TZU-CHIEH LIAO1, NICHOLAS YANG2, KAI-YU HO3, SHAWN FARROKHI4, and CHRISTOPHER M. POWERS1 1 Jacquelin Perry Musculoskeletal Biomechanics Research Laboratory, Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, CA; 2Guidance, Engineering and Applied Research, Seattle, WA; 3Department of Physical Therapy, University of Nevada, Las Vegas, NV; and 4Department of Physical Therapy, University of Pittsburgh, PA
ABSTRACT LIAO, T.-C., N. YANG, K.-Y. HO, S. FARROKHI, and C. M. POWERS. Femur Rotation Increases Patella Cartilage Stress in Females with Patellofemoral Pain. Med. Sci. Sports Exerc., Vol. 47, No. 9, pp. 1775–1780, 2015. Purpose: This study aimed to test the hypothesis that internal rotation of the femur increases patellofemoral joint stress in persons with patellofemoral pain (PFP). Methods: Patella cartilage stress profiles of nine female participants with PFP were obtained during squatting using subject-specific finite element (FE) models of the patellofemoral joint (15- and 45- of knee flexion). Input parameters for the FE model included joint geometry, quadriceps muscle forces during squatting, and weight-bearing patellofemoral joint kinematics. The femur of each model was then internally rotated 5- and 10- along its long axis beyond that of the natural degree of rotation. Using a nonlinear FE solver, quasistatic loading simulations were performed to quantify patellofemoral joint stress. Results: Compared with those at the natural position of the femur, mean hydrostatic pressure and mean octahedral shear stress were significantly higher when the femur was internally rotated 5- and 10-. No significant differences in stress variables were observed when the femur was rotated from 5- to 10-. These findings were consistent across both knee flexion angles (15- and 45-). Conclusions: The finding of elevated hydrostatic pressure and octahedral shear stress with internal rotation of the femur supports the premise that females with PFP who exhibit abnormal hip kinematics may be exposed to elevated patellofemoral joint stress. Key Words: ARTICULAR CARTILAGE, FINITE ELEMENT ANALYSIS, FEMUR INTERNAL ROTATION, PATELLOFEMORAL PAIN
P
It has been reported that the primary cause of increased patellofemoral joint stress in persons with PFP is decreased contact area associated with abnormal patella alignment and/ or maltracking (8,37). Recent research has suggested that patellofemoral joint maltracking in weight bearing is the result of excessive femur internal rotation as opposed to abnormal patella motion (31,34). In addition, biomechanical studies have shown that persons with PFP exhibit a greater degree of hip internal rotation during functional activities such as running, jumping, and stepping when compared with that in healthy individuals (2,26,28,29,35,38). In support of the premise that excessive hip internal rotation may contribute to the development of PFP, experimental studies have shown that internal rotation of the femur relative to the tibia increases patellofemoral joint stress. Using a cadaveric model, Lee et al. (22,23) observed a nonlinear increase in contact pressure on the lateral facet of the patella when the femur was internally rotated to 20- and 30- at knee flexion angles of 30-, 60-, 90-, and 120-. However, Besier et al. (4) reported no changes in patellofemoral cartilage stress using finite element (FE) analysis when the femur was internally rotated to 5-, 10-, and 15- at a knee flexion angle of 60-. In the study of Besier et al. (4), only 35% of subjects experienced a 10% increase in contact stress when the femur was rotated to 15-. The contrasting findings of Lee et al. (22,23) and Besier et al. (4) may be explained by the different knee flexion
atellofemoral pain (PFP) is a common condition seen in orthopedic practice. For example, PFP is the second most common lower extremity diagnosis and accounts for approximately 25%–40% of all knee injuries (13,36). In addition, women have a 2.2 times higher incidence of PFP when compared with that in men (6). A commonly cited hypothesis as to the cause of PFP is increased patellofemoral joint stress (7,8,37). Studies have reported that persons with PFP exhibit elevated patellofemoral joint stress during walking and running and greater patella and femur cartilage stresses during squatting when compared with those in pain-free individuals (3,15). Although cartilage is aneural (32), increased cartilage stress has been shown to lead to increased subchondral bone stress, which has been proposed to be a source of retropatellar pain (19).
Address for correspondence: Christopher M. Powers, P.T., Ph.D., F.A.C.S.M., F.A.P.T.A., Jacquelin Perry Musculoskeletal Biomechanics Research Laboratory, Division of Biokinesiology and Physical Therapy, University of Southern California, 1540 E. Alcazar St., CHP-155, Los Angeles, CA 90089-9006; E-mail: [email protected]. Submitted for publication July 2014. Accepted for publication January 2015. 0195-9131/15/4709-1775/0 MEDICINE & SCIENCE IN SPORTS & EXERCISEÒ Copyright Ó 2015 by the American College of Sports Medicine DOI: 10.1249/MSS.0000000000000617
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Femur Rotation Increases Patella Cartilage Stress in Females with Patellofemoral Pain
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angles and femur rotation angles evaluated. Besier et al. (4) examined the influence of femur internal rotation at rotation angles of 5-, 10-, and 15-, whereas Lee et al. (21,22) evaluated much higher rotation angles, 20- and 30-. Souza et al. (34) have reported that femur rotation angles in persons with PFP during a single-leg squat range from 4- to 12-, suggesting that the femur rotation angles evaluated in the studies of Lee et al. (22,23) may not have been physiologically possible. However, Besier et al. (4) evaluated the influence of femur rotation at a relative high knee flexion angle (60-). This is problematic because Souza et al. (34) have reported that internal rotation of the femur in persons with PFP is more pronounced as the knee extends from 45- to full knee extension. The influence of femur internal rotation on patellofemoral joint stress may be more pronounced at lower knee flexion angles. Given the limitations of previous research in this area, the purpose of the current study was to determine the influence of femur internal rotation on patella cartilage stress in females with PFP. For purposes of this study, we evaluated physiological degrees of femur rotation (5- and 10-) at relatively small knee flexion angles (15- and 45-). Using a subjectspecific FE modeling approach, we hypothesized that patella cartilage stress would increase with greater degrees of femur rotation. Information gained from this study will clarify the role of femur rotation in contributing to patellofemoral joint stress.
