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Plantar pressure modifications in experienced runners following an exhaustive run
Sports Biomechanics
Abstract
Running-induced fatigue alters foot strike pattern. The purpose of this study was to assess plantar pressure and centre of pressure (CoP) trajectory alterations after a 30-minute run at sub-maximal speed in experienced long-distance runners. Plantar pressure data from 9 experienced heel-to-toe male runners was collected before and after a 30-minute run on a treadmill at a speed 5% above the respiratory compensation point (RCP) of each participant. Significant changes in the plantar-pressure map were found post-run, including increased impulses in the first metatarsal head (9.92%, p < 0.001) and hallux areas (16.19%, p < 0.001), and decreased impulses in the fourth and fifth metatarsal heads (4.95%, p < 0.05). The CoP curve showed a medial shift (p < 0.01). The plantar-pressure map and CoP trajectory were altered following a 30-minute exhausting run. These changes may indicate an increase in stress on joints and tissues when individuals are fatigued and may promote overload injuries.
... The studies were published between 1997 and 2020. Studies were performed mostly in Europe (Spain, France, Germany, the Netherlands, Switzerland, and the United Kingdom) (55%), [2,21,[50][51][52][53][54][55][56][57][58] followed by North America (USA) (7%) [22,43,[59][60][61][62][63], South America (5%) [62], and Asia (5%) [64], and no study was performed in Africa (0%). Most of the included studies were published by authors affiliated with the USA. ...
... Bercovitz et al. [64]. Israel ...
... The quality assessment revealed that all the included studies [2,21,22,43,[50][51][52][53][54][55][57][58][59][60][61][62][63][64][65] showed a low risk of bias. The risk of bias was presented in the traffic-light plot ( Figure 2) and summary plot (Figure 3). ...
Fatigue has the potential to alter how impact forces are absorbed during running, heightening the risk of injury. Conflicting findings exist regarding alterations in both kinematics and plantar pressure. Thus, this systematic review and subsequent meta-analysis were conducted to investigate the impact of general and localized muscle fatigue on kinematics and plantar pressure distribution during running. Initial searches were executed on 30 November 2021 and updated on 29 April 2023, encompassing PubMed, The Cochrane Library, SPORTDiscus, and Web of Science without imposing any restrictions on publication dates or employing additional filters. Our PECOS criteria included cross-sectional studies on healthy adults during their treadmill running to mainly evaluate local muscle fatigue, plantar pressure distribution, biomechanics of running (kinematics, kinetics, and EMG results), and temporospatial parameters. The literature search identified 6626 records, with 4626 studies removed for titles and abstract screening. Two hundred and one articles were selected for full-text screening, and 20 studies were included in qualitative data synthesis. The pooled analysis showed a non-significant decrease in maximum pressure under the right forefoot’s metatarsus, which was more than the left rearfoot after local muscle fatigue at a velocity of 15 km/h (p-values = 0.48 and 0.62). The results were homogeneous and showed that local muscle fatigue did not significantly affect the right forefoot’s stride frequency and length (p-values = 0.75 and 0.38). Strength training for the foot muscles, mainly focusing on the dorsiflexors, is recommended to prevent running-related injuries. Utilizing a standardized knee and ankle joint muscle fatigue assessment protocol is advised. Future experiments should focus on various shoes for running and varying foot strike patterns for injury prevention.
... Running due to its cyclic nature, creates different levels of fatigue among runners and can play a crucial role in RRI development, due to changes in running mechanics [7,8]. Changes in the plantar pressure distribution pattern is an important factor in the development of lower limb and foot injuries, and is associated with lower limb injuries [9,10]. ...
... Every two minutes, the treadmill speed increased by 1 km/h. Participants were asked to rate the RPE (rate of perceived exertion) by a 15-point Borg scale (a range score of [6][7][8][9][10][11][12][13][14][15][16][17][18][19][20]. Heart rates were also observed simultaneously using a heart rate monitor (Polar RS100, Woodbury, NY). ...
... These results are consistent with the results of Kim et al., that showed changes in running mechanics by fatigue [10]. Bercivitz et al. also showed that running-induced fatigue is associated with changes in plantar pressure distribution pattern in runners [8]. It has been reported that running-induced fatigue reduces lower limb muscle activity [11], which can reduce muscle shock absorption capacity [13] and could alter plantar pressure distribution patterns. ...
Background
Running induced-fatigue is an important factor in running related injuries. Runners with different strike types have different running mechanics and suffer from different injury patterns. Underlying mechanism of this difference is not well understood.
Research question
The aim of this study was to examine the effects of running-induced fatigue on plantar pressure distribution in runners with different strike types.
Methods
30 rearfoot (age = 21.56 ± 2.28 years; height = 1.67 ± 0.08 m; mass = 61.43 ± 11.57 kg; BMI = 21.77 ± 2.9 kg.m⁻²) and 30 forefoot (age = 19.73 ± 1.68 years; height = 1.71 ± 0.08 m; mass = 65.7 ± 13.45; BMI = 22.53 ± 3.39 kg.m⁻²) strike male and female recreational runners were recruited to this study. Participants ran in 3.3 m/s barefoot along the plantar pressure measuring device (Footscan®, Rsscan International) before and after running-induced fatigue. Fatigue protocol was performed on a treadmill. Peak plantar pressure and peak plantar force (% body weight), contact time and medio-lateral force ratio were calculated while running. Repeated measures ANOVA test was used to investigate the effect of running-induced fatigue on plantar pressure variables (p ≤ 0.05).
Results
After running-induced fatigue, in the rearfoot strike group, increases in loading of medial and lateral portions of the heel, first metatarsal and big toe was observed, and in lesser toes and in the forefoot push off phase, the medio-lateral force ratio decreased. While, in the forefoot strike group first to third metatarsals loading increased and fifth metatarsal loading decreased after fatigue, and medio-lateral force ratio in the foot flat and forefoot push off phase increased. In both groups contact time increased after fatigue.
Significance
Our data indicate that running-induced fatigue has different effects on plantar pressure distribution pattern in runners with different strike type. These different effects reflect different adaptation strategies in runners with different strike types, and could explain existence of different injury patterns in runners with different strike types.
... When a healthy person participates in sports such as badminton or running, muscle fatigue of the lower limb may be expected. These fatigued muscles can result in compromised reaction times, joint stability, and dynamic balance, thereby reducing impact absorption, which heightens the risk of injuries [21,38]. Athletes and coaches should monitor for fatigue alerts and ensure timely rest to recover muscle strength, preventing performance issues and injuries [39]. ...
