Abstract
Objective:
The objective of this study was to examine the association of quadriceps strength symmetry and surgical status (ACL reconstruction or nonoperative management) with early clinical knee OA 5 years after ACL injury or reconstruction.
Methods:
204/300 athletes were analyzed 5 years after ACL injury or reconstruction (ACLR). Quadriceps strength was measured and reported as a limb symmetry index. We identified participants with early clinical knee OA using criteria that two of four Knee Injury and Osteoarthritis Outcome Score (KOOS) subscales score ≤85% (Luyten et al. 2018). We calculated odds ratios (OR) and 95% confidence intervals (CI) using logistic regression, adjusted for age, sex, meniscal injury, and BMI, to examine the associations between quadriceps strength and surgical status with clinical knee OA.
Results:
21% of participants met KOOS criteria for clinical knee OA (Luyten et al. 2018). For every 1% increase in quadriceps limb symmetry index, there was 4% lower odds of clinical OA (adjusted OR 0.96, 95% CI 0.93–0.99) at 5 years. Surgical status was not associated with clinical knee OA (adjusted OR 0.58, 95% CI 0.23, 1.50).
Conclusions:
More symmetrical quadriceps strength, but not surgical status, 5 years after ACL injury or reconstruction was associated with lower odds of clinical knee OA.
Introduction
After anterior cruciate ligament (ACL) rupture, the chances of developing knee osteoarthritis (OA) increase rapidly. Patients after ACL rupture have a 60 to 90% chance of developing knee OA, with approximately 50% of individuals developing OA within 5–10 years of ACL reconstruction (ACLR). (1,2) Post-traumatic knee OA (PTOA), which may develop after a joint injury, has devastating effects, including lower participation in activity, more pain, and worse self-reported quality of life compared to non-injured individuals. (3) Strategies are needed to identify individuals after ACL rupture who would benefit from targeted intervention to mitigate the disease process before symptoms and joint damage occurs.
OA is traditionally diagnosed radiographically by the presence of osteophytes and the loss of joint space, but we know that the OA disease starts early, long before it is visible on radiographs.(4) Secondary prevention (i.e., implementing interventions after the initiating trauma has occurred) may be the most ideal time to intervene clinically. However, we lack targets for intervention at this level. Secondary prevention depends on the detection and treatment of risk factors for development and progression of OA. The ability to clinically detect early OA prior to widespread joint damage would allow for early clinical intervention and education after ACL rupture. Identifying modifiable risk factors for post-traumatic OA, such as muscle weakness, where we can clinically intervene at an earlier time point may delay OA progression.
Previously identified modifiable factors associated with early development of PTOA after ACL rupture and reconstruction include asymmetrical knee walking mechanics, functional performance and changes in knee joint loading. (5–8) Although quadriceps weakness has not been directly implicated in developing PTOA after ACL rupture, loss of quadriceps strength over time is associated with symptomatic knee OA long term. (9) Furthermore, quadriceps weakness has shown to be associated with an increased risk of developing knee OA. (10) Patients with quadriceps weakness also show movement asymmetries at the knee joint and poor functional performance and patient-reported outcomes. (11) Quadriceps weakness contributes to altered walking mechanics early after ACLR. (12) Similarly, quadriceps weakness is associated with radiographic knee OA and lower patient-reported outcomes early after ACLR. (13) After meniscectomy, weaker quadriceps are associated with more severe radiographic OA changes of the operated and contralateral knee at 11 year follow-up. (14)
Quadriceps strength is a critical objective measurement used to make clinical decisions throughout rehabilitation. (15,16) Limb symmetry indexes are often used to express quadriceps strength, and are calculated as the involved limb’s strength value as a percentage of the uninvolved limb value. For safe return to sport and prior activity level, quadriceps strength symmetry is highly recommended to be >90%. (17) Similarly, individuals who present with minimal strength deficits (quadriceps strength symmetry >90%) at the time of return to sport perform similar functionally compared to uninjured individuals. (18) Quadriceps strength may therefore be an important modifiable component of a clinical evaluation to identify individuals at risk for developing PTOA.