METHODS Subjects. Nine female participants with a diagnosis of PFP participated in this study. The average age, height, and weight of the participants were 27.7 T 4.3 yr, 1.7 T 0.1 m, and 63.3 T 8.4 kg, respectively. Before participation, all subjects were informed as to the nature of the study and signed a human subject’s consent form approved by the Healthy Sciences Institutional Review Board of the University of Southern California. Individuals with PFP were admitted to the study if their pain originated from behind the patella (i.e., retropatellar pain). Only subjects that reported an insidious onset of symptoms were accepted. Subjects were screened through physical examination to rule out evidence of large knee effusion and peripatellar pain. The screening procedure also included a functional assessment of activities commonly associated with PFP (squatting, stair climbing, and isometric quadriceps contraction). Subjects were included in the study if they reported pain of at least 3 out of 10 (based on a visual analog scale) with one or more of the aforementioned functional tasks. Individuals with PFP were excluded from participation if they reported any of the following: 1) history of knee surgery, 2) history of traumatic patella dislocation, 3) neurological involvement that would influence performance of functional activities, and 4) implanted biological devices that could interact with the magnetic field of the MRI. Procedures. Subjects completed two data collection sessions. The first session consisted of magnetic resonance
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(MR) assessment of the knee and patellofemoral joints, whereas the second session consisted of biomechanical testing. For all subjects, testing was performed on the painful side. In cases of bilateral pain, the more symptomatic limb was evaluated. MR assessment. Subject-specific cartilage morphology and bone geometry of the knee and the patellofemoral joints were obtained using a 3.0-T MR scanner (General Electric Healthcare, Milwaukee, WI). Images were acquired with an eight-channel knee coil using a three-dimensional (3D), highresolution, fat-suppressed, fast spoiled gradient recalled echo (SPGR) sequence (repetition time, 14.5 ms; echo time, 2.8 ms; flip angle, 10-; matrix, 320 320; field of view, 16 cm; slice thickness, 1.0 mm; scan time, 8:58 min). During this scan, subjects were positioned supine with the knee extended. To obtain the relative weight-bearing orientations of the patella, femur, and tibia, a custom-made nonferromagnetic loading apparatus providing a force equivalent to 25% of subjects’ body weight was used. Loaded MR images of the subjects’ knees were acquired at 15- and 45- of knee flexion using a 3D, fast SPGR sequence (repetition time, 14.3 ms; echo time, 3.6 ms; flip angle, 10-; matrix, 320 160; field of view, 16 cm; slice thickness, 2.0 mm; scan time, 1:45 min). Quadriceps muscle morphology was assessed from sagittal plane MR images of the thigh using a 3D SPGR protocol (repetition time, 9.4 ms; echo time, 4.1 ms; flip angle, 20-; matrix, 384 384; field of view, 46 cm; slice thickness, 2 mm; scan time, 8:03 min). The sagittal plane images of the thigh were subsequently reconstructed in the coronal and axial planes and were used to estimate the 3D fiber orientation of each of the quadriceps muscles (see next section for details). The axial images of the thigh were used to measure the cross-sectional area of the quadriceps muscles, which was subsequently used as an input variable for the biomechanical model to estimate the magnitude of muscle forces. Biomechanical testing. Subjects were instrumented for 3D motion and EMG analyses as described in previous publications (8,37). Lower extremity kinematics was collected using an eight-camera motion analysis system at 60 Hz (Vicon; Oxford Metrics Ltd., Oxford, England). Ground reaction forces were recorded at a rate of 1560 Hz using two AMTI force plates (model #OR6-6-1; Newton, MA). EMG signals of muscles crossing the knee joint (see next section for details) were recorded at 1560 Hz using preamplified, bipolar surface electrodes (Motion Lab Systems, Baton Rouge, LA). After a standing calibration trial, subjects were asked to hold a bilateral squat position at 15- and 45- of knee flexion, with each foot positioned on a separate force plate. To account for the influence of the trunk position on the lower extremity demands during weight bearing (16), the subjects’ trunk position was controlled by asking the subjects to flex their knees to the desired angle while keeping fingertip contact with the pole placed at arm’s length. While holding the desired squatting position, kinematic, kinetic, and EMG data were recorded. These information were used for estimation of quadriceps muscle forces, which was required as an input variable in the FE model.
