Background
The frequent occurrence of stress-fracture injuries during basic combat training (BCT) remains a leading concern for the United States (US) military [
1]. Epidemiological studies have shown that the most commonly injured sites for stress fractures include the tibia, femoral neck, tarsal navicular, metatarsals, and pelvis [
2‐
4]. Stress fractures are caused by repeated application of sub-critical mechanical insults associated with common BCT exercises, including walking, running, and jumping [
1,
5‐
7]. Furthermore, military personnel are often required to carry loads that reach a considerable percentage of their body weight, which have been shown to be associated with an increased risk of stress fracture [
8,
9]. To understand the impact of load carriage and ultimately help reduce the risk of stress fracture, previous studies have examined systematic changes in metabolic parameters (e.g., energy cost) [
10‐
12], ground reaction forces (GRFs) [
13], joint kinematics [
10,
14], and muscle activities [
15] due to load carriage. However, the effects of load carriage on bone biomechanical responses (e.g., bone stress and strain), which play a crucial role in bone health, have been less extensively investigated.
The technical challenges and ethical restrictions associated with implanting strain gauges make it impractical to experimentally measure bone strains in healthy individuals [
16]. Therefore, computational methods have been implemented in recent years to quantify mechanical bone stress and strain [
17]. For example, our group has developed an integrated musculoskeletal-finite-element (FE) modeling framework and used it to quantify the impact of load carriage during walking in a woman [
18] on a number of measures, including joint kinematics, joint kinetics (joint reaction forces or JRFs), and biomechanical responses of the tibia (i.e., spatiotemporal stress distribution, and its cumulative effect during one gait cycle).
Previous studies have shown that the muscles involved during walking and running are almost identical, and that switching from walking to running is associated with changes in both the timing and intensity of muscle activation [
19]. However, our understanding of how the body adjusts its kinetics, kinematics, and biomechanics over a range of load carriages during running remains fragmentary. Here, we sought to answer the following research question: how do the joint angles, JRFs, and tibial mechanical stresses change in response to load carriage when women run at their preferred speeds? We hypothesized that:
1) running with load carriage would increase both peak JRFs and the percentage of the tibial volume subjected to high stress and
2) the changes in JRFs and tibial stress would not be proportional to the change in load carriage.
Discussion
We performed integrated musculoskeletal-FE simulations to emulate the effects of load carriage on joint kinematics, joint kinetics, tibial mechanical stress, and cumulative tibial stress per gait cycle in four women running at their preferred speeds. We chose the tibia as the bone of interest because it is the most frequently injured site in athletes [
29‐
31] and military recruits [
32]. We chose female subjects because of the growing number of women serving in the Army [
33]. As are their male counterparts, women are required to wear body armor and carry heavy loads averaging 45.5 kg [
34]. Consequently, they are at a higher risk for developing stress-fracture injuries than are men [
33].
In support of our first hypothesis, both the peak JRFs and the percentage of the tibial volume subjected to high stresses and cumulative stresses per cycle increased with an increase in load carriage. It is noteworthy that the fraction of tibial volume subjected to pre-defined stress thresholds changed in response to load carriage in a non-monotonic manner. Specifically, carrying a 30% BW load increased the average peak JRFs of the ankle, knee, and hip by 4.8%, 20.6%, and 49.1%, respectively, when compared with the baseline condition (Table
1). The tibial volume subjected to stresses between 4.7 MPa and 17.8 MPa increased from 25.0% for the baseline condition to 25.8% for a 20% BW and 29.4% for a 30% BW load carriage, whereas that subjected to stresses greater than17.8 MPa increased from 25.0% for the baseline condition to 27.2% for 20% BW but only to 25.7% for 30% BW load carriage. This might be the result of the quadratic muscle-recruitment criterion adopted in the model, because such a mechanism, which tends to recruit more muscles during high-intensity tasks, distributes the load among several muscles spanning the joint to prevent a few muscles from being overloaded and consequently undergoing muscle fatigue [
21]. Overall, the percentage changes in the JRFs, tibial peak stress, and cumulative stress were disproportional to that of the load carriage, consistent with our second hypothesis.
Our results showed that both the kinematics and kinetics of the hip changed substantially during running with load carriage. When compared with the baseline condition, carrying a 30% BW load decreased the mean peak hip extension at toe off by 54.7% and increased the mean peak hip flexion and extension moments by 10.0% and 62.5%, respectively, in addition to increasing the mean peak hip JRFs (49.1%, Table
1). These results highlight the importance of hip muscles in high-intensity physical activity (e.g., running with load carriage), and are supported by previous studies linking them with sports injuries. For example, in collegiate female athletes with patellofemoral injury, hip abductors and external rotators are significantly weaker in the injured leg than in the unaffected leg [
35]. Furthermore, if the hip extensors do not generate enough power, either other muscles in the lower extremities will compensate for the reduced force, or movement patterns will change, which in turn may result in increased energy costs and early muscle fatigue [
36]. Such changes may be related to a number of biomechanical alterations that potentially increase the risk of impact-related injuries in the lower extremities (e.g., Achilles tendinosis, patellofemoral dysfunction, and tibial stress fracture) [
37]. Preparatory strength and endurance training exercises before military BCT, such as squats, incline sit-ups, leg raises, and interval training, which are designed to strengthen hip flexor muscles and pelvic-stabilizing muscles (gluteus medius), are effective in assisting prospective Service members to endure BCT without injuries [
38].
