3637. Available from: https://www.mdpi.com/1660-4601/18/7/3637.

40.

Reid

D MP

. Effects of a six week lower limb stretching programme on range of motion, peak passive torque and stiffness in people with and without osteoarthritis of the knee. New Zeal J Physiother. 2011; 39(1): 2-9.

41.

Lee

Jang

K-M

Kim

Rhim

Kim

H-D

. Effects of static and dynamic stretching with strengthening exercises in patients with patellofemoral pain who have inflexible hamstrings: A randomized controlled trial. Sports Health [Internet]. 2020/08/13. 2021; 13(1): 49-56. Available from: https://pubmed.ncbi.nlm.nih.gov/32790575.

42.

Trindade

Neto

Pita

JCN

Tavares

VD de O

Dantas

PMS

Schoenfeld

, et al. Pre-stretching of the hamstrings before squatting acutely increases biceps femoris thickness without impairing exercise performance. Front Physiol. 2020; 11(July): 1-9.

43.

Bokaeian

Bakhtiary

Mirmohammadkhani

Moghimi

. Quadriceps strengthening exercises may not change pain and function in knee osteoarthritis. J Bodyw Mov Ther. 2018; 22(2): 528-33.

44.

Caliskan

Akkoc

Bayramoglu

Gozubuyuk

Kural

Azamat

, et al. Effects of static stretching duration on muscle stiffness and blood flow in the rectus femoris in adolescents. Med Ultrason. 2019; 21(2): 136-43.

45.

Mahmoud

Samhan

Abd-Elhalim

Mustafa

, Mahmoud. Effect of different time durations of static stretching of the calf muscle on vascular response in popliteal artery. J Am Sci. 2013; 9(5): 369-74.

46.

Gribble

Guskiewicz

Prentice

Shields

. Effects of static and hold-relax stretching on hamstring range of motion using the FlexAbility LE1000. J Sport Rehabil. 1999; 8(3): 195-208.

47.

Reid

McNair

. Passive force, angle, and stiffness changes after stretching of hamstring muscles. Med Sci Sports Exerc. 2004; 36(11): 1944-8.

48.

Bassett

Howley

. Limiting factors for maximum oxygen uptake and determinants of endurance performance. Med Sci Sports Exerc. 2000; 32(1): 70-84.

49.

Cronin

Nash

Whatman

. The acute effects of hamstring stretching and vibration on dynamic knee joint range of motion and jump performance. Phys Ther Sport Off J Assoc Chart Physiother Sport Med. 2008 May; 9(2): 89-96.

50.

Onigbinde

Ojoawo

Talabi

Adedoyin

Onifade

Olaitan

, et al. Effects of glucosamine sulphate iontophoresis on hamstring flexibility of subjects with knee osteoarthritis. Med Sport. 2010; 4(3): 1405-10.

Radiological and clinical outcomes of concurrent hamstring stretching with quadriceps strengthening in patients with knee osteoarthritis: A randomized clinical trial

Abstract

BACKGROUND:

PURPOSE:

METHODS:

RESULTS:

CONCLUSION:

Keywords

1. Introduction

2. Methods

2.1 Subjects

2.3 Exclusion criteria

2.4 Randomization and allocation

2.4.1 Study plan

2.5 Assessment procedures

2.5.1 Radiographic outcomes

2.5.2 Joint space narrowing (OARSI JSN)

2.5.3 Medial joint space width (mJSW)

2.5.4 Physical abilities

2.5.5 Active knee extension test (AKEt)

2.5.6 Strength of quadriceps muscle

2.6 Treatment procedures

2.6.1 Quadriceps strength training

2.6.2 Static stretching of hamstring

2.7 Sample size calculation

2.8 Statistical analysis

3. Results

3.1 Basic and demographic characteristics

Table 1 Basic and demographic characteristics of two groups

4.1 Limitations

5. Conclusion

Author contributions

Ethical considerations

Funding

Footnotes

Acknowledgments

Conflict of interest

References

Table 1
Basic and demographic characteristics of two groups