Background:
Muscle fatigue, characterized by reduced force generation during repetitive contractions, impacts older adults doing daily activities and athletes during sports activities. While various sensors detect muscle fatigue via muscle activity, biochemical markers, and kinematic parameters, a real-time wearable solution with high usability remains limited. Plantar pressure monitoring detects muscle fatigue through foot loading changes, seamlessly integrating into footwear to improve the usability and compliance for home-based monitoring.
Objective:
This study aimed to investigate the effects of muscle fatigue on plantar pressure measurements using a self-developed wearable plantar pressure system.
Methods:
Twelve healthy participants completed a 5-minute calf muscle fatigue protocol. The plantar pressures and surface electromyography (sEMG) activity of the gastrocnemius muscles were recorded before and after exercise. The plantar pressures at 6 regions and the median frequency (MDF) of sEMG were analyzed to quantify fatigue.
Results:
The self-developed foot pressure system showed a significant decrease in plantar pressure peak values at the heel of the left (P=.003) and right feet (P=.001) and at the lateral toe of the left (P=.001) and right feet (P=.026). A significant increase was observed at the metatarsal head of both the left foot (P=.001) and the right foot (P=.017). The MDF of sEMG signals significantly decreased in the left (P=.001) and right gastrocnemius (P<.001).
Conclusions:
Plantar pressure changes and sEMG signals effectively detect gastrocnemius muscle fatigue using the proposed wearable system, supporting the development of a wearable solution for detecting muscle fatigue suitable for home-use.
... Among the many wearable devices used to evaluate neuromuscular fatigue, surface electromyography (EMG) [5,7] [8,9], inertial measurement unit (IMU) [10][11][12][13][14][15], and plantar force sensors [16][17][18] are the most common. However, surface EMG sensors are sensitive to skin cleanliness and placement, and their repeatability and portability are suboptimal. ...
Purpose
This study aimed to assess the feasibility of early detection of fatigued gait patterns for older adults through the development of a smart portable device.
Methods
The smart device incorporated seven force sensors and a single inertial measurement unit (IMU) to measure regional plantar forces and foot kinematics. Data were collected from 18 older adults walking briskly on a treadmill for 60 min. The optimal feature set for each recognition model was determined using forward sequential feature selection in a wrapper fashion through fivefold cross-validation. The recognition model was selected from four machine learning models through leave-one-subject-out cross-validation.
Results
Five selected characteristics that best represented the state of fatigue included impulse at the medial and lateral arches (increased, p = 0.002 and p < 0.001), contact angle and rotation range of angle in the sagittal plane (increased, p < 0.001), and the variability of the resultant swing angular acceleration (decreased, p < 0.001). The detection accuracy based on the dual signal source of IMU and plantar force was 99%, higher than the 95% accuracy based on the single source. The intelligent portable device demonstrated excellent generalization (ranging from 93 to 100%), real-time performance (2.79 ms), and portability (32 g).
Conclusion
The proposed smart device can detect fatigue patterns with high precision and in real time. Significance: The application of this device possesses the potential to reduce the injury risk for older adults related to fatigue during gait.
... In this study, participants complained of pain after running but did not present an injury. Besides injury, fatigue can alter the foot strike pattern [18] or modify the coordination pattern of several muscles [19]. Also, harmonics may indicate fatigue in specific sound frequencies in runners with pain, which is not visible in the pressure values. ...
Purpose
Humans interact with the environment using sensory channels. Although vision is the main sensory channel, the auditory channel is excellent for learning when trained. Movement learning via auditory inputs requires sound analysis, such as sonification.
Methods
Data on peak plantar pressure from 43 recreational runners were collected using Flexinfit resistive insoles. Participants wore Run Falcon 1.0 (Adidas) running shoes and were categorised into four groups: without pain; spine or hip pain; thigh or knee pain; and leg, ankle, or foot pain. Participants responded to whether they presented pain and whether it was related to running (training or races). Sonification data were collected using the twotone software. We used the c note in the first octave to transform numerical data into sounds according to the pressure magnitude. the sound file was decomposed using the Audacity software into a spectrogram illustrating the main frequency components and their amplitudes.
Results
The spectrogram made it possible to identify qualitative differences between the runners with and without pain after running. the frequency spectrum showed that some frequencies had greater sound intensity in runners without pain.
Conclusions
Our results indicated differences between runners with and without pain after running using sonification. the frequency spectrum also indicated a difference in the sound intensity produced between the groups at specific frequencies.
... Measurements captured with these devices include movement classifications (i.e. walking vs running) Marcos Mazon et al., 2022), accelerations to classify whole body loads/workload, kinematics (Reenalda et al., 2019), predictions of ground reaction forces and joint moments (Johnson et al., 2021) and pressures and forces under the feet (Bercovitz et al., 2022). With careful understanding and treatment of wearable data (Hughes et al., 2021), this paired with smart watch information can truly tell us step by step the interaction of the runner with their environment in real time and allow us to develop real-time biofeedback interventions (e.g. ...
Footwear plays a critical role in our daily lives, affecting our performance, health and overall well-being. Well-designed footwear can provide protection, comfort and improved foot function-ality, while poorly designed footwear can lead to mobility problems and declines in physical activity. The overall goal of footwear research is to provide a scientific basis for professionals in the field to provide an optimal footwear solution for a given person, for a given task, in a given environment, while using sustainable manufacturing processes. This article suggests potential directions for future research with a focus on athletic footwear biomechanics. Directions include the evidence-based individualisation of footwear, the interaction between design and prolonged use, and improving the sustainability of footwear. The authors also provide a speculative outlook on methodological developments that may provide greater insight into these areas. These developments may include: (1) the use of larger scale, real-world and representative data, (2) the use of 3D printing to create experimental footwear, (3) the advancement of in silico research methods, and (4) furthering multidisciplinary collaboration. If successfully applied in the future, footwear research will contribute to active and healthy lifestyles across the lifespan.
... Plantar foot pain occurs mainly in the forefoot under the metatarsal heads [7] and the heel [25] and is believed to be caused by an excessive load from repetitive impact to these regions [29]. During an endurance or exhaustive run, when muscle fatigue occurs, there is an increased loading to the metatarsal and midfoot regions [2,19]. These are possible reasons for foot pain occurrence in both heel and forefoot regions, and this load may also cause metatarsal bone deformation and metatarsal stress fracture [1]. ...
