Eric Magrum, Siobhan Statuta, David Hryvniak, and Robert Wilder
Running is one of the most common forms of exercise that is used by a wide variety of elite and recreational athletes. Nearly all sports involve some type of running, if not during play, then certainly as a part of training. The incidence of lower extremity running injuries ranges from 19.4% to 79.3% (1). The most common area of injury is the knee; other areas of injury from running include the shin, Achilles tendon, calf, heel, foot, hamstring, and quadriceps (1). Other chapters of this book describe the sex-specific difference in these lower extremity injuries. This chapter is dedicated to understanding the sex-specific differences of lower extremity biomechanics that may predispose an athlete to injury during running. Sex differences in static lower extremity alignment have been well described. Differences in static structure have been theorized to contribute to running injuries. Females generally have greater anterior pelvic tilt, femoral internal rotation, genus valgus, and recurvatum than males (2). More recently, sex-specific differences in running mechanics have been reported in the literature. The most consistent trend is with frontal and transverse plane hip and knee kinematics. Female runners most consistently demonstrate increased femoral adduction and internal rotation. In addition to kinematic differences, sex-specific differences in kinetics, spatiotemporal differences, muscle activation, and timing as well as pathomechanics have been reported. Controversy exists though, as not all studies support these differences between sexes. This chapter reviews the literature regarding sex-specific running mechanics and attempts to draw some meaningful clinical conclusions to guide the clinician in specific management of runners with musculoskeletal pain related to running pathomechanics.
BIOMECHANICS AND MOTOR CONTROL
Running requires a complicated series of muscle activations throughout a range of multiple joint motions occurring within the gait cycle. The gait cycle of running includes a stance phase (40% of the cycle) and a swing phase (30% of the cycle), but the main difference between running and walking is due to the period between stance and swing phases. In running, there are two float phases (15% of the cycle each) in which neither limbs are on the ground. During walking, the phase between stance and swing consists of a period of double support, where both limbs are in contact with the ground. Running is a complex process that cannot easily be summarized by one measure. Sex differences can exist at multiple levels of the biomechanics and motor control involved with running (see Figure 11.1 in the Conclusion section). A study with a comparatively large sample size (483 recreational and competitive runners) attempted to identify kinematic differences between the sexes to assist with improving the understanding of injury pattern differences (3). The authors reported their significant findings in each plane of movement and phase of the gait cycle. In the frontal plane, female runners demonstrated greater maximum and minimum peak hip adduction and knee abduction, greater hip adduction at initial contact, and greater hip adduction and knee abduction at terminal stance compared to males. Female runners also exhibited reduced peak ankle eversion compared to males. In the transverse plane, female runners exhibited greater external rotation of the femur at initial contact and maximum external rotation. In the sagittal plane, female runners exhibited lower minimum peak knee flexion, lower knee flexion at terminal stance, and lower peak ankle dorsiflexion compared to males (3).
Correlations between the sex differences in frontal and transverse motion and kinematics, muscle activation, and timing across various running speeds and inclines have been investigated (4). As with many previous studies, females displayed significantly greater peak hip internal rotation and adduction during stance, as well as hip adduction excursion compared to males. These differences were demonstrated at all walking and running speeds and surface inclinations. Females displayed significantly greater nonsagittal hip and pelvis motion during walking and running across a range of speeds and inclines, whereas sagittal motion at the hip was consistent between sexes.
Significant sex-specific muscle activity differences have been demonstrated. Gluteus maximus activity was consistently greater in females during walking and running. Gluteus maximus activity across the stride cycle in females was approximately twice that of males during all speed-incline conditions. Gluteus medius and vastus lateralis activity also differed in response to speed between sexes. A significant speed by sex interaction was present for gluteus medius and vastus lateralis activity across the stride cycle, particularly during terminal swing to initial loading of running, indicating females increased gluteus medius and vastus lateralis activity with speed to a greater extent than males. Males maintained a fairly consistent level of gluteus medius and vastus lateralis activity across running speeds, whereas females displayed a progressive increase in activity with speed. The sex-specific response of these muscles to changes in speed and incline supports the concept that as task challenge increases, males and females use different neuromuscular strategies. It appears that there are clear sex differences in hip kinematics and muscle activity across a variety of walking and running speeds and surface inclinations. Females display greater peak hip internal rotation and adduction as well as gluteus maximus activity for all walk and run conditions, are likely working at a greater percentage of maximum, and therefore are possibly more susceptible to the effects of fatigue (4,5).