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the femur (25). As described in a previous publication (12), the most lateral and medial borders of quadriceps line of pull (i.e., the vastus lateralis and vastus medialis) were determined from the sagittal and frontal plane fiber orientation of each muscle as measured from MR images of the subject’s thigh. Six connector elements representing each muscle group were then distributed uniformly from the medial to lateral borders. In addition, six uniaxial tension-only elements with total stiffness of 4334 NImmj1 were used to represent the patella tendon, which connected the patella and the tibia (18). Simulations were performed using a hard contact algorithm with a surface coefficient of friction of 0.02 (3). Quasistatic loading simulations were performed using a nonlinear FE solver (Abaqus; SIMULIA, Providence, RI). For all simulations, the bony structures (i.e., femur, tibia, and patella) were modeled as rigid bodies. The initial orientations of the bony rigid bodies were determined from the weight bearing MR images. To obtain the weight-bearing positioning of the patella, femur, and tibia at 15- and 45- of knee flexion, the FE mesh of each bone was registered to the corresponding bony surfaces obtained from the weight bearing images. To simulate a stable weight bearing condition, the femur and tibia were fixed in space. To examine the influence of internal rotation on cartilage stress, the femur was rotated 5- and 10- along its long axis beyond that of the natural degree of rotation. This procedure was repeated at 15- and 45- of knee flexion. To represent an initial unloaded condition, the patella was moved anteriorly to create a gap between the articulating surfaces of the patellofemoral joint. Because the soft tissues controlling the rotation of the patellofemoral joint were not included in the models, the three rotational degrees of freedom of the patella were constrained.
FIGURE 1—Subject-specific input parameters used to create FE models of the patellofemoral joint.
FEMUR ROTATION PFP
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FE model development. Subject-specific input parameters entered into the modeling pipeline included the following: joint geometry, quadriceps muscle forces, and weight-bearing patellofemoral joint kinematics (Fig. 1). Using a commercial software package (Sliceomatic; Tomovision, Montreal, Quebec), the high-resolution sagittal plane MR images of the knee were manually segmented and 3D surfaces of the femur, tibia, patella, and articular cartilage covering of the femur and patella were created. Surfaces created for the femur, tibia, and patella were subsequently used to create rigid body shells of each bony structure using a proprietary FE preprocessor (Hypermesh; Altair Engineering Inc., Troy, MI). The articular cartilage of the patella and femur was modeled as homogeneous isotropic tetrahedral continuum elements with an elastic modulus of 4.0 MPa (14) and a Poisson ratio of 0.47 (3). An average element size of 0.75 mm was used because a previous convergence analysis revealed that decreasing the element size did not result in a meaningful change in stress but resulted in longer computational time for the simulation (15). The methods used to estimate the individual quadriceps muscle forces from the biomechanical testing session have been described previously (12). Briefly, a subject-specific representation of the extensor mechanism was created using the SIMM modeling software (MusculoGraphics, Santa Rosa, CA). Subject-specific biomechanical data (kinematics, kinetics, and EMG) were used to drive the model (via an optimization routine), and 3D quadriceps muscle forces were computed. The elements representing the quadriceps muscles were separated into three functional groups made up of six equivalent uniaxial force actuators (the rectus femoris/vastus intermedius, vastus medialis, and vastus lateralis muscles). The direction of muscle line of pull for the rectus femoris/ vastus intermedius group was set parallel to the long axis of
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Model output and postprocessing. Articular cartilage stress was quantified in terms of two invariants, as follows: 1) hydrostatic pressure and 2) octahedral shear stress (9–11). As scalar parameters, hydrostatic pressure and octahedral shear stress represent different aspects of the stress field (10). Hydrostatic pressure reflects the magnitude of the portion of the stress tensor that tends to uniformly compress the cartilage, whereas octahedral shear stress reflects the portion of the stress field that tends to distort the tissue (10). A mesh surface was created to represent the chondroosseous interface by selecting the element faces of the tetrahedral elements that were adjacent to the subchondral bone surface. The stress values were estimated at the centroids of cartilage element faces closest to the bone. Elements with only one node at the interface were not included in the analyses. To establish a clinically meaningful measure of mean patella hydrostatic pressure and octahedral shear stress, only elements with stress values above a threshold of 271 kPa were considered when calculating the mean stress. This threshold corresponds to the minimum bone stress–pain threshold previously established for healthy subjects (33). Statistical analyses. To test the hypothesis that cartilage stress differed between femur rotation angles, a 3 2 ANOVA with repeated measures was performed (femur rotation angle knee angle). This analysis was repeated for mean hydrostatic pressure and mean octahedral shear stress of the patella cartilage elements at the chondroosseous interface. For all ANOVA tests, significant main effects were reported if there were no significant interactions. For all statistical tests, the alpha level was set at 0.05.
significant interaction (P = 0.77). However, the main effects for femur rotation angle and knee flexion angle were significant (P = 0.02 and P G 0.01, respectively). When collapsed across knee flexion angles, mean octahedral shear stress was significantly higher with the femur rotated to 5and 10- when compared with that at natural degree of rotation (Table 2). There were no significant differences in mean hydrostatic pressure between the 5- and 10- femur rotation conditions. When collapsed across femur rotation angles, the mean octahedral shear stress was significantly higher at 45- knee flexion when compared with that at 15- knee flexion (Table 1).