Background
Foot pain experienced by long-distance runners could be relieved by functional insoles which aim at evenly distributing the plantar pressure.
Research question
We hypothesised that an individually moulded insole with medial arch support would reduce the impact and loading under the heel and metatarsal regions.
Methods
Twelve male recreational runners ran on a treadmill at 10 km/h for 1 hour with flat insoles and medial arch supported insoles. A pressure insole system (Novel Pedar, Germany) was used to obtain the peak pressure, peak force, time normalised pressure-time integrals, and the percentage of the total force-time integrals under 10 regions.
Results
Medial arch supported insoles reduced the peak force under the heel (medial: -15.3%, p = 0.001; lateral: -19.2%, p = 0.037) during the initial run, and reduced peak pressure under the heel (medial: -13.3%, p = 0.005; lateral: -9.9%, p = 0.006), and peak force under the medial heel (-17.8%, p = 0.006) after the run. The percentage of the total force-time integrals under the heel was reduced (medial: -23.8%, p = 0.004; lateral: -13.6%, p = 0.022) after the run. No significant difference was found under the metatarsal regions. There is shift of load from the metatarsal regions to the medial mid-foot as indicated by the change of the percentage of total force-time integrals.
Significance
Medial arch supported insoles were effective in reducing the impact and loading under the heel region in prolonged running on a treadmill.
Level of evidence
Controlled laboratory study, Level V
Background:
The injury of the knee joint is found to be directly related to the fatigue caused by excessive exercise. Many previous studies used wearable devices to measure the angle of knee joint during activities, but did not pay enough attention to the load of knee joint related to the fatigue degree of it.
Objective:
A wearable embedded system was designed to sense the motion state and load of knee joint and uses the sensoring data to estimate and predict the fatigue degree of knee joint during exercise in real time, so as to prevent it from being injured.
Methods:
An economical wearable system is designed to measure the parameters of the knee joint during exercises. Then the warning message and recommended healthy lasting time are able to be sent to users to avoid excessive exercise. 24 healthy volunteers aged 20-25 years were involved in the experiments. Two famous evaluation scales for knee joint from Department of Orthopedics (Lysholm score and IKDC score) were adopted to evaluate the protective effect.
Results:
After 14 days of the first stage testing, all the participants with wearable devices reported healthy knee joint state to verify the effectiveness of the system. For the second stage, the testing group equipped with wearable warning devices did not receive obvious change in the two scales. However, Lysholm score of control group dropped by at least 7.4 and IKDC score dropped by at least 11.1 which were significantly reduced.
Conclusion:
Only using human perception to prevent knee joint fatigue had a risk of failure while the designed wearable system could protect the knee successfully from injuries during exercises, such as running, badminton, table tennis and basketball. Moreover, female gender and a high BMI value may be two factors that increase the risk of knee injuries during sports.
With marathon-running grew in popularity, the effect of long-distance running on plantar pressure has been more attractive. It has been proposed that long-distance running influences the deviation in the center of pressure (COP) during standing and the changes to plantar pressure during walking. The objective of this study was to observe the effects on the COP motion amplitude of static standing and the plantar pressure distribution of walking after long-distance running. The influence of a 10-km run on changes to plantar pressure was assessed during standing and walking. Plantar pressure was measured before and immediately after running. In the study, seven males and five females participated in barefoot tests of static standing and dynamic walking. In the static standing tests, COP was measured under the following four ordered conditions: (1) bipedal, eyes open, standing; (2) bipedal, eyes closed, standing; (3) unipedal, eyes open, standing and (4) unipedal, eyes closed, standing. Under each condition, the data was collected while a stable standing posture for 10 s. In the dynamic walking tests, the contact duration and plantar pressure were recorded. The standing tests results revealed no significant differences between males and females while slight differences before vs. after running. Running for a single time had no effect on COP deviation during standing. The walking tests results revealed an initial landing on the lateral heel. After landing on the lateral heel, the females quickly transferred to the medial heel. The movement of the pressure to the medial heel was slower in males than females. After running, the pressure of females was more inward, while that of males was more outward under the metatarsal zones in the propulsion phase.
Background
Knee injury is always a trouble for people in daily life. It not only threatens the career of an athlete but also affects a normal engineer through morning running. The injury of the knee joint is found to be directly related to the fatigue caused by excessive exercise.
Methods
An economical embedded system with a designed acceleration-weighted curve fitting method was developed to estimate and predict the knee fatigue state. Then the warning message and recommended lasting time were sent to users to avoid excessive exercise. 24 healthy volunteers were involved in the experiments to verify the effectiveness of the system compared to human perception.
Results
Only using human perception to prevent knee joint fatigue had a risk of failure while the designed wearable system could protect knee successfully. It was also found that the knee of female was more likely to be injured than the one of male in intense exercises and a high BMI value could influence the risk of knee injuries during sports. However, a short break in sports could significantly extend the healthy time for knee.
Conclusions
Early warning from the specially designed embedded system can successfully help people avoid knee joint fatigue and injuries during exercises, such as running, badminton, table tennis and basketball.
Pressure-sensitive measuring devices have been identified as appropriate tools for measuring an array of parameters during running. It is unclear which biomechanical characteristics relate to running-related injury (RRI) and which data-processing techniques are most promising to detect this relationship. This systematic review aims to identify pertinent methodologies and characteristics measured using plantar pressure devices, and to summarise their associations with RRI. PubMed, Embase, CINAHL, ScienceDirect and Scopus were searched up until March 2015. Retrospective and prospective, biomechanical studies on running using any kind of pressure-sensitive device with RRI as an outcome were included. All studies involving regular or recreational runners were considered. The study quality was assessed and the measured parameters were summarised. One low quality, two moderate quality and five high quality studies were included. Five different subdivisions of plantar area were identified, as well as five instants and four phases of measurement during foot–ground contact. Overall many parameters were collated and subdivided as plantar pressure and force, plantar pressure and force location, contact area, timing and stride parameters. Differences between the injured and control group were found for mediolateral and anteroposterior displacement of force, contact area, velocity of force displacement, relative force–time integral, mediolateral force ratio, time to peak force and inter-stride correlative patterns. However, no consistent results were found between studies and no biomechanical risk patterns were apparent. Additionally, conflicting findings were reported for peak force in three studies. Based on these observations, we provide suggestions for improved methodology measurement of pertinent parameters for future studies.
