Running is a globally popular form of sport and exercise with numerous metabolic (1), cardiovascular (1), musculoskeletal (2), and mental health benefits (3). Out of the almost 17 million runners who completed races in the United States in 2016, female runners accounted for 9.7 million finishers representing 57% of the running population (4). Many runners experience an injury every year (5), which may contribute to discontinuation of running (6). Injuries at the knee account for about 50% of all running-related injuries (5,7) and may be more common among females than males (5,7). Notably, there is a reduction in the participation of female runners in competitive races beyond the fifth decade of life (4).
One of the common age-related chronic degenerative disorders that occurs at the knee joint is osteoarthritis (OA) (8). Knee OA can occur in the patellofemoral joint, tibiofemoral joint (TFJ), or both. TFJ OA is most common in the medial tibiofemoral compartment (8). Women are at greater risk for developing TFJ OA compared with men, particularly those older than 50 yrs (9). Excessive and repetitive TFJ loading during gait has been linked to the onset, progression, and severity of TFJ OA (8,10). Compression forces perpendicular to the joint/articular surface are important in regulating cellular metabolism and maintaining normal cartilage matrix, but elevated forces could damage the extracellular collagen–proteoglycan matrix of the articular cartilage (11). In addition, anterior shear forces act parallel to the TFJ surface and may contribute to friction-induced wear at the knee joint (12).
Previous studies have explored the acute effects of altered step length (SL) and step frequency (SF) on lower extremity mechanics during running (13–17). It is consistently determined that a 5%–10% increase in SF decreases compressive joint contact forces at the hip, TFJ, patellofemoral, and ankle joints (16,17). This same SF increase results in reduced knee joint energy absorption, center of mass excursion, and shock attenuation during running (15). Allowing runners to run at their self-selected SF rather than manipulating their SF would assist in understanding the TFJ loading patterns that they typically experience during running compared with observing acute effects of gait retraining interventions of SF manipulation. This could also help to explain the differences in lower extremity running biomechanics especially at the TFJ in runners naturally adjusted to their running pattern running at higher self-selected SF compared with running at low SF (LSF).
Previous research has explored the effects of SF manipulation on axial TFJ forces, but no study has investigated the relationship between SF and TFJ axial forces among runners running at different self-selected SF (17). Further, TFJ anterior shear forces during running have not been previously compared among recreational runners with varied SF. The purpose of this study was to evaluate peak TFJ anterior shear and compression forces among female recreational runners demonstrating different self-selected SF. We hypothesized that at a fixed pace, runners with the highest SF would demonstrate lower peak TFJ anterior shear and compressive forces.
METHODS
The study was approved by the university institutional review board, and all participants provided their informed consent before participation. Fifty-five healthy female recreational runners between the ages of 18 and 65 yr who ran at least 10 miles per week volunteered to participate in the study. To be eligible, they had to be free of injury at the moment of data collection and during the previous 6 months. An injury was defined as an interruption of their routine training schedules due to any pain in the bilateral lower extremities. The right lower extremity of all subjects was used for analysis. All participants wore the same type of shoe (model 690; New Balance, Boston, MA) during testing. A standing calibration trial with 39 retroreflective markers was collected to establish joint centers, body segment coordinate systems, segment dimensions, and local positions of tracking markers. Segments were defined by joint markers on the iliac crests, greater trochanters, medial and lateral femoral condyles, medial and lateral malleoli, and first and fifth metatarsal heads. After the standing calibration trial, 16 joint markers were removed and only 23 tracking markers remained. Tracking markers were positioned as clusters on the shank, thigh, and the pelvis. The rearfoot was tracked using three retroreflective markers placed on the participant’s shoe over the superior and inferior posterior calcaneus and the lateral aspect of the calcaneus. Gait analysis was conducted on an instrumented treadmill (Treadmetrix, Park City, UT) while participants ran at 2.98 m·s−1, which corresponds to 6 mph and is a typical self-selected training pace for female recreational runners. Previous studies have demonstrated similar preferred running pace for recreational runners (13,15,16). All the runners ran at the same pace to independently assess the influence of self-selected SF on mechanical outcomes. Kinematic data were collected using a five-camera motion analysis system (OQUS 3; Qualisys, Goteborg, Sweden) at 120 Hz, which was synchronized with ground reaction force data sampled at 1200 Hz. Six consecutive stance phases for the right limb were extracted for analysis. Stance phase was determined using an 80-N threshold at initial contact and toe-off. SF for every participant was calculated by counting the number of complete footsteps on both limbs (right–left) over a 30-s interval and multiplying by 2.