Recent criteria, proposed by Luyten et al. (19) after an international workshop and consensus process, were developed to classify early stage OA in a primary care setting. Development of a consensus classification criteria is an important step towards detecting early knee OA, however the validity, sensitivity, and responsiveness of these criteria are not yet known. The classification criteria included: two of the four Knee Injury and Osteoarthritis Outcome score (KOOS) subscales and a clinical examination of joint line tenderness and crepitus in those with no radiographic OA (i.e., Kellgren and Lawrence (KL) grade of 0–1). As a first step towards classifying presence of clinical knee OA, the KOOS component of the Luyten et al. (19) criteria may offer a strategy to monitor patient symptoms remotely, with no procedures such as an office visit, or imaging, required. These clinical criteria have the potential to be used to identify individuals who may be candidates for secondary prevention strategies during rehabilitation after ACL injury as well as during post-operative rehabilitation and may bridge the gap between primary and tertiary levels of prevention.
The purpose of this study was to examine the association of quadriceps strength with presence of early clinical knee OA 5 years after ACL rupture. We hypothesized that more symmetrical quadriceps strength would be associated with lower odds of clinical knee OA. Secondarily, we hypothesized that surgical status was not associated with clinical knee OA.
Patients and Methods
This was a secondary analysis of prospectively collected data from an international cohort study through the University of Delaware (Newark, Delaware, USA) and the Oslo University Hospital (Oslo, Norway). The University of Delaware Institutional Review Board and the Regional Committee for Medical Research Ethics of South-Eastern Norway approved this study. All participants provided written informed consent prior to inclusion.
Only participants between 13 and 60 years old who were regularly (>50 hours per year) involved in level I (e.g., soccer, basketball) or II (e.g., racket sports, baseball) sports (20) at the time of ACL rupture were eligible. Participants were excluded if they had a concomitant grade III ligamentous injury, articular cartilage lesions > 1 cm2, bilateral lower extremity injury (e.g., contralateral ligamentous injury), or an obviously repairable meniscal tear. ACL ruptures were confirmed with magnetic resonance imaging (MRI) and a side-to-side difference of ≥ 3mm measured with a KT-1000 arthrometer (MEDmetric, San Diego, California). The cohort included those who elected either ACLR or rehabilitation alone as management after ACL injury. This decision was made via a shared decision-making process during a period in which the participant performed a prehabilitation program. (21) Those who selected ACL reconstruction had a bone-patellar tendon-bone autograft, single-bundle hamstring autograft, or double-bundle hamstring autograft. For this analysis, we included 204/300 individuals who returned for their 5-year follow-up data collection and had complete data sets including KOOS and bilateral quadriceps strength measures at 5 years (Figure 1).
Figure 1.
Delaware-Oslo ACL Cohort Study Consort Diagram.
Quadriceps Femoris Muscle Strength Testing
Quadriceps femoris muscle strength was measured using an electromechanical dynamometer (Kin-com; DJO Global, Chula Vista, CA, UA or System 3; Biodex, Shirley, NY, USA) during a maximal voluntary isometric contraction (MVIC) knee extension test in Delaware. Participants were seated with their knees and hips flexed to 90 degrees. The dynamometer’s axis of rotation was aligned with the axis of rotation of the knee, and the leg was strapped in at the pelvis, thigh, and shank during testing to minimize accessory motion. Each participant completed 3 submaximal practice trials, and then 3 maximal effort trials for the uninvolved limb, followed by the involved limb. In Oslo, Norway, quadriceps strength was measured with an isokinetic dynamometer (Biodex 6000; Biodex Medical Systems). Participants performed four submaximal practice trials, a 1-minute rest, and then 5 recorded maximal effort repetitions for the uninvolved limb, followed by the involved limb. For the purposes of this study, we defined strength as symmetric peak strength values between limbs. Quadriceps strength was reported as a limb symmetry index (LSI), which was calculated as the involved limb maximum torque divided by the uninvolved limb maximum torque expressed as a percentage.