Test the hypothesis that greater baseline peak external knee adduction moment (KAM), KAM impulse, and peak external knee flexion moment (KFM) during the stance phase of gait are associated with baseline-to-2-year medial tibiofemoral cartilage damage and bone marrow lesion progression, and cartilage thickness loss.
Participants all had knee OA in at least one knee. Baseline peak KAM, KAM impulse, and peak KFM (normalized to body weight and height) were captured and computed using a motion analysis system and 6 force plates. Participants underwent MRI of both knees at baseline and two years later. To assess the association between baseline moments and baseline-to-2-year semiquantitative cartilage damage and bone marrow lesion progression and quantitative cartilage thickness loss, we used logistic regression with generalized estimating equations (GEE), adjusting for gait speed, age, gender, disease severity, knee pain severity, and medication use.
The sample consisted of 391 knees (204 persons): mean age 64.2 years (SD 10.0); BMI 28.4 kg/m(2) (5.7); 156 (76.5%) women. Greater baseline peak KAM and KAM impulse were each associated with worsening of medial bone marrow lesions, but not cartilage damage. Higher baseline KAM impulse was associated with 2-year medial cartilage thickness loss assessed both as % loss and as a threshold of loss, whereas peak KAM was related only to % loss. There was no relationship between baseline peak KFM and any medial disease progression outcome measures.
Findings support targeting KAM parameters in an effort to delay medial OA disease progression.
Copyright © 2015. Published by Elsevier Ltd.
Context:
Fatigue-induced alterations in foot mechanics may lead to structural overload and injury.
Objectives:
To investigate how a high-intensity running exercise to exhaustion modifies ankle plantar-flexor and dorsiflexor strength and fatigability, as well as plantar-pressure distribution in adolescent runners.
Design:
Controlled laboratory study.
Setting:
Academy research laboratory.
Patients or other participants:
Eleven male adolescent distance runners (age = 16.9 ± 2.0 years, height = 170.6 ± 10.9 cm, mass = 54.6 ± 8.6 kg) were tested.
Intervention(s):
All participants performed an exhausting run on a treadmill. An isokinetic plantar-flexor and dorsiflexor maximal-strength test and a fatigue test were performed before and after the exhausting run. Plantar-pressure distribution was assessed at the beginning and end of the exhausting run.
Main outcome measure(s):
We recorded plantar-flexor and dorsiflexor peak torques and calculated the fatigue index. Plantar-pressure measurements were recorded 1 minute after the start of the run and before exhaustion. Plantar variables (ie, mean area, contact time, mean pressure, relative load) were determined for 9 selected regions.
Results:
Isokinetic peak torques were similar before and after the run in both muscle groups, whereas the fatigue index increased in plantar flexion (28.1%; P = .01) but not in dorsiflexion. For the whole foot, mean pressure decreased from 1 minute to the end (-3.4%; P = .003); however, mean area (9.5%; P = .005) and relative load (7.2%; P = .009) increased under the medial midfoot, and contact time increased under the central forefoot (8.3%; P = .01) and the lesser toes (8.9%; P = .008).
Conclusions:
Fatigue resistance in the plantar flexors declined after a high-intensity running bout performed by adolescent male distance runners. This phenomenon was associated with increased loading under the medial arch in the fatigued state but without any excessive pronation.
The effects of treadmill running on impact acceleration were examined together with the interaction between running surface and runner's fatigue state. Twenty recreational runners (11 men and 9 women) ran overground and on a treadmill (at 4.0 m/s) before and after a fatigue protocol consisting of a 30-minute run at 85% of individual maximal aerobic speed. Impact accelerations were analysed using two lightweight capacitive uniaxial accelerometers. A two-way repeated-measure analysis of variance showed that, in the pre-fatigue condition, the treadmill running decreased head and tibial peak impact accelerations and impact rates (the rate of change of acceleration), but no significant difference was observed between the two surfaces in shock attenuation. There was no significant difference in acceleration parameters between the two surfaces in the post-fatigue condition. There was a significant interaction between surface (treadmill and overground) and fatigue state (pre-fatigue and post-fatigue). In particular, fatigue when running overground decreased impact acceleration severity, but it had no such effect when running on the treadmill. The effects of treadmill running and the interaction need to be taken into account when interpreting the results of studies that use a treadmill in their experimental protocols, and when prescribing physical exercise.
To review the cases of stress fracture seen over a 2-year period at a sports medicine clinic.
One hundred and eighty cases diagnosed as stress fractures on the basis of clinical picture and radiological evidence were reviewed. The following features of each stress fracture were noted: age, sex, site, sport/activity.
A sports medicine centre in Melbourne, Australia.
The average age was 21.8 years. Seventy eight of these stress fractures were seen in women, 102 in men.
The most common sites of stress fractures were the metatarsal bones (n = 42), tibia (n = 36), fibula (n = 30), tarsal navicular (n = 26) and pars interarticularis (n = 17). The most common sport was track (n = 54). Other common sports activities were jogging/distance running (n = 35), dance (n = 32) and Australian football (n = 14). The distribution of sites of stress fractures varied from sport to sport. Among the track athletes (n = 54), navicular (n = 19), tibia (n = 14) and metatarsal (n = 9) were the most common stress fracture sites. The distance runners (n = 35) predominantly sustained tibia (n = 15), and fibula (n = 8) stress fractures, while metatarsal stress fractures (n = 18) were the most common among dancers. The distribution of sports varied with the site of the stress fracture. In the metatarsal stress fractures (n = 42), dance was the most common activity. Distance running (n = 15) and track (n = 14) were the most common sports in the group to have sustained tibia stress fractures (n = 36). Track athletes (n = 14) were particularly prevalent in the navicular stress fracture group (n = 26).
The distribution of sites of stress fractures in this study shows some differences from previously published studies.