DISSUSSION
The ANOVA comparing mean hydrostatic pressure across femur rotation and knee flexion angles did not reveal a significant interaction (P = 0.59). However, the main effects for femur rotation angle and knee flexion angle were significant (P = 0.01 and P = 0.02, respectively). When collapsed across knee flexion angles, mean hydrostatic pressure was significantly higher with the femur rotated to 5- and 10- when compared with that at natural degree of rotation (Table 1). There were no significant differences in mean hydrostatic pressure between the 5- and 10- femur rotation conditions. When collapsed across femur rotation angles, mean hydrostatic pressure was significantly higher at 45- knee flexion when compared with that at 15- knee flexion (Table 1). The ANOVA comparing mean octahedral shear stress across femur rotation and knee flexion angles did not reveal
The purpose of this study was to evaluate whether internal rotation of the femur results in elevated patella cartilage stress in females with PFP. Two scalar invariants, hydrostatic pressure and octahedral shear stress, at the chondroosseous interface of the patella were used to quantify articular cartilage loading. Consistent with our hypothesis, patella cartilage stress was significantly higher when the femur was internally rotated 5- and 10- beyond that of the natural degree of rotation. When collapsed across knee flexion angles, mean hydrostatic pressure increased to 26% and 36% when the femur was rotated 5- and 10- from the natural position, respectively. Similarly, mean octahedral shear stress increased to 25% and 30% when the femur was rotated 5- and 10- from the natural position, respectively. Our finding of higher patella cartilage stress with femur internal rotation is consistent with the in vitro studies of Lee et al. (22,23). These authors reported 22%–24% increases in patella contact pressure when the femur was internally rotated to 30- at 30- and 60- of knee flexion. However, our results are in contrast to the FE study of Besier et al. (4), who reported that only 35% of subjects exhibited a 10% increase in patella cartilage stress when the femur was rotated to 15-. When evaluating potential reasons for the conflicting results between Besier et al. (4) and the current study, it is important to note that Besier et al. (4) examined patella stress profiles at 60- of knee flexion, which is higher than the knee flexion angles evaluated in the current study. Given that the patella is fully engaged in the trochlear groove at 60- of knee flexion, it is likely that femur internal rotation would have less of an impact on contact area and therefore patellofemoral joint stress at higher knee flexion angles. This premise is supported by the findings of Powers et al. (31) and Souza et al. (34) who reported that patella maltracking is more pronounced at lesser knee flexion angles (G20-) during a single-limb squatting task.
TABLE 1. Mean hydrostatic pressure at the chondroosseous interface of patella (mean T SD).
TABLE 2. Mean octahedral shear stress at the chondroosseous interface of patella (mean T SD).
RESULTS
Mean Hydrostatic Pressure (MPa)
Femur Rotation
15- Flexion
Natural 5- rotation 10- rotation Average
0.99 T 1.31 T 1.49 T 1.26 T
0.40 0.37 0.53 0.47
45- Flexion 1.65 2.01 2.10 1.92
T 0.32 T 0.57 T 0.54 T 0.50**
Average 1.32 T 0.49 1.66 T 0.58* 1.79 T 0.60*
*Indicates significant difference from natural rotation condition. **Indicates significant difference from 15- condition.
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Mean Octahedral Shear Stress (MPa)
Femur Rotation
15- Flexion
Natural 5- rotation 10- rotation Average
0.42 T 0.54 T 0.58 T 0.52 T
0.11 0.12 0.17 0.15
45- Flexion 0.72 T 0.87 T 0.91 T 0.82 T
0.09 0.23 0.18 0.17**
Average 0.57 T 0.18 0.71 T 0.24* 0.74 T 0.24*
*Indicates significant difference from natural rotation condition. **Indicates significant difference from 15- condition.
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CLINICAL SCIENCES FIGURE 2—Hydrostatic pressure distribution of a representative subject at 15- and 45- of knee flexion at 5- and 10- of femur internal rotation.
Previous studies have reported that females with PFP exhibit increased patellofemoral joint stress during functional activities when compared with that in pain-free individuals (7,8,37). In the current study, higher patella cartilage stresses were observed on the lateral facet of the patella (Fig. 2). This is logical, as femur internal rotation would move the lateral condyle of the femur closer to the lateral facet of patella. In addition, the laterally directed force caused by quadriceps muscle contraction also would contribute to higher lateral pressure. On average, higher stresses were observed at 45- of knee flexion compared with those at 15-. This is logical, given that quadriceps muscle forces are larger at higher degrees of knee flexion during squatting. From a mechanical standpoint, patellofemoral stress is influenced by contact area (30). A post hoc analysis of our data revealed that the area of contact between the patella and femur decreased significantly as the femur rotation angle increased. On average, contact area decreased to 22% and 31% when the femur was rotated 5- and 10- from the natural position, respectively. However, the relatively small decrease in contact area from 5- and 10- of femur rotation did not translate to a significant increase in stress. Previous biomechanical studies have shown that females with PFP exhibit increased hip internal rotation during functional activities when compared with that in pain-free individuals (2,26,28,29,35,38). The observed increase in hip internal rotation in females with PFP has been attributed to weakness of the hip external rotators (5,26,35). Our study provides evidence that excessive hip (femur) internal rotation may contribute to mechanical overloading of the patellofemoral joint. This finding is supported by a recent study that reported a moderate association between hip kinematics and pain in persons with PFP (27). In addition, our
findings are consistent with studies that have shown that hip external rotation strengthening decreases pain and improves functional status in persons with PFP (1,17,20,21). In light of the findings reported here, there are several limitations that should be noted. From a mechanical perspective, the biomechanical function of articular cartilage is best understood when the tissue is viewed as a multiphasic medium, with material properties that vary with location (inhomogeneity), direction (anisotropy), loading rate (viscoelasticity), and load magnitude (nonlinearity) (11,24). That being said, the modeling approach used in the current study was based on the assumption that the cartilage material was homogeneously distributed and that the effects of anisotropy and viscoelasticity were not considered. Given that articular cartilage has been modeled previously as a single-phase, linear, elastic continuum material (9,10,24), this simplification was deemed acceptable to assess the fundamental aspects of cartilage loading (31).