Data processing
Marker trajectory and ground reaction force data were filtered using a fourth-order zero lag Butterworth filter with a cutoff frequency of 20 Hz. Stance phase hip, knee, and ankle joint angles, net joint moments, and joint reaction forces were calculated using an inverse dynamics approach (C-motion, Inc., Germantown, MD). Joint angles were calculated as Cardan angles between adjacent local segments using a flexion/extension–abduction/adduction–axial rotation sequence. Net knee internal joint moments were expressed in the proximal segment coordinate system and normalized to body mass and height. The hip, knee, and ankle joint angles, joint moments, and knee joint reaction forces served as inputs for a biomechanical TFJ contact force model that has been described in detail elsewhere (18). Briefly, hamstring, quadriceps, and gastrocnemius muscle force estimates during walking were derived using inputs of hip, knee, and ankle angles, net joint moments, muscle moment arms, and cross-sectional areas. Muscle moment arms as a function of joint position were calculated using nonlinear equations fit to the data of previous studies (18–20). Muscle cross-sectional areas were based on data provided by Ward et al. (21). These muscle forces were combined with the joint reaction forces to yield total TFJ compression force. Because the proximal tibia slopes posteriorly relative to its longitudinal axis, estimated axial TFJ compression and shear forces using this model were reported relative to an 8.8° posterior tibial slope (22). The proportion of the axial TFJ compression force acting on the medial tibial compartment was estimated based on the assumptions that total TFJ compression force exists completely on two contact points at the lateral and medial tibial plateau and that these contact locations follow a sagittal path during gait (23). As such, total axial TFJ force was distributed to contact points at 25% (medial) and 75% (lateral) of subject-specific knee joint width in a manner that achieves the frontal plane knee joint moment throughout stance phase (24). Peak axial TFJ force and TFJ impulse estimates using this model were previously compared with in vivo measurements from an instrumented prosthesis during walking (25). Using the synchronized gait data provided with the in vivo loads as input to our model, we determined the peak axial total TFJ force and TFJ impulse model estimate to be within 3% and 7%, respectively, of in vivo measurements (see Figure, Supplemental Digital Content 1, TFJ contact forces [A] and medial compartment TFJ forces [B] comparisons with Fregly el al. [2012] during the normal walking condition, https://links.lww.com/MSS/B512). Estimated medial TFJ peak force and medial TFJ impulse were within 7% and 4%, respectively, of in vivo measurements. To our knowledge, gait data with in vivo measurements from an instrumented prosthesis during running are not available. However, axial TFJ force estimates derived using this model are well within the range of estimates made at similar running speeds using alternative methods (26). To our knowledge, in vivo sagittal plane shear forces during running have also not been previously reported. Dependent variables analyzed in this study included peak TFJ anterior shear force, peak axial TFJ compression force, and peak TFJ medial compartment compression force.
Statistical analyses
Three SF subgroups were created by dividing all the participants in the group in to thirds as follows: low (≤166), middle (168–176), and high (≥178) steps per minute. Differences between SF groups for each dependent variable were compared using one-way ANOVA. If significantly different, Tukey’s post hoc tests were performed to provide individual comparisons between groups. Levene’s test for homogeneity of variance was used to assess equality of variance for all the dependent variables. SAS® software, version 9.3 for Windows (SAS Institute Inc., Cary, NC), was used for all statistical analyses with an alpha level of 0.05 considered statistically significant.