In previous reports we have shown that in long distance running the impact acceleration on the shank increases with progressing fatigue. The aim of the present study was to test whether, in parallel to this increase, an imbalance in the activities between the ankle plantar and dorsi flexor muscles develops. The tests were made on fourteen subjects during 30 min treadmill running above their anaerobic thresholds. Respiratory data were collected to determine the anaerobic threshold speed and to indicate the progressively developing metabolic fatigue. Surface electromyogram (EMG) was monitored to indicate the changing activity of the shank muscles. In the tibialis anterior the average integrated EMG (iEMG) and the mean power frequency (MPF) significantly decreased from the beginning to the end of running. In the gastrocnemius iEMG did not change, while MPF increased during the course of running. The impact acceleration, measured by means of an accelerometer attached to the tibial tuberosity, significantly increased during the course of running. It was concluded that, with developing fatigue, an imbalance in the contraction of the shank muscles develops in parallel to an increase in shank shock acceleration. The combination of these two changes may hamper the loading balance on the tibia since the bone becomes exposed to excessive bending stresses and to higher risk of stress injury. © 2000 Biomedical Engineering Society.
PAC00: 8719St, 0180+b, 8719Rr, 8719Nn, 8719Ff
To provide an extensive and up to date database for specific running related injuries, across the sexes, as seen at a primary care sports medicine facility, and to assess the relative risk for individual injuries based on investigation of selected risk factors.
Patient data were recorded by doctors at the Allan McGavin Sports Medicine Centre over a two year period. They included assessment of anthropometric, training, and biomechanical information. A model was constructed (with odds ratios and their 95% confidence intervals) of possible contributing factors using a dependent variable of runners with a specific injury and comparing them with a control group of runners who experienced a different injury. Variables included in the model were: height, weight, body mass index, age, activity history, weekly activity, history of injury, and calibre of runner.
Most of the study group were women (54%). Some injuries occurred with a significantly higher frequency in one sex. Being less than 34 years old was reported as a risk factor across the sexes for patellofemoral pain syndrome, and in men for iliotibial band friction syndrome, patellar tendinopathy, and tibial stress syndrome. Being active for less than 8.5 years was positively associated with injury in both sexes for tibial stress syndrome; and women with a body mass index less than 21 kg/m(2) were at a significantly higher risk for tibial stress fractures and spinal injuries. Patellofemoral pain syndrome was the most common injury, followed by iliotibial band friction syndrome, plantar fasciitis, meniscal injuries of the knee, and tibial stress syndrome.
Although various risk factors were shown to be positively associated with a risk for, or protection from, specific injuries, future research should include a non-injured control group and a more precise measure of weekly running distance and running experience to validate these results.
The mechanical effects of genu valgum and varum deformities on the subtalar joint were investigated. First, a theoretical model of the forces within the foot and lower extremity during relaxed bipedal stance was developed predicting the rotational effect on the subtalar joint due to genu valgum and varum deformities. Second, a kinetic gait study was performed involving 15 subjects who walked with simulated genu valgum and genu varum over a force plate and a plantar pressure mat to determine the changes in the ground reaction force vector within the frontal plane and the changes in the center-of-pressure location on the plantar foot. These results predicted that a genu varum deformity would tend to cause a subtalar pronation moment to increase or a supination moment to decrease during the contact and propulsion phases of walking. With genu valgum, it was determined that during the contact phase a subtalar pronation moment would increase, whereas in the early propulsive phase, a subtalar supination moment would increase or a pronation moment would decrease. However, the current inability to track the spatial position of the subtalar joint axis makes it difficult to determine the absolute direction and magnitudes of the subtalar joint moments.
The purpose of this study was to present a systematic overview of published reports on the incidence and associated potential risk factors of lower extremity running injuries in long distance runners. An electronic database search was conducted using the PubMed-Medline database. Two observers independently assessed the quality of the studies and a best evidence synthesis was used to summarise the results. The incidence of lower extremity running injuries ranged from 19.4% to 79.3%. The predominant site of these injuries was the knee. There was strong evidence that a long training distance per week in male runners and a history of previous injuries were risk factors for injuries, and that an increase in training distance per week was a protective factor for knee injuries.
Background:
Osteoarthritis (OA) is a chronic condition characterized by pain, impaired function, and reduced quality of life. A number of risk factors for knee OA have been identified, such as obesity, occupation, and injury. The association between knee OA and physical activity or particular sports such as running is less clear. Previous reviews, and the evidence that informs them, present contradictory or inconclusive findings.
Purpose:
This systematic review aimed to determine the association between running and the development of knee OA.
Study design:
Systematic review and meta-analysis.
Methods:
Four electronic databases were searched, along with citations in eligible articles and reviews and the contents of recent journal issues. Two reviewers independently screened the titles and abstracts using prespecified eligibility criteria. Full-text articles were also independently assessed for eligibility. Eligible studies were those in which running or running-related sports (eg, triathlon or orienteering) were assessed as a risk factor for the onset or progression of knee OA in adults. Relevant outcomes included (1) diagnosis of knee OA, (2) radiographic markers of knee OA, (3) knee joint surgery for OA, (4) knee pain, and (5) knee-associated disability. Risk of bias was judged by use of the Newcastle-Ottawa scale. A random-effects meta-analysis was performed with case-control studies investigating arthroplasty.
Results:
After de-duplication, the search returned 1322 records. Of these, 153 full-text articles were assessed; 25 were eligible, describing 15 studies: 11 cohort (6 retrospective) and 4 case-control studies. Findings of studies with a diagnostic OA outcome were mixed. Some radiographic differences were observed in runners, but only at baseline within some subgroups. Meta-analysis suggested a protective effect of running against surgery due to OA: pooled odds ratio 0.46 (95% CI, 0.30-0.71). The I(2) was 0% (95% CI, 0%-73%). Evidence relating to symptomatic outcomes was sparse and inconclusive.
Conclusion:
With this evidence, it is not possible to determine the role of running in knee OA. Moderate- to low-quality evidence suggests no association with OA diagnosis, a positive association with OA diagnosis, and a negative association with knee OA surgery. Conflicting results may reflect methodological heterogeneity. More evidence from well-designed, prospective studies is needed to clarify the contradictions.
Excessive foot loading has been considered as a contributing factor for fatigue fractures of the metatarsal bones and may thus be potentially limiting the individual's training capacity and athletic performance. This study investigated the fatiguing effects of long-distance running on foot loading characteristics in a cohort of runners and triathletes. Twenty-three experienced runners were measured before, during and after a 25-km training run with in-shoe plantar pressure measurements with PEDAR insoles. An EMED platform was used to compare plantar pressures during barefoot walking before and after the run. The comparisons revealed distinct foot loading changes, especially a significant load reduction under the toes (up to 30% difference) and midfoot (up to 14% difference) and significantly increased loading under the central forefoot (up to 14% difference). These results confirm the potentially detrimental effect of running when fatigued and may help to understand the occurrence of fatigue fractures in the metatarsals. The findings could be used to design appropriate footwear and/or insoles in order to prevent overloading in extended running.