SUMMARY Internal rotation of the femur resulted in elevated patella cartilage stress during a squatting task. Our results support the premise that females with PFP who exhibit excessive hip internal rotation may be exposed to abnormal patellofemoral joint loading. As increased patellofemoral joint stress has been shown to result in higher subchondral bone strain and pain (19), clinicians may consider screening for altered hip kinematics in this population.
There was no external funding provided for this study, and the authors declared that there were no conflicts of interest. The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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ABSTRACT LIAO, T.-C., N. YANG, K.-Y. HO, S. FARROKHI, and C. M. POWERS. Femur Rotation Increases Patella Cartilage Stress in Females with Patellofemoral Pain. Med. Sci. Sports Exerc., Vol. 47, No. 9, pp. 1775–1780, 2015. Purpose: This study aimed to test the hypothesis that internal rotation of the femur increases patellofemoral joint stress in persons with patellofemoral pain (PFP). Methods: Patella cartilage stress profiles of nine female participants with PFP were obtained during squatting using subject-specific finite element (FE) models of the patellofemoral joint (15- and 45- of knee flexion). Input parameters for the FE model included joint geometry, quadriceps muscle forces during squatting, and weight-bearing patellofemoral joint kinematics. The femur of each model was then internally rotated 5- and 10- along its long axis beyond that of the natural degree of rotation. Using a nonlinear FE solver, quasistatic loading simulations were performed to quantify patellofemoral joint stress. Results: Compared with those at the natural position of the femur, mean hydrostatic pressure and mean octahedral shear stress were significantly higher when the femur was internally rotated 5- and 10-. No significant differences in stress variables were observed when the femur was rotated from 5- to 10-. These findings were consistent across both knee flexion angles (15- and 45-). Conclusions: The finding of elevated hydrostatic pressure and octahedral shear stress with internal rotation of the femur supports the premise that females with PFP who exhibit abnormal hip kinematics may be exposed to elevated patellofemoral joint stress. Key Words: ARTICULAR CARTILAGE, FINITE ELEMENT ANALYSIS, FEMUR INTERNAL ROTATION, PATELLOFEMORAL PAIN
P
It has been reported that the primary cause of increased patellofemoral joint stress in persons with PFP is decreased contact area associated with abnormal patella alignment and/ or maltracking (8,37). Recent research has suggested that patellofemoral joint maltracking in weight bearing is the result of excessive femur internal rotation as opposed to abnormal patella motion (31,34). In addition, biomechanical studies have shown that persons with PFP exhibit a greater degree of hip internal rotation during functional activities such as running, jumping, and stepping when compared with that in healthy individuals (2,26,28,29,35,38). In support of the premise that excessive hip internal rotation may contribute to the development of PFP, experimental studies have shown that internal rotation of the femur relative to the tibia increases patellofemoral joint stress. Using a cadaveric model, Lee et al. (22,23) observed a nonlinear increase in contact pressure on the lateral facet of the patella when the femur was internally rotated to 20- and 30- at knee flexion angles of 30-, 60-, 90-, and 120-. However, Besier et al. (4) reported no changes in patellofemoral cartilage stress using finite element (FE) analysis when the femur was internally rotated to 5-, 10-, and 15- at a knee flexion angle of 60-. In the study of Besier et al. (4), only 35% of subjects experienced a 10% increase in contact stress when the femur was rotated to 15-. The contrasting findings of Lee et al. (22,23) and Besier et al. (4) may be explained by the different knee flexion
atellofemoral pain (PFP) is a common condition seen in orthopedic practice. For example, PFP is the second most common lower extremity diagnosis and accounts for approximately 25%–40% of all knee injuries (13,36). In addition, women have a 2.2 times higher incidence of PFP when compared with that in men (6). A commonly cited hypothesis as to the cause of PFP is increased patellofemoral joint stress (7,8,37). Studies have reported that persons with PFP exhibit elevated patellofemoral joint stress during walking and running and greater patella and femur cartilage stresses during squatting when compared with those in pain-free individuals (3,15). Although cartilage is aneural (32), increased cartilage stress has been shown to lead to increased subchondral bone stress, which has been proposed to be a source of retropatellar pain (19).
Address for correspondence: Christopher M. Powers, P.T., Ph.D., F.A.C.S.M., F.A.P.T.A., Jacquelin Perry Musculoskeletal Biomechanics Research Laboratory, Division of Biokinesiology and Physical Therapy, University of Southern California, 1540 E. Alcazar St., CHP-155, Los Angeles, CA 90089-9006; E-mail: [email protected]. Submitted for publication July 2014. Accepted for publication January 2015. 0195-9131/15/4709-1775/0 MEDICINE & SCIENCE IN SPORTS & EXERCISEÒ Copyright Ó 2015 by the American College of Sports Medicine DOI: 10.1249/MSS.0000000000000617
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Femur Rotation Increases Patella Cartilage Stress in Females with Patellofemoral Pain
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angles and femur rotation angles evaluated. Besier et al. (4) examined the influence of femur internal rotation at rotation angles of 5-, 10-, and 15-, whereas Lee et al. (21,22) evaluated much higher rotation angles, 20- and 30-. Souza et al. (34) have reported that femur rotation angles in persons with PFP during a single-leg squat range from 4- to 12-, suggesting that the femur rotation angles evaluated in the studies of Lee et al. (22,23) may not have been physiologically possible. However, Besier et al. (4) evaluated the influence of femur rotation at a relative high knee flexion angle (60-). This is problematic because Souza et al. (34) have reported that internal rotation of the femur in persons with PFP is more pronounced as the knee extends from 45- to full knee extension. The influence of femur internal rotation on patellofemoral joint stress may be more pronounced at lower knee flexion angles. Given the limitations of previous research in this area, the purpose of the current study was to determine the influence of femur internal rotation on patella cartilage stress in females with PFP. For purposes of this study, we evaluated physiological degrees of femur rotation (5- and 10-) at relatively small knee flexion angles (15- and 45-). Using a subjectspecific FE modeling approach, we hypothesized that patella cartilage stress would increase with greater degrees of femur rotation. Information gained from this study will clarify the role of femur rotation in contributing to patellofemoral joint stress.