Consistent with telemeterized bilateral joint-replacement studies [
39,
40], our findings suggest that, for the subject who completed both walking [
18] and running experiments, the peak running JRFs were more than two times greater than the peak walking JRFs, with the contribution from the hip muscles increasing during running with load carriage. Specifically, when running without a load, the knee experienced the highest JRF (15.8 BW vs. ankle, 11.3 BW; hip, 12.2 BW) for the subject who completed both walking and running experiments. In contrast, when walking without a load, her ankles were exposed to the highest JRF (4.7 BW vs. knee, 4.4 BW; hip, 4.3 BW). Carrying a 30% BW load increased her JRFs at the hip by 35.2% (ankle, 6.2%; knee, 20.1%) during running, as compared to an increase of 26.2% in her knee JRFs (ankle, 16.4%; hip, 19.0%) during walking [
18]. Although this subject ran substantially slower than the others, her running speed (3.0 m/s) was still well above the preferred transition speed between walking and running for nonrunners [2.01 (SD = 0.07) m/s] and runners [2.06 (SD = 0.07) m/s] [
41]. Moreover, we observed the same trend in all running participants: the JRF at the knee was greater than that at the ankle or hip under the baseline running condition, whereas the hip JRF was more sensitive and increased markedly as the load carriage increased. The relatively small increase in the peak ankle JRFs in response to load carriage during running reflects the lower degree of the plantarflexor involvement in forward movements when running than when walking [
18]. Likewise, the increase in hip JRFs associated with load carriage during running suggests that compared with walking, running requires a relatively greater contribution from the hip extensors to meet the increased mechanical and energetic demands of the leg [
42].
For the subject who completed both walking [
18] and running experiments, the tibial stress during running was substantially different from that during walking. For the baseline condition, the peak running tibial stress (tension, 90.6 MPa; compression, 136.2 MPa) was more than three times greater than the peak walking tibial stress (tension, 24.1 MPa; compression, 40.3 MPa). Surprisingly, the cumulative stress per cycle for walking (13.6 MPa · s) was 88% of that for running (15.2 MPa · s). A one-time elevation of the peak JRF or tibial stress does not necessarily increase the risk of stress fracture, because elevated mechanical loading is only one factor that contributes to stress-fracture injuries. The total cumulative stress, which is affected by the duration of the stance (i.e., of foot-ground contact time) and is much shorter in running than in walking [
43], plays a major role in the biomechanical and biological responses of bone, as do the total time and frequency of training [
1].
During BCT, military recruits on average run 36 min and march 129 min a day, depending on their company and initial fitness level [
44,
45]. Assuming that a BCT recruit adopts a common step frequency of 60 steps/min for walking and a recommended step frequency of 180 steps/min for running [
46], the peak cumulative tibial stress to complete a 36-min running distance reaches 98,496 MPa · s [15.2 (cumulative stress per running cycle) × 180 × 36], and that to complete a 129-min walking distance reaches 105,264 MPa · s [13.6 (cumulative stress per walking cycle) × 60 × 129]. When carrying a 30% BW load under these conditions, the daily cumulative stress due to 36 min of running is 83.3% of that due to 129 min of walking. In other words, the biomechanical impact on the tibia resulting of marching for 129 min is equivalent to that of running for 43 min when the individual carries a 30% BW load. The relatively shorter duration of ground contact in running presumably offsets the effect of the high tibial stress per stride. This is an important finding because, while Service members are not encouraged to run while carrying heavy loads during military training, they are required to complete long-distance tactical foot marches carrying mission-essential equipment (up to 25 kg or 45% BW), which, in essence, leads to the same cumulative stress as a short run with load. If the cumulative effect of internal forces and bone stresses increases the risk of stress-fracture injury, our results suggest that BCT recruits could be more prone to injury when marching an excessive distance than when running a short distance.
One major limitation of the present study stems from the simplifications and assumptions made to construct the model. For example, the knee joint in the current model does not include medial and lateral compartments of joint loads, nor does it fully incorporate complex three-dimensional motions, including translations and rotations. In the absence of medical images necessary for reconstructing subject-specific tibial geometrical structures for FE analyses, we used anthropometric measurements to scale a 50
th percentile European female generic musculoskeletal model. Similarly, given that all participants were young and healthy (i.e., ~30 years old), we used tibial material properties mapped from a BMI-matched subject of the same sex for the FE analysis. This approach, along with the use of assumptions regarding material properties (e.g., linear elasticity and isotropy) may affect tibial stress/strain predictions. Furthermore, we chose an effort-based cost function to solve the muscle redundancy problem in the musculoskeletal model. Although this commonly used method predicted patterns of muscle activation qualitatively similar to those of the EMG recordings, it is not suitable for predicting subject-specific muscle activities. This is evident from the discrepancy between the predictions and EMG recordings in the tibialis anterior activation at toe off and rectus femoris activation during early swing (Fig.
2). Lastly, although we quantified the biomechanical alterations during running with load carriage, we only assessed acute effects and did not test for a cause-and-effect relationship between load carriage and stress fracture. Therefore, until more research is conducted in this area, we believe it is premature to identify a correlation between our results and clinically observed injury sites.
Acknowledgements
We thank Dr. Tatsuya Oyama for editorial assistance. We also acknowledge the high-performance computing resources made available by the US Department of Defense High Performance Computing Modernization Program at the Air Force Research Laboratory.