The objective of this study was to record plantar pressures using an in-shoe measuring system before, during, and after a mara-thon run in ten experienced long-distance runners with a mean age of 37.7 ± 11.5 years. Peak and mean plantar pressures were recorded before, after, and every three km during a marathon race. There were no significant changes over time in peak and mean plantar pressures for either the dominant or non-dominant foot. There were significant between foot peak and mean plantar pressure differences for the total foot (p = 0.0001), forefoot (p = 0.0001), midfoot (p = 0.02 resp. p = 0.006), hindfoot (p = 0.0001), first ray (p = 0.01 resp. p = 0.0001) and MTP (p = 0.05 resp. p = 0.0001). Long-distance runners do not demonstrate significant changes in mean or peak plantar foot pressures over the distance of a marathon race. However, athletes consistently favoured their dominant extremity, applying significantly higher plantar pressures through their dominant foot over the entire marathon distance.
This study aimed to assess the effects of running-induced fatigue on plantar pressure parameters in novice runners with low and high medial longitudinal arch. Plantar pressure data from 42 novice runners (21 with high, and 21 with low arch) were collected before and after running-induced fatigue protocol during running at 3.3 m/s along the Footscan® platform. Peak plantar pressure, peak force and force-time integral (impulse) were measured in ten anatomical zones. Relative time for foot roll-over phases and medio-lateral force ratio were calculated before and after the fatigue protocol. After the fatigue protocol, increases in the peak pressure under the first-third metatarsal zones and reduction under the fourth-fifth metatarsal regions were observed in the low arch individuals. In the high arch group, increases in peak pressure under the fourth-fifth metatarsal zones after the running-induced fatigue was observed. It could be concluded that running-induced fatigue had different effects on plantar pressure distribution pattern among novice runners with low and high medial longitudinal foot arch. These findings could provide some information related to several running injuries among individuals with different foot types.
• This prospective study of 583 habitual runners used baseline information to examine the relationship of several suspected risk factors to the occurrence of running-related injuries of the lower extremities that were severe enough to affect running habits, cause a visit to a health professional, or require use of medication. During the 12-month follow-up period, 252 men (52%) and 48 women (49%) reported at least one such injury. The multiple logistic regression results identified that running 64.0 km (40 miles) or more per week was the most important predictor of injury for men during the follow-up period (odds ratio=2.9). Risk also was associated with having had a previous injury in the past year (odds ratio = 2.7) and with having been a runner for less than 3 years (odds ratio=2.2). These results suggest that the incidence of lower-extremity injuries is high for habitual runners, and that for those new to running or those who have been previously injured, reducing weekly distance is a reasonable preventive behavior.(Arch Intern Med. 1989;149:2565-2568)
Footwear-generated biomechanical manipulation of lower-limb joints has been shown to influence lower-limb biomechanics. Numerous studies report the influence of such interventions on the knee, however little is known about the influence of these interventions on the hip. The present study analyzed kinetic and kinematic changes about the hip of 12 healthy young males who underwent biomechanical manipulation utilizing the APOS biomechanical device (APOS–Medical and Sports Technologies Ltd., Herzliya, Israel) allowing controlled foot center of pressure manipulation. Subjects underwent gait testing in four para-sagittal device configurations: Medial, lateral, neutral, and regular shoes. In the medial configuration, subjects demonstrated no change in step width (i.e., distance between right and left foot center of pressure), however inter-malleolar distance significantly increased. Likewise with the medial setting, greater hip abduction was recorded, while hip adduction moment and joint reaction force decreased significantly. We speculate that subjects adopt a modified gait pattern aimed to maintain constant base of support. As a result, hip abductor muscle moment arm increases and adduction moment and joint reaction force decreases. To the best of our knowledge this is the first study to show this relationship. These results contribute to the understanding of lower-limb biomechanics and warrant further investigation. © 2014 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res
In-shoe plantar pressure measurement has the potential to play a crucial role in the screening, treatment and behavior modification of patients who are at risk of, or are experiencing a variety of foot problems. In this article we review the instrumentation, methodology, applications, and rationale for in-shoe plantar pressure measurement. Possible new applications in the future are also discussed. In-shoe techniques are advantageous compared to the more traditional platform devices because they permit the most important interface, that between the foot and shoe, to be monitored and they allow for increased versatility of measurement for the calculation of more robust statistical estimates. Both discrete transducers and matrix systems have been developed; each approach has its advantages and disadvantages but, in general, matrix systems are preferable. Although there are still device limitations which must be overcome the technique of in-shoe measurement has opened the door to a whole new realm of pressure studies both in research and clinical practice.
The differences produced when running on a treadmill vs overground may call into question the use and validity of the treadmill as a piece of equipment commonly used in research, training, and rehabilitation. The aim of the present study was to analyze under pre/post fatigue conditions the effect of treadmill vs overground on plantar pressures. Twenty-seven recreational runners (17 men and 10 women) ran on a treadmill and overground at two speeds: S1=3.33m/s and S2=4.00m/s, before and after a fatigue protocol consisting of a 30-min run at 85% of their individual maximal aerobic speed (MAS). Contact time (CT in seconds), peak pressure (PP in kPa), and relative load (RL in %) were analyzed under nine foot zones of the left foot using an in-shoe plantar pressure device. A two-way repeated measures ANOVA showed that running on a treadmill increases CT (7.70% S1 and 9.91% S2), modifies the pressure distribution and reduces PP (25.98% S1 and 31.76% S2), especially under the heel, medial metatarsals, and hallux, compared to running overground. Moreover, on both surfaces, fatigue (S2) led to a reduced stride frequency (2.78%) and reduced PP on the lateral heel and hallux (15.96% and 16.35%, respectively), and (S1) increased relative load on the medial arch (9.53%). There was no significant interaction between the two factors analyzed (surface and fatigue). Therefore, the aforementioned surface effect, which occurs independently of the fatigue state, should be taken into account when interpreting the results of studies that use the treadmill in their experimental protocols, and when prescribing physical exercise on a treadmill.