Knee Injury and Osteoarthritis Outcome Score
The KOOS, a patient-reported outcome of knee pain and function, was administered to all participants. The KOOS is comprised of five subscales (pain, symptoms, activities of daily living, sports and recreation function, and knee-related quality of life). (22) The KOOS subscales scores range from 0 to 100, with 100 indicating no impairment. We applied the patient-reported criteria of the proposed early clinical OA symptoms by Luyten et al. (19) The criteria for early clinical knee OA was defined as ≤ 85% in two of the four KOOS subscales (pain, symptoms, activities of daily living, knee-related quality of life) at the 5 year follow up of the Delaware-Oslo ACL Cohort Study. (19)
Statistical Analyses
Statistical analyses were performed using SAS 9.4 (SAS Institute, Cary, NC, USA). A significance level of p<0.05 was set a priori. Descriptive statistics were calculated to describe the participant demographics. The exposures of interest were quadriceps strength LSI (continuous variable) and surgical status (ACL reconstruction or nonoperative management). For descriptive purposes, we also dichotomized quadriceps strength LSI into symmetric (≥90% LSI) and asymmetric (<90% LSI). The outcome was presence or absence of early clinical knee OA based on the Luyten et al. (19) KOOS criteria (2 of 4 KOOS subscales scoring ≤85%). We calculated odds ratios (OR) and 95% confidence intervals (CI) using logistic regression to examine the association of quadriceps strength symmetry and surgical status with presence of early clinical knee OA 5 years after ACL rupture, adjusting for sex, age, body mass index (BMI), and meniscus injury at baseline.
Results
Of 300 participants who enrolled in the Delaware-Oslo ACL Cohort Study at baseline, 204 (149 ACLR, 55 underwent rehabilitation alone) who returned for the 5-year follow up completed the KOOS questionnaire and quadriceps strength testing (Table 1). Of 204 participants, 21% (41/200) were classified as having early clinical knee OA according to the modified Luyten et al. criteria. (19) Fifty-four percent of participants scored ≤85% on the KOOS knee related quality of life subscale (111/204) (Table 2). Fewer participants had scores ≤85% on the symptoms (38/204) and pain (24/204), or activities of daily living (8/204) subscales.
Table 1.
Participant Demographics (Mean or % (n) ± SD).
| Total Sample | Early OA† | Without Early OA | |
|---|---|---|---|
|
| |||
| n | 204 | 41 | 163 |
|
| |||
| Time since screening, y | 5.5 ± 0.5 | 5.7 ± 0.6 | 5.5 ± 0.5 |
|
| |||
| Age, y | 32.7 ± 10.0 | 32.4 ± 9.8 | 32.6 ± 10.1 |
|
| |||
| Female | 47% (96) | 51% (21) | 47% (76) |
|
| |||
| *Body mass index, kg/m2 | 25.4 ± 4.0 | 25.5 ± 4.6 | 25.5 ± 3.8 |
|
| |||
| * Graft Type | |||
| Nonoperative | 27% (55) | 19% (8) | 29% (47) |
| Allograft | 20% (41) | 27% (11) | 19% (30) |
| BPTB | 15% (30) | 15% (6) | 15% (24) |
| Hamstrings | 38% (76) | 39% (16) | 37% (60) |
|
| |||
| Operative Status | |||
| ACLR | 73% (149) | 80% (33) | 71% (116) |
| Nonoperative rehabilitation | 27% (55) | 20% (8) | 29% (47) |
|
| |||
| Quadriceps strength LSI | 97.3% ± 15.1 | 91.9% ± 15.1% | 97.8% ± 14.8% |
|
| |||
| KOOS | |||
| Pain | 93.8 ± 9.3 | 81.5 ± 11.9 | 97.06 ± 4.8 |
| Symptoms | 89.8 ± 12.6 | 70.8 ± 14.1 | 94.5 ± 5.9 |
| ADL | 97.6 ± 6.2 | 91.6 ± 11.4 | 99.1 ± 1.9 |
| Sports/Recreation | 88.4 ± 16.3 | 69.4 ± 22.7 | 93.3 ± 9.3 |
| QoL | 79.4 ± 19.3 | 57.5 ± 20.1 | 84.9 ± 14.6 |
Abbreviations: SD, standard deviation; OA, osteoarthritis; ACLR, anterior cruciate ligament reconstruction; LSI, limb symmetry index; KOOS, knee injury and osteoarthritis outcome score; ADL, activities of daily living; QoL, quality of life
Early OA as defined by KOOS criteria within Luyten et al. (19)
Body mass index was carried forward from the 2 year follow up for 2 participants; 2 unknown graft types in the group without early OA
Table 2.