RESULTS
Of the 55 female runners who completed the study, data from two subjects each in the LSF group and the middle SF (MSF) group and one subject in the high SF (HSF) group were eliminated from the analysis as their values of peak TFJ shear forces or peak TFJ compression forces were outside two SD from the mean values resulting in a nonnormal distribution of data. As a result, the LSF group had 16 subjects, the MSF group had 20 subjects, and the HSF group had 14 subjects. The results with all the 55 subjects have been included (see Table, Supplemental Digital Content 2, Participant values for peak anterior TFJ shear forces, peak TFJ compression forces and peak medial compartment TFJ compression forces for the three SF groups, https://links.lww.com/MSS/B513). There were no differences between subjects in the SF groups for height, weight, or BMI. However, age was significantly different with post hoc analysis revealing that the HSF group was significantly older than the LSF group (Table 1).
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TABLE 1: Participant demographics for the three SF groups.
Peak TFJ anterior shear force
Peak anterior TFJ shear forces differed significantly among groups (LSF, 1.68 ± 0.33 BW; MSF, 1.63 ± 0.30 BW; HSF, 1.43 ± 0.22 BW; P = 0.04). Post hoc analysis revealed that these values in the LSF group were different from the HSF group (Fig. 1).
FIGURE 1: Peak TFJ anterior shear forces among runners with different SF. *Significant difference within the three groups. For peak TFJ anterior shear, post hoc analysis revealed that low and HSF groups were significantly different.
Peak TFJ compression force
There was a significant difference between the three SF groups for peak TFJ compression forces (LSF, −9.65 ± 1.13 BW; MSF, −9.22 ± 1.16 BW; HSF, −8.15 ± 1.12 BW; P = 0.01). Post hoc analysis revealed that the HSF group was significantly lower than the MSF and LSF groups (Fig. 2). Similarly, peak TFJ medial compartment forces differed among groups (LSF, −6.22 ± 0.91 BW; MSF, −6.02 ± 0.71 BW; HSF, −5.22 ± 0.79 BW; P = 0.01). Post hoc analysis revealed that values in the HSF group were lower relative to the MSF and LSF groups (Fig. 3).
FIGURE 2: Peak TFJ compression forces among runners with different SF. *Significant difference within the three groups. For peak TFJ compression forces, post hoc analysis revealed that low and HSF groups in addition to the middle and HSF groups were significantly different.
FIGURE 3: Peak TFJ medial compartment compression forces among runners with different SF. *Significant difference within the three groups. For peak TFJ medial compartment compression forces, post hoc analysis revealed that low and HSF groups in addition to the middle and HSF groups were significantly different.
DISCUSSION
The primary purpose of this study was to determine the differences in peak TFJ anterior shear and compression forces among female recreational runners with different self-selected SF. We hypothesized that, at a fixed pace, the group of runners with the highest SF would demonstrate lower peak TFJ anterior shear and compressive forces compared with the other groups. The results supported our hypothesis that running with an SF of ≥178 steps per minute was associated with a reduction in peak TFJ anterior shear and compressive forces.