Objective:
The adduction moment at the knee during gait is the primary determinant of medial-to-lateral load distribution. If the adduction moment contributes to progression of osteoarthritis (OA), then patients with advanced medial tibiofemoral OA should have higher adduction moments. The present study was undertaken to investigate the hypothesis that the adduction moment normalized for weight and height is associated with medial tibiofemoral OA disease severity after controlling for age, sex, and pain level, and to examine the correlation of serum hyaluronan (HA) level with disease severity and with the adduction moment in a subset of patients.
Methods:
Fifty-four patients with medial tibiofemoral OA underwent gait analysis and radiographic evaluation. Disease severity was assessed using the Kellgren-Lawrence (K-L) grade and medial joint space width. In a subset of 23 patients with available sera, HA was quantified by sandwich enzyme-linked immunosorbent assay. Pearson correlations, a random effects model, and multivariate regression models were used.
Results:
The adduction moment correlated with the K-L grade in the left and right knees (r = 0.68 and r = 0.60, respectively), and with joint space width in the left and right knees (r = -0.45 and r = -0.47, respectively). The relationship persisted after controlling for age, sex, and severity of pain. The partial correlation between K-L grade and adduction moment was 0.71 in the left knees and 0.61 in the right knees. For every 1.0-unit increase in adduction moment, there was a 0.63-mm decrease in joint space width. In the subset of patients in whom serum HA levels were measured, HA levels correlated with medial joint space width (r = -0.55), but not with the adduction moment.
Conclusion:
There is a significant relationship between the adduction moment and OA disease severity. Serum HA levels correlate with joint space width but not with the adduction moment. Longitudinal studies will be necessary to determine the contribution of the adduction moment, and its contribution in conjunction with metabolic markers, to progression of medial tibiofemoral OA.
The purpose of this study was to assess plantar pressure alterations after long-distance running. Prior to and after a 20 km run, force distribution underneath the feet of 52 participants was registered using Footscan(®) pressure plates while the participants ran shod at a constant self-selected pace. Peak force, mean force and impulse were registered underneath different zones of the foot. In addition, temporal data as total foot contact time, time of contact and end of contact were derived for these zones. Furthermore, a medio-lateral pressure distribution ratio was calculated in different phases of the roll-off. After the run, increases in the loading of the forefoot, midfoot and medial heel were noted and decreases in loading of the lateral toes. In the forefoot push off phase a more lateral pressure distribution was observed. The results of this study demonstrated plantar pressure deviations after long-distance running which could give additional information related to several running injuries.
Footwear-generated biomechanical manipulations (e.g., wedge insoles) have been shown to reduce the magnitude of adduction moment about the knee. The theory behind wedged insoles is that a more laterally shifted location of the center of pressure reduces the distance between the ground reaction force and the center of the knee joint, thereby reducing adduction moment during gait. However, the relationship between the center of pressure and the knee adduction moment has not been studied previously. The aim of this study was to examine the association between the location of the center of pressure and the relative magnitude of the knee adduction moment during gait in healthy men.
A novel foot-worn biomechanical device which allows controlled manipulation of the center of pressure location was utilized. Twelve healthy men underwent successive gait analysis testing in a controlled setting and with the device set to convey three different para-sagittal locations of the center of pressure: neutral, medial offset and lateral offset.
The knee adduction moment during the stance phase significantly correlated with the shift of the center of pressure from the functional neutral sagittal axis in the coronal plane (i.e., from medial to lateral). The moment was reduced with the lateral sagittal axis configuration and augmented with the medial sagittal axis configuration.
The study results confirm the hypothesis of a direct correlation between the coronal location of the center of pressure and the magnitude of the knee adduction moment.
Ground reaction forces and center of pressure (C of P) patterns were studied in 17 subjects running at 4.5 ms−1. The subjects were classified as rearfoot or midfoot strikers according to the location of the C of P at the time of first contact between foot and ground. The C of P path in the rearfoot group showed a continuous anterior movement during support while the C of P in most of the midfoot group migrated posteriorly during the first 20 ms of the support phase. Variability in both groups was most marked during early support. The mean peak to peak force components were 3 BW, 1 BW and 0.3 BW in the vertical, anteroposterior and mediolateral directions respectively. Consistent differences between groups were noted in all three components, but individual differences within a given group were also considerable. The C of P patterns are presented in conjunction with ground reaction force data, and the implications of the results in the areas of running mechanics, shoe design and sports injury are discussed.
The measurement of center of pressure has been widely used in the evaluation of foot function. This article will describe center of pressure and indicate how it can be used to calculate moments about the joint axes of the foot. Various uses of center of pressure described in the literature will be examined. A model based on the use of the location of center of pressure relative to the location of the subtalar joint axis will be proposed as a theoretical explanation of selected foot pathologies and their treatment.
To study posterior tibialis tendon dysfunction using an in vitro model of the foot and ankle during the heel-off instant of gait.
Previous studies have concentrated primarily on the effect of posterior tibialis tendon dysfunction on the kinematics of the hindfoot and the arch.
The specimens were loaded using a custom designed axial and tendon loading system and the location of the center of pressure was used to validate heel-off. Arch position, hindfoot position and plantar pressure data were recorded before and after the posterior tibialis tendon was unloaded. These data were recorded with the ligaments intact and after creating a flatfoot deformity.
Unloading the posterior tibialis tendon caused significant posterior movement in the center of pressure for the intact and flatfoot conditions. This also resulted in a medial shift in the force acting on the forefoot. The forefoot loads shifted medially after a flatfoot was created even when the posterior tibialis tendon remained loaded. The spatial relationships of the bones of the arch and the bones of the hindfoot also changed significantly for the intact specimen, and to a lesser extent after a flatfoot.
The posterior tibialis tendon plays a fundamental role in shifting the center of pressure anteriorly at heel-off. Posterior tibialis tendon dysfunction causes posterior shift in the center of pressure and abnormal loading of the foot's medial structures. This may be the reason that posterior tibialis tendon dysfunction leads to an acquired flatfoot deformity. Conversely, flatfoot deformity may be a predisposing factor in the onset of posterior tibialis tendon dysfunction. This tendon also acts to lock the bones of the arch and the hindfoot in a stable configuration at heel-off, but a flatfoot deformity compromises this ability.
Stress fractures are common overuse injuries in runners and appear most frequently in the metatarsals.
To investigate fatigue-related changes in surface electromyographic activity patterns and plantar pressure patterns during treadmill running as potential causative factors for metatarsal stress fractures.
Prospective cohort study with repeated measurements.