Total sample (n) categorized by Luyten et al. (19) criteria application (% n ± SD).
| n (%) | |
|---|---|
|
| |
| KOOS ≤85 | |
| Pain | 24 (12%) |
| Symptoms | 38 (19%) |
| ADL | 8 (4%) |
| QoL | 111 (54%) |
|
| |
| Number of KOOS subscales ≤85 | |
| 0 | 89 (44%) |
| 1 | 74 (36%) |
| 2 | 24 (12%) |
| 3 | 9 (4%) |
| 4 | 8 (4%) |
Abbreviations: KOOS, knee injury and osteoarthritis outcome score; ADL, activities of daily living; QoL, quality of life
Quadriceps asymmetry (<90% LSI) was observed in 54% of those with clinical knee OA and 35% of those without clinical knee OA. More symmetrical quadriceps strength was associated with lower odds of clinical knee OA (adjusted OR 0.96, 95% CI 0.93, 0.99). Specifically, for every 1% higher quadriceps strength LSI, there was 4% lower odds of clinical knee OA. Fourteen percent of those managed with rehabilitation alone and 22% of those after ACLR had clinical knee OA. (9) Surgical status was not associated with clinical OA (adjusted OR 0.58, 95% CI 0.23, 1.50).
Discussion
The results supported our primary hypothesis that higher quadriceps LSI was associated with lower odds of clinical knee OA. When considering clinical application and utility of our results, our analysis suggests a modest 1% higher quadriceps LSI was associated with 4% lower odds of clinical knee OA. Five years after ACL rupture or reconstruction, 54% of those classified with clinical knee OA had a quadriceps LSI <90%. The importance of maintaining quadriceps strength after ACL rupture that has been underscored in the literature is further supported by this analysis. Quadriceps weakness is associated with the development of symptomatic knee OA. (13,23) In people with diagnosed knee OA, stronger quadriceps are correlated with increased physical activity. (24) At the time of return to sport, patients with weaker quadriceps demonstrate poorer knee joint function and altered landing patterns. (18,25) Our results, taken with previous literature, highlight the importance of maintaining symmetric quadriceps strength after traumatic knee injury, such as ACL rupture, for long-term joint health.
Treatment choice (i.e. ACLR plus rehabilitation vs. rehabilitation alone) was not associated with early clinical knee OA in our cohort. Prior studies also reported that long term outcomes, including development of OA, are not different between those who undergo ACLR vs. rehabilitation alone after for ACL injury. (26,27) Maintaining long-term quadriceps strength symmetry is an important component of rehabilitation and long-term joint health regardless of how ACL ruptures are managed.
Our results support the use of the modified KOOS classification component of Luyten et al. (19) to identify participants who may benefit from continued further clinical intervention (i.e., quadriceps strength training) beyond discharge from rehabilitation, and education on quadriceps weakness being a significant risk factor for the development and progression of knee OA. (10) After ACL rupture, nearly all patients (98%) assume they have no or only slightly increased risk of developing post-traumatic OA. (28) Patients may benefit from discussions with health care practitioners regarding outcomes on the KOOS classification component of Luyten et al. (19) including strategies for maintaining joint health, such as maintaining quadriceps strength symmetry. Our results provide a direction for targeted secondary OA prevention after ACL rupture or reconstruction.