METHODS Subjects. Nine female participants with a diagnosis of PFP participated in this study. The average age, height, and weight of the participants were 27.7 T 4.3 yr, 1.7 T 0.1 m, and 63.3 T 8.4 kg, respectively. Before participation, all subjects were informed as to the nature of the study and signed a human subject’s consent form approved by the Healthy Sciences Institutional Review Board of the University of Southern California. Individuals with PFP were admitted to the study if their pain originated from behind the patella (i.e., retropatellar pain). Only subjects that reported an insidious onset of symptoms were accepted. Subjects were screened through physical examination to rule out evidence of large knee effusion and peripatellar pain. The screening procedure also included a functional assessment of activities commonly associated with PFP (squatting, stair climbing, and isometric quadriceps contraction). Subjects were included in the study if they reported pain of at least 3 out of 10 (based on a visual analog scale) with one or more of the aforementioned functional tasks. Individuals with PFP were excluded from participation if they reported any of the following: 1) history of knee surgery, 2) history of traumatic patella dislocation, 3) neurological involvement that would influence performance of functional activities, and 4) implanted biological devices that could interact with the magnetic field of the MRI. Procedures. Subjects completed two data collection sessions. The first session consisted of magnetic resonance
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(MR) assessment of the knee and patellofemoral joints, whereas the second session consisted of biomechanical testing. For all subjects, testing was performed on the painful side. In cases of bilateral pain, the more symptomatic limb was evaluated. MR assessment. Subject-specific cartilage morphology and bone geometry of the knee and the patellofemoral joints were obtained using a 3.0-T MR scanner (General Electric Healthcare, Milwaukee, WI). Images were acquired with an eight-channel knee coil using a three-dimensional (3D), highresolution, fat-suppressed, fast spoiled gradient recalled echo (SPGR) sequence (repetition time, 14.5 ms; echo time, 2.8 ms; flip angle, 10-; matrix, 320 320; field of view, 16 cm; slice thickness, 1.0 mm; scan time, 8:58 min). During this scan, subjects were positioned supine with the knee extended. To obtain the relative weight-bearing orientations of the patella, femur, and tibia, a custom-made nonferromagnetic loading apparatus providing a force equivalent to 25% of subjects’ body weight was used. Loaded MR images of the subjects’ knees were acquired at 15- and 45- of knee flexion using a 3D, fast SPGR sequence (repetition time, 14.3 ms; echo time, 3.6 ms; flip angle, 10-; matrix, 320 160; field of view, 16 cm; slice thickness, 2.0 mm; scan time, 1:45 min). Quadriceps muscle morphology was assessed from sagittal plane MR images of the thigh using a 3D SPGR protocol (repetition time, 9.4 ms; echo time, 4.1 ms; flip angle, 20-; matrix, 384 384; field of view, 46 cm; slice thickness, 2 mm; scan time, 8:03 min). The sagittal plane images of the thigh were subsequently reconstructed in the coronal and axial planes and were used to estimate the 3D fiber orientation of each of the quadriceps muscles (see next section for details). The axial images of the thigh were used to measure the cross-sectional area of the quadriceps muscles, which was subsequently used as an input variable for the biomechanical model to estimate the magnitude of muscle forces. Biomechanical testing. Subjects were instrumented for 3D motion and EMG analyses as described in previous publications (8,37). Lower extremity kinematics was collected using an eight-camera motion analysis system at 60 Hz (Vicon; Oxford Metrics Ltd., Oxford, England). Ground reaction forces were recorded at a rate of 1560 Hz using two AMTI force plates (model #OR6-6-1; Newton, MA). EMG signals of muscles crossing the knee joint (see next section for details) were recorded at 1560 Hz using preamplified, bipolar surface electrodes (Motion Lab Systems, Baton Rouge, LA). After a standing calibration trial, subjects were asked to hold a bilateral squat position at 15- and 45- of knee flexion, with each foot positioned on a separate force plate. To account for the influence of the trunk position on the lower extremity demands during weight bearing (16), the subjects’ trunk position was controlled by asking the subjects to flex their knees to the desired angle while keeping fingertip contact with the pole placed at arm’s length. While holding the desired squatting position, kinematic, kinetic, and EMG data were recorded. These information were used for estimation of quadriceps muscle forces, which was required as an input variable in the FE model.