Thirty experienced runners volunteered to participate in a maximally exhaustive run above the anaerobic threshold. Surface electromyographic activity was monitored for 14 muscles, and plantar pressures were measured using an in-shoe monitoring system. Fatigue was documented with blood lactate measurements.
The results demonstrated an increased maximal force (5%, P < .01), peak pressure (12%, P < .001), and impulse (9%, P < .01) under the second and third metatarsal head and under the medial midfoot (force = 7%, P < .05; pressure = 6%, P < .05; impulse = 17%, P < .01) toward the end of the fatiguing run. Contact area and contact time were only slightly affected. The mean electromyographic activity was significantly reduced in the medial gastrocnemius (-9%, P < .01), lateral gastrocnemius (-12%, P < .01), and soleus (-9%, P < .001) muscles.
The demonstrated alteration of the rollover process with an increased forefoot loading may help to explain the incidence of stress fractures of the metatarsals under fatiguing loading conditions.
The purpose of this study was to establish a representative reference dataset for temporal characteristics of foot roll-over during barefoot jogging, based on plantar pressure data collected from 220 healthy young adults. The subjects ran at 3.3 ms-1 over a 16.5 m long running track, having a built-in pressure platform mounted on a force platform. The initial contact, final contact, time to peak pressure and the duration of contact at the lateral and medial heel, metatarsal heads I to V and the hallux were measured. Temporal plantar pressure variables were found to be reliable (93% of ICC coefficients above 0.75) and both gender and asymmetry influences could be neglected. Foot roll-over during jogging started with heel contact followed by a latero-medial contact of the metatarsals and finally the hallux. After heel off, the forefoot started to push off at the lateral metatarsals, followed by a more central push off over the second metatarsal and finally over the hallux. Based on the plantar pressure data, the stance phase during running was divided into four distinct phases: initial contact (8.2%), forefoot contact (11.3%), foot flat (25.3%) and forefoot push off (55.1%). These findings provide a reliable and representative reference dataset for temporal characteristics of foot roll-over during jogging of young adults that may also be relevant in the evaluation of running patterns.
This review examines recent in-vivo studies of ambulation and discusses the fundamental role of mechanics of ambulation in the initiation and progression of osteoarthritis at the knee.
Recent studies have supported earlier findings that a high adduction moment at the knee during ambulation was most frequently reported to influence the progression of medial compartment osteoarthritis. In contrast to previous findings in patients with osteoarthritis, recent work on healthy subjects reports that cartilage thickness increases with high ambulatory loads. Kinematic changes were associated with the initiation of osteoarthritis. Recent studies of subjects with high risk factors for knee osteoarthritis (obesity and anterior cruciate ligament injury) reported a relationship between kinematic changes during ambulation and the initiation of osteoarthritis at the knee. This review also contrasts the relative influence on osteoarthritis of knee mechanics measured during ambulatory and nonambulatory activities.
The initiation of osteoarthritis occurs when healthy cartilage experiences some condition (traumatic or chronic) that causes kinematic changes during ambulation at the knee to shift the load-bearing contact location of the joint to a region not conditioned to the new loading. The rate of progression of osteoarthritis is associated with increased load during ambulation.
Our purpose was to assess the effect of foot intrinsic muscle fatigue on pronation, as assessed with navicular drop, during static stance. Twenty-one healthy young adults participated. Navicular drop was measured before and after fatiguing exercise of the plantar foot intrinsic muscles. Surface electromyography of the abductor hallucis muscle was recorded during maximum voluntary isometric contractions (MVIC) in order to find the baseline median frequency (MedF). Subjects then performed sets of 75 repetitions of isotonic flexion contractions of the intrinsic foot muscles against a 4.55 kg weight on a custom pulley system. After each set an MVIC was performed to track shifts in MedF. After a MedF shift of at least 10%, navicular drop measurements were repeated. Subjects exhibited 10.0+/-3.8mm of navicular drop at baseline and 11.8+/-3.8mm after fatigue (p<0.0005). The change in navicular drop was significantly correlated with change in MedF (r=.47, p=.03). The intrinsic foot muscles play a role in support of the medial longitudinal arch in static stance. Disrupting the function of these muscles through fatigue resulted in an increase in pronation as assessed by navicular drop.
The growing popularity of endurance sports activities is associated with a growing number of metatarsal stress fractures in recreational runners. Excessive foot loading has been suggested as a potential cause for these problems [Bennell, K, Matheson G, Meeuwisse W, Brukner P. Risk factors for stress fractures. Sports Med 1999;28(2):91-122]. Therefore, the question arises whether long distance running affects foot loading characteristics like ground reaction forces and peak pressure in specific areas of the foot.
To investigate the effects of long distance running on plantar pressure patterns before and after a marathon race.
Repeated measurements of recreational runners before and after a marathon race.
Two hundred participants of the third Muenster marathon, 2004, were measured before and after the race with plantar pressure measurements during barefoot walking on a capacitive platform. The ratio between forefoot and toe loading was calculated to assess a suggested loading shift between these areas.
The results of the whole group of participants revealed a significant difference in foot loading characteristics before and after the race. Post-race peak pressure and impulse values were higher in the forefoot regions and reduced under the toes.
The increased peak pressure under the metatarsal heads after the race indicates a load shift from the toes to the metatarsal heads. This suggests an increased loading of the metatarsal bones and could explain the increased incidence of metatarsal stress fractures in long distance runners.
There are many suspected risk factors for running-related overuse injuries; however, this remains a difficult area to adequately study. Numerous studies concerning factors that contribute to running injuries now exist in the literature, but inconsistent and sometimes conflicting results are found. This is likely due to different methodologies, definitions, outcome measures, and studied populations. This article reviews and summarizes several relevant studies on this topic, focusing on anatomic (intrinsic) risk factors as well as risk factors related to training (extrinsic). Due to the likely multifactorial nature of running injuries, very few firm conclusions can be made based on the existing studies. Training volume (mileage) and the occurrence of previous injuries seem to be the two most consistent risk factors across epidemiologic studies.
Knee adduction moment, serum hyaluronan level, and disease severity in medial tibiofemoral osteoarthritis
- T P Andriacchi
Andriacchi,T.P.
(1998). Knee adduction moment, serum hyaluronan level, and disease severity in medial
tibiofemoral osteoarthritis. Arthritis and Rheumatism, 41, 1233-1240. doi:10.1002/1529-0131
(199807)41:7<1233::AID-ART14>3.0.CO;2-L