Sex differences with gluteal muscle activation and timing have also been correlated with kinematic and kinetic measurements (4,5). No difference in gluteus medius or gluteus maximus activation timing was noted between males and females while running. However, differences were identified in gluteal muscle activation levels between male and female during running. Normalized gluteus maximus peak activation level was 40% greater and the average activation level was 53% greater in females compared to males. Associated kinematic differences between males and females were also observed. Females made initial contact with the running surface with 4.0° more hip adduction and 2.8° more knee abduction compared to males. Females also demonstrated 5.1° greater hip adduction at peak vertical ground reaction force. The authors concluded that these results highlight the relative importance of the gluteus maximus compared with the gluteus medius to the sex bias for patellofemoral pain syndrome (PFPS) and related sex-specific pathomechanics. They theorize that greater gluteus maximus activation levels in females during running may lead to the earlier onset of fatigue in females compared to males, thereby reducing their force-generating capacity following exertion. A reduction in gluteus maximus force during prolonged running may promote aberrant hip and knee joint kinematics and greater retropatellar stress. If premature gluteus maximus fatigue is expected among females during a prolonged run, hip extension (gluteus maximus) endurance training may be warranted in efforts to prevent altered hip kinematics (increased hip internal rotation or adduction) that may contribute to increased patellofemoral joint stress and PFPS (4). Conversely, females demonstrated lower levels of fatigue in knee extensors and plantar flexors during ultra-running. It is suggested that this could contribute to the relatively improved performance of females during ultra-running compared to shorter distances (6).
Sex differences have been reported in pelvic and thoracic coupled motions. Female runners demonstrated greater pelvic obliquity and thoracic axial range of motion as well as greater pelvic tilt and anterior lean compared to male runners (7). Relationships between pelvic and thoracic motion and hip strength have also been reported (7). At all running speeds, as hip abductor strength increased, pelvic obliquity motion decreased. As hip extensor strength increased, thoracic axial rotation range of motion (ROM) decreased during all running speeds. The authors discuss clinical implications based on the biomechanical coupling, discussing that it is likely that internal femoral rotation, femoral adduction, pelvic tilt, and thorax axial rotation exhibit some form of coupling during stance. They discuss that during initial ground contact during running, the trunk is near maximum posterior axial rotation on the contralateral side of the stance limb and then undergoes maximum forward rotation near terminal stance. If the sex-prevalent pathomechanics of femoral internal rotation and adduction increases through stance phase, the thorax will have increased rotation at terminal stance to maintain forward-directed motion. This might result in increased thoracic transverse plane rotation with decreased hip strength.
Researchers have identified spatiotemporal sex differences in the three-dimensional angular rotations of the lumbopelvic-hip complex during running (8). Females displayed shorter stance time, swing time, stride time, and stride length and a higher stride rate than males. Females also tended to begin hip flexion immediately before toe-off, whereas males remained in hip extension for a short period during the initial swing. Regarding kinematic differences, there were significant differences throughout the lumbopelvic-hip complex in all planes of movement at various points of the running gait cycle. Females tended to display a greater peak-to-peak oscillation for most of the angular rotations (8). At the hip in the sagittal plane, females tended to have a greater angle of peak hip flexion during the latter third of swing and a greater amplitude of frontal plane hip adduction-abduction than their male counterparts. At the lumbar spine, females displayed significantly greater amplitudes of lumbar spine frontal plane side bending and transverse plane axial rotation. At the pelvis, females demonstrated greater frontal plane anterior-posterior pelvis tilt, frontal plane obliquity, and transverse plane axial rotation. Females statically stood with a greater anterior pelvic angle, ran with a greater sagittal plane pelvic excursion, and ran with a greater average position of anterior pelvic tilt compared to males throughout the entire gait cycle.
Sex-specific kinetic differences have been described. Most specifically, females have demonstrated greater knee loading than males (9). Females have demonstrated greater knee extensor moments, greater patellofemoral forces and loading rates, and increased patellofemoral contact pressures than males (10,11,12). Females have also demonstrated higher initial peak hip adduction moments, lower ankle plantar flexor moments, and lower Achilles tendon loads than males (13,14,15).
COMMON CLINICAL SYNDROMES
Kinematic and kinetic differences have been proposed to contribute to running injuries, most specifically patellofemoral pain syndrome, iliotibial band syndrome, and stress fractures. One of the most widely studied of these injuries is PFPS. Females are twice as likely to experience PFPS compared with males (16). Female U.S Naval Academy recruits were 25% more likely to have a history of PFPS than males, and female recruits were more than twice as likely to subsequently develop PFPS as males (17). Recent studies have suggested that abnormal hip and knee mechanics are associated with PFPS in females (12,18,19,20,21,22). These abnormal mechanics include excessive peak contralateral pelvic drop, peak hip adduction (5,18,23), peak hip internal rotation (14,18,24), decreased peak knee adduction (11,21,22), and increased tibial rotation (11). In combination, these motions result in dynamic valgus of the knee, resulting in lateral patellar tracking and an increase in the loading forces on the lateral aspect of the patellofemoral joint (10,11,19,20,25). Importantly, these abnormal mechanics appear to be present in females with PFPS across a variety of activities, including both running and during a single leg squat (14,18,22,23,24,26). Willy et al. also reported that females with patellofemoral pain performed a single leg squat and ran with greater femoral adduction when compared with the males with patellofemoral pain (22).