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the femur (25). As described in a previous publication (12), the most lateral and medial borders of quadriceps line of pull (i.e., the vastus lateralis and vastus medialis) were determined from the sagittal and frontal plane fiber orientation of each muscle as measured from MR images of the subject’s thigh. Six connector elements representing each muscle group were then distributed uniformly from the medial to lateral borders. In addition, six uniaxial tension-only elements with total stiffness of 4334 NImmj1 were used to represent the patella tendon, which connected the patella and the tibia (18). Simulations were performed using a hard contact algorithm with a surface coefficient of friction of 0.02 (3). Quasistatic loading simulations were performed using a nonlinear FE solver (Abaqus; SIMULIA, Providence, RI). For all simulations, the bony structures (i.e., femur, tibia, and patella) were modeled as rigid bodies. The initial orientations of the bony rigid bodies were determined from the weight bearing MR images. To obtain the weight-bearing positioning of the patella, femur, and tibia at 15- and 45- of knee flexion, the FE mesh of each bone was registered to the corresponding bony surfaces obtained from the weight bearing images. To simulate a stable weight bearing condition, the femur and tibia were fixed in space. To examine the influence of internal rotation on cartilage stress, the femur was rotated 5- and 10- along its long axis beyond that of the natural degree of rotation. This procedure was repeated at 15- and 45- of knee flexion. To represent an initial unloaded condition, the patella was moved anteriorly to create a gap between the articulating surfaces of the patellofemoral joint. Because the soft tissues controlling the rotation of the patellofemoral joint were not included in the models, the three rotational degrees of freedom of the patella were constrained.
FIGURE 1—Subject-specific input parameters used to create FE models of the patellofemoral joint.
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FE model development. Subject-specific input parameters entered into the modeling pipeline included the following: joint geometry, quadriceps muscle forces, and weight-bearing patellofemoral joint kinematics (Fig. 1). Using a commercial software package (Sliceomatic; Tomovision, Montreal, Quebec), the high-resolution sagittal plane MR images of the knee were manually segmented and 3D surfaces of the femur, tibia, patella, and articular cartilage covering of the femur and patella were created. Surfaces created for the femur, tibia, and patella were subsequently used to create rigid body shells of each bony structure using a proprietary FE preprocessor (Hypermesh; Altair Engineering Inc., Troy, MI). The articular cartilage of the patella and femur was modeled as homogeneous isotropic tetrahedral continuum elements with an elastic modulus of 4.0 MPa (14) and a Poisson ratio of 0.47 (3). An average element size of 0.75 mm was used because a previous convergence analysis revealed that decreasing the element size did not result in a meaningful change in stress but resulted in longer computational time for the simulation (15). The methods used to estimate the individual quadriceps muscle forces from the biomechanical testing session have been described previously (12). Briefly, a subject-specific representation of the extensor mechanism was created using the SIMM modeling software (MusculoGraphics, Santa Rosa, CA). Subject-specific biomechanical data (kinematics, kinetics, and EMG) were used to drive the model (via an optimization routine), and 3D quadriceps muscle forces were computed. The elements representing the quadriceps muscles were separated into three functional groups made up of six equivalent uniaxial force actuators (the rectus femoris/vastus intermedius, vastus medialis, and vastus lateralis muscles). The direction of muscle line of pull for the rectus femoris/ vastus intermedius group was set parallel to the long axis of
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Model output and postprocessing. Articular cartilage stress was quantified in terms of two invariants, as follows: 1) hydrostatic pressure and 2) octahedral shear stress (9–11). As scalar parameters, hydrostatic pressure and octahedral shear stress represent different aspects of the stress field (10). Hydrostatic pressure reflects the magnitude of the portion of the stress tensor that tends to uniformly compress the cartilage, whereas octahedral shear stress reflects the portion of the stress field that tends to distort the tissue (10). A mesh surface was created to represent the chondroosseous interface by selecting the element faces of the tetrahedral elements that were adjacent to the subchondral bone surface. The stress values were estimated at the centroids of cartilage element faces closest to the bone. Elements with only one node at the interface were not included in the analyses. To establish a clinically meaningful measure of mean patella hydrostatic pressure and octahedral shear stress, only elements with stress values above a threshold of 271 kPa were considered when calculating the mean stress. This threshold corresponds to the minimum bone stress–pain threshold previously established for healthy subjects (33). Statistical analyses. To test the hypothesis that cartilage stress differed between femur rotation angles, a 3 2 ANOVA with repeated measures was performed (femur rotation angle knee angle). This analysis was repeated for mean hydrostatic pressure and mean octahedral shear stress of the patella cartilage elements at the chondroosseous interface. For all ANOVA tests, significant main effects were reported if there were no significant interactions. For all statistical tests, the alpha level was set at 0.05.
significant interaction (P = 0.77). However, the main effects for femur rotation angle and knee flexion angle were significant (P = 0.02 and P G 0.01, respectively). When collapsed across knee flexion angles, mean octahedral shear stress was significantly higher with the femur rotated to 5and 10- when compared with that at natural degree of rotation (Table 2). There were no significant differences in mean hydrostatic pressure between the 5- and 10- femur rotation conditions. When collapsed across femur rotation angles, the mean octahedral shear stress was significantly higher at 45- knee flexion when compared with that at 15- knee flexion (Table 1).