No previous study to our knowledge has tested if different self-selected SF are associated with TFJ axial compression or shear forces in healthy female recreational runners. Cadence retraining via systematic manipulation of SL and SF at a constant speed has been demonstrated in previous studies to significantly alter knee joint kinematics and kinetics (14,15). Heiderscheit et al. (15) asked subjects to manipulate their SF at constant speed under various SF conditions (preferred, ±5%, and ±10%) using a digital audio metronome and demonstrated that the knee joint is most sensitive to changes in step rate. There was a significant reduction in energy absorption and mechanical work at the knee joint coupled with a decrease in peak knee flexion angle and knee extension moment (15). Lenhart et al. (16) showed that a 10% increase in SF at a fixed speed resulted in a significant decrease in patellofemoral joint loading and patellar tendon forces in healthy recreational runners. Both the above studies had similar running speeds to our study (2.8–2.9 m·s−1), and the 10% increased SF condition (174 ± 9 steps per minute) in the two studies (15,16) was comparable with the SF values of the MSF (172) and HSF (182) groups. Willy et al. (17) observed a decrease in peak TFJ contact forces by 9.1%, in 16 healthy runners with a 7.5% increase in step rate running at an average self-selected speed of 3.21 m·s−1. Boyer et al. (14) manipulated SL in recreational runners while they ran at 3.35 m·s−1 with 5% and 10% decrease in preferred SL generating a 3.2% and 7% decrease in TFJ axial forces. Our study demonstrates 18% lower peak TFJ shear and compression forces in healthy runners with naturally higher SF, without manipulating their SF, rather allowing them to run at their own self-selected SF.
One of the potential mechanisms that could explain the decrease in peak anterior TFJ shear forces in the MSF and the HSF groups would be decreased quadriceps force. A post hoc analysis of peak quadriceps force among the three SF groups revealed that the LSF group had significantly greater quadriceps force (LSF, 5.69 ± 0.88 BW; MSF, 5.49 ± 0.76 BW; HSF, 4.52 ± 0.81 BW; P = 0.01) compared with runners in the MSF and HSF groups, respectively. We also observed a significant decrease in peak knee extension moment with runners in the HSF group compared with the LSF and MSF groups (LSF, 0.97 ± 0.17 N·m·kg−1⋅m−1; MSF, 1.20 ± 0.15 N·m·kg−1⋅m−1; HSF, 1.21 ± 0.18 N·m·kg−1⋅m−1; P = 0.01). Bowersock et al. (27) observed a decrease in peak knee extension moment as one of the factors associated with lower quadriceps forces in individuals post anterior cruciate ligament surgery during running with a shortened SL. Our values of peak quadriceps forces were similar to the previous study. The quadriceps also contributes to anterior TFJ shear forces during functional activities (12,28). Contacting the ground with the knee in the range of 0° to 20° of knee flexion increases the anterior shear force at the proximal end of the tibia by increasing the angle between the patella tendon and the longitudinal axis of the tibia (28). Harding et al. (29) found that during walking in individuals with knee OA, peak quadriceps forces contributed to anterior shear force generation during the early stance phase. We did not find any differences between the three SF groups for knee flexion angle at initial contact (LSF, −16.19° ± 4.68°; MSF, −16.03° ± 4.75°; HSF, −15.57° ± 4.83°; P = 0.93) and or for foot strike pattern (LSF, 4.20° ± 6.05°; MSF, 6.55° ± 4.27°; HSF, 2.49° ± 5.17°; P = 0.08). Similarly, Bowersock et al. (13) concluded that the magnitude of TFJ forces during running is independent of foot strike pattern. The increase in SF also results in a decrease in posterior ground reaction forces (braking impulse), which may have contributed to the reduction in the knee extension moment, quadriceps force, and TFJ compressive forces in the MSF and HSF groups (30).
The increase in SF results in taking more steps per minute, which leads to cyclical compressive loading that may improve articular cartilage stiffness and proteoglycan synthesis (11). Decreased peak and cumulative compressive knee joint loading have been reported in response to increased SF while maintaining running velocity (13,14,17,27). The inverse association between self-selected SF and peak TFJ axial and anteroposterior forces during running observed in this study suggests that for a given velocity, individuals who run with a higher SF will routinely experience TFJ forces of lesser magnitude. Future studies should evaluate which load-related variables during running are central to joint health and how these variables relate to cartilage stresses and risk of knee OA in recreational runners.