Practitioners and patients may be able to use the KOOS classification component of Luyten et al. (9) to monitor clinical OA risk. Fifty-four percent of the study sample had deficits in the knee related quality of life (KOOS QoL ≤85), and this included nearly all (40 of 41) participants classified with early clinical OA. While deficits in knee related quality of life were common, participants were required to report deficits in at least one more subscale (Pain, Symptoms, or ADL) to be classified with clinical knee OA for the KOOS portion of the Luyten et al. criteria. (19) Worse scores on the KOOS pain subscale are associated with poorer patient-reported outcomes (e.g., worse function, greater fear of movement, worse knee confidence) after ACLR. (29) Additionally, lower KOOS sports and recreation and pain subscales are associated with low self-reported knee stability in individuals with knee OA after ACLR. (30)
When compared to the general population KOOS scores, those in our cohort without early clinical knee OA as defined by modified Luyten et al. criteria exceeded uninjured, age matched scores on each subscale. (31) Those in our sample with early clinical OA, however, had lower mean values on every subscale than uninjured, age matched population scores. (31) These data indicate use of the KOOS subscales may assist in differentiating those with clinically relevant knee symptoms. Compared to individuals who report their knee status as acceptable after ACLR, (32) our group with early clinical knee OA had worse KOOS pain, ADL, sports and recreation, and quality of life scores. Patient acceptable symptom state (PASS), a state where individuals consider the current state of their knee to be satisfactory, was established in a cross-sectional analysis of individuals 1 to 5 years after ACLR (mean follow up 3.4 ± 1.3 years). (32) The PASS threshold was 88.9 for KOOS pain, 57.1 for KOOS symptoms, 100.0 for KOOS ADL, 75.0 for KOOS sports and recreation, and 62.5 for KOOS quality of life. In our sample classified with early OA, only the KOOS symptoms subscale exceeded the PASS threshold, while KOOS pain, KOOS ADL, KOOS sports and recreation, and KOOS quality of life did not. Conversely, in those without early OA, only the KOOS ADL subscale did not exceed the PASS threshold (99.1 vs 100). Our results, taken with these data, suggest that poor scores on at least 2 of 4 KOOS subscales (pain, symptoms, activities of daily living, knee-related quality of life) may be an important identifier of those who may be at risk of early OA development. If we can identify people who are at risk earlier, we can intervene with secondary prevention strategies such as quadriceps strengthening and potentially delay irreversible joint damage.
There are limitations of this study to consider when interpreting our results. Due to the cross-sectional study design and our statistical model, we cannot be sure that restoring quadriceps strength symmetry will change the clinical or structural trajectory for developing osteoarthritis after ACL rupture and we cannot assume a linear relationship. Additionally, we only applied the patient-reported component of the Luyten et al. (9) criteria to our sample. The full Luyten et al. (13) criteria have not yet been validated. Therefore, we are unable to conclude that quadriceps strength asymmetry was a direct contributor to clinical osteoarthritis. Further analysis is needed to examine the association of quadriceps strength with early clinical knee OA when the full criteria are applied. Strength testing differed slightly between sites, however we reported limb symmetry measures to ensure strength data are comparable. Caution should be used when interpreting limb symmetry indexes as using the contralateral limb as a benchmark may overestimate knee function; therefore, we cannot draw definite conclusions on absolute strength. Future analysis should consider the association of quadriceps strength with the development of radiographic OA.
In conclusion, more symmetrical quadriceps strength, but not surgical status, 5 years after ACL rupture was associated with lower odds of clinical knee OA. These results indicate that maintaining stronger quadriceps after ACL rupture, with or without reconstruction, could reduce the odds of clinical knee OA.
Significance and Innovation.
More symmetrical quadriceps strength, but not management (ACLR or rehabilitation alone), 5 years after ACL rupture was associated with lower odds of early clinical knee OA.
Our results provide a potential target (i.e., quadriceps strength symmetry) for secondary OA prevention programs after ACL rupture, allowing clinicians the possibility of intervening with quadriceps strengthening to potentially delay symptomatic knee OA.
Acknowledgements
The authors would like to acknowledge Håvard Moksnes, Ingrid Eitzen, Annika Storevold, Ida Svege, Espen Selboskar, Karin Rydevik, Marte Lund, Kristine Roberg Hytten, Andrew Lynch, Mathew Failla, Airelle Giordano, and Angela Smith for their assistance with data collection for this study. The authors acknowledge the Norwegian Sports Medicine Clinic, Nimi (www.nimi.no), for supporting the Norwegian Research Center for Active Rehabilitation with rehabilitation facilities and research staff. Additionally, the authors acknowledge the University of Delaware Physical Therapy Clinic rehabilitation resources and staff, and Martha Callahan and the Delaware Rehabilitation Institute ResCore staff.
This study was supported by the National Institutes of Health (R37-HD037985; F32-AR073090) and the University of Delaware Department of Physical Therapy PT PhD Endowment Grant. The authors certify they have no financial disclosures or direct financial interest in the subject matter. The authors have no conflicts of interest to disclose.
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