The precise kinematics and kinetics behind the incidence of patellofemoral pain in female runners, however, are not consistent across the literature and remain ambiguous. A recent study recognized the discrepancies in the literature and investigated the patellofemoral joint loads produced by female runners in contrast to males in order to gain further insight into the increased incidence of patellofemoral disorders in females (9). The authors used musculoskeletal modeling to calculate patellofemoral joint forces and pressures from healthy males and females to determine sex differences. Their results add to the body of knowledge regarding forces acting on the patellofemoral joint and assist in drawing clinical conclusions to guide sex-specific exercise prescription and gait training. Females exhibited significantly greater peak knee extensor moments compared to males. Females also had greater patellofemoral force and patellofemoral force load rates, significantly increased patellofemoral contact pressures, and significantly increased peak knee abduction moment compared to healthy males.
It is theorized that several mechanisms may serve to explain the increased forces, related moments, and kinematic findings that are fairly consistent across the literature. Female runners have been associated with hip musculature weakness and lack of neuromuscular control at the knee joint during dynamic activities. Related studies examining landing mechanics have also associated weakness of the hip musculature to a compensatory strategy whereby landing mechanics in females relied more heavily on the knee extensor moment to absorb impact forces (15). Female runners have also been shown to exhibit reduced ankle plantar flexor moments and Achilles tendon loads in comparison to males. Enhanced plantar flexion from the ankle joint may be a sex-specific mechanism by which the loads at the knee joint are reduced in male runners (13). Female recreational runners exhibit significantly greater knee loading compared to males. Given the proposed relationship between knee joint loading and patellofemoral pathology, the current investigation does appear to provide some insight into the high incidence of patellofemoral pain in females (9).
Iliotibial band syndrome (ITBS) is another common running injury where frontal and transverse plane pathomechanics have been shown to be related to injury etiology. Female runners with ITBS have exhibited significantly greater peak hip adduction, knee internal rotation angles, and peak rearfoot invertor moment compared with healthy controls (27,28). Transverse plane kinematic differences in male and female runners with ITBS have been described. Female runners with ITBS demonstrated significantly greater hip external rotation angles during 52% to 54% (and meaningful differences during 23% to 60%) of the running gait cycle as compared to male runners with ITBS. A different running kinematic profile was also found for female and male runners with ITBS in comparison to sex-matched healthy controls. Specifically, female ITBS runners exhibited significant differences in transverse plane hip kinematic gait patterns while male ITBS runners exhibited significant differences in transverse plane ankle kinematic gait patterns as compared with their respective healthy counterparts. The authors therefore conclude that clinicians treating female runners with ITBS should focus on proximal muscle strengthening programs, whereas male runners should focus on distal muscle strengthening programs to prevent ITBS injury (27).
Spatiotemporal sex differences, particularly in the three-dimensional angular rotations of the lumbopelvic-hip complex during running, are felt related to the higher incidence of pelvic and femoral stress fractures in females than males. In one prospective study of high-level track and field athletes, Bennell et al. found pelvic and femoral stress fractures only in female track and field athletes, mostly mid-distance and long-distance runners (29).
Taunton et al. reported similar rates of overuse Achilles tendon injuries in male (8% of running injuries) and female (10% of running injuries) runners (16). Overall, however, males experience a greater number of Achilles tendon injuries compared to females at a rate of 2:1 to 12:1 (13,30,31,32,33).
This discrepancy between the sexes may be related to a greater level of participation in ball sports by males (13,34). Increased Achilles tendon loading in males compared to females may also predispose to Achilles tendon injury (13). Males have demonstrated a greater peak plantar flexion moment and Achilles tendon loading than females during running. Additionally, average and instantaneous Achilles tendon loading rates were significantly greater in male runners (13). The greater Achilles tendon loading and loading rates may contribute to the greater rate of Achilles injury reported in males. Higher stiffness of the plantar flexor muscles and Achilles tendon, evidenced by lower active elasticity, has been reported in men compared with women and has also been theorized to contribute to the higher incidence of Achilles tendon injury in men (35).