The TFJ shear and compression forces estimates during running are reasonable relative to previously reported results. Peak TFJ anterior shear forces can range from 0.5 BW during walking to 2 BW for vertical jump landings (31). Our values ranged from 1.43 to 1.68 BW. Similarly, for TFJ compressive forces, studies during walking have reported values of 2.1–3.5 BW (18,29,32). Saxby et al. (32) calculated TFJ contact forces during functional activities and demonstrated that contact forces increased from walking (1–2.8 BW) to running (3–8 BW). Using this as a reference, our values of 8–9 times BW for peak compressive forces seems reasonable. Previous studies reported values of 11–15 BW for knee contact forces although their running speed was faster (4.25–4.4 m·s−1) compared with our speed of 2.98 m·s−1, which could potentially explain the difference (33). Miller et al. (34) reported contact forces of 8–9 times BW during running at 3.17 m·s−1 which is similar to our study.
Currently, there are no SF thresholds or standardized methods based on injury or performance to divide runners in different groups of SF’s. In a similar manner as Luedke et al. (35), we created SF groups by dividing our sample into tertiles. Our group sizes were slightly unbalanced partially because of runners using the same SF near the group cut points. Regardless, the SF tertile cut points were similar to Luedke et al. (35) but slightly higher, possibly due to our sample being all female or more experienced (36). Using these cut points, there is some evidence of a relationship between SF and running-related injury (35). Luedke et al. (35) prospectively followed high school cross-country runners throughout their season and concluded that runners with SF of ≤164 steps per minute had higher odds of experiencing a shin injury than runners with SF of ≥174 steps per minute. Future studies are necessary to determine whether SF is associated with knee injuries in adult runners, particularly those with risk factors for OA.
Limitations
There were significant differences for age between the three SF groups, but these differences did not seem to affect peak TFJ anterior shear and compression forces. The findings from our study report an association between SF and peak TFJ forces in female recreational runners and are not causal in nature. The values of peak TFJ anterior shear and compressive forces described in this study have been derived from biomechanical knee joint models that include limitations such as lack of subject specificity for muscle properties and the assumption of no hip flexor or ankle dorsiflexor cocontraction during stance phase. These limitations have been described in detail in other studies (37). We only included female participants who were recreational runners and those who did not present with history of any lower extremity injuries over the past 6 months, so it is unclear if these results are generalizable to elite runners, male runners, and/or runners with history of recent injuries. We did not assess the simultaneous effect of self-selected SF on hip and ankle joint axial forces, which could have been altered with decrease in forces at the TFJ. We recommend caution and monitoring when clinicians and coaches suggest running at higher SF. We calculated SF by counting the number of steps for 30 s and multiplying it by 2, which resulted in values being in even numbers only. We had one participant each with SF of 166 and 168 and three participants each with SF of 176 and 178. Because of the 2 step per minute SF resolution, participants right on the end points (166–168 and 176–178) may have been assigned to different SF groups had we used an SF measurement technique with higher resolution. We did not include data of five subjects from our study as their values were outside two standard deviations from the mean values resulting in a nonnormal distribution of data (see Table, Supplemental Digital Content 2, https://links.lww.com/MSS/B513). As seen in the supplemental data, similar trends were observed before removing outliers (see Table, Supplemental Digital Content 3, Values for peak TFJ anterior shear forces, peak TFJ compression forces, peak TFJ medial compartment compression forces for participants from the three step frequency groups eliminated from the study. §Indicates values outside two standard deviations from the mean, https://links.lww.com/MSS/B514). However, when using data from all participants, we did not find any statistically significant differences for peak anterior TFJ shear forces between groups.
CONCLUSIONS
Running is an appealing form of aerobic exercise and physical activity as it offers many health benefits. Thus, it is critically important to identify strategies that can protect individuals from stimuli that deter participation in running. This study demonstrated that female recreational runners with the highest SF experience lower TFJ anterior shear and compressive forces. Increasing running cadence may be an effective intervention to reduce knee joint contact forces in runners concerned about knee OA. However, future studies are necessary to confirm this association in female runners with or at risk for knee OA.
There was no funding received for this project. The authors have no conflicts of interests to disclose.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
The results of the study are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation.
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