DISSUSSION
The ANOVA comparing mean hydrostatic pressure across femur rotation and knee flexion angles did not reveal a significant interaction (P = 0.59). However, the main effects for femur rotation angle and knee flexion angle were significant (P = 0.01 and P = 0.02, respectively). When collapsed across knee flexion angles, mean hydrostatic pressure was significantly higher with the femur rotated to 5- and 10- when compared with that at natural degree of rotation (Table 1). There were no significant differences in mean hydrostatic pressure between the 5- and 10- femur rotation conditions. When collapsed across femur rotation angles, mean hydrostatic pressure was significantly higher at 45- knee flexion when compared with that at 15- knee flexion (Table 1). The ANOVA comparing mean octahedral shear stress across femur rotation and knee flexion angles did not reveal
The purpose of this study was to evaluate whether internal rotation of the femur results in elevated patella cartilage stress in females with PFP. Two scalar invariants, hydrostatic pressure and octahedral shear stress, at the chondroosseous interface of the patella were used to quantify articular cartilage loading. Consistent with our hypothesis, patella cartilage stress was significantly higher when the femur was internally rotated 5- and 10- beyond that of the natural degree of rotation. When collapsed across knee flexion angles, mean hydrostatic pressure increased to 26% and 36% when the femur was rotated 5- and 10- from the natural position, respectively. Similarly, mean octahedral shear stress increased to 25% and 30% when the femur was rotated 5- and 10- from the natural position, respectively. Our finding of higher patella cartilage stress with femur internal rotation is consistent with the in vitro studies of Lee et al. (22,23). These authors reported 22%–24% increases in patella contact pressure when the femur was internally rotated to 30- at 30- and 60- of knee flexion. However, our results are in contrast to the FE study of Besier et al. (4), who reported that only 35% of subjects exhibited a 10% increase in patella cartilage stress when the femur was rotated to 15-. When evaluating potential reasons for the conflicting results between Besier et al. (4) and the current study, it is important to note that Besier et al. (4) examined patella stress profiles at 60- of knee flexion, which is higher than the knee flexion angles evaluated in the current study. Given that the patella is fully engaged in the trochlear groove at 60- of knee flexion, it is likely that femur internal rotation would have less of an impact on contact area and therefore patellofemoral joint stress at higher knee flexion angles. This premise is supported by the findings of Powers et al. (31) and Souza et al. (34) who reported that patella maltracking is more pronounced at lesser knee flexion angles (G20-) during a single-limb squatting task.
TABLE 1. Mean hydrostatic pressure at the chondroosseous interface of patella (mean T SD).
TABLE 2. Mean octahedral shear stress at the chondroosseous interface of patella (mean T SD).
RESULTS
Mean Hydrostatic Pressure (MPa)
Femur Rotation
15- Flexion
Natural 5- rotation 10- rotation Average
0.99 T 1.31 T 1.49 T 1.26 T
0.40 0.37 0.53 0.47
45- Flexion 1.65 2.01 2.10 1.92
T 0.32 T 0.57 T 0.54 T 0.50**
Average 1.32 T 0.49 1.66 T 0.58* 1.79 T 0.60*
*Indicates significant difference from natural rotation condition. **Indicates significant difference from 15- condition.
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Mean Octahedral Shear Stress (MPa)
Femur Rotation
15- Flexion
Natural 5- rotation 10- rotation Average
0.42 T 0.54 T 0.58 T 0.52 T
0.11 0.12 0.17 0.15
45- Flexion 0.72 T 0.87 T 0.91 T 0.82 T
0.09 0.23 0.18 0.17**
Average 0.57 T 0.18 0.71 T 0.24* 0.74 T 0.24*
*Indicates significant difference from natural rotation condition. **Indicates significant difference from 15- condition.
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CLINICAL SCIENCES FIGURE 2—Hydrostatic pressure distribution of a representative subject at 15- and 45- of knee flexion at 5- and 10- of femur internal rotation.
Previous studies have reported that females with PFP exhibit increased patellofemoral joint stress during functional activities when compared with that in pain-free individuals (7,8,37). In the current study, higher patella cartilage stresses were observed on the lateral facet of the patella (Fig. 2). This is logical, as femur internal rotation would move the lateral condyle of the femur closer to the lateral facet of patella. In addition, the laterally directed force caused by quadriceps muscle contraction also would contribute to higher lateral pressure. On average, higher stresses were observed at 45- of knee flexion compared with those at 15-. This is logical, given that quadriceps muscle forces are larger at higher degrees of knee flexion during squatting. From a mechanical standpoint, patellofemoral stress is influenced by contact area (30). A post hoc analysis of our data revealed that the area of contact between the patella and femur decreased significantly as the femur rotation angle increased. On average, contact area decreased to 22% and 31% when the femur was rotated 5- and 10- from the natural position, respectively. However, the relatively small decrease in contact area from 5- and 10- of femur rotation did not translate to a significant increase in stress. Previous biomechanical studies have shown that females with PFP exhibit increased hip internal rotation during functional activities when compared with that in pain-free individuals (2,26,28,29,35,38). The observed increase in hip internal rotation in females with PFP has been attributed to weakness of the hip external rotators (5,26,35). Our study provides evidence that excessive hip (femur) internal rotation may contribute to mechanical overloading of the patellofemoral joint. This finding is supported by a recent study that reported a moderate association between hip kinematics and pain in persons with PFP (27). In addition, our
findings are consistent with studies that have shown that hip external rotation strengthening decreases pain and improves functional status in persons with PFP (1,17,20,21). In light of the findings reported here, there are several limitations that should be noted. From a mechanical perspective, the biomechanical function of articular cartilage is best understood when the tissue is viewed as a multiphasic medium, with material properties that vary with location (inhomogeneity), direction (anisotropy), loading rate (viscoelasticity), and load magnitude (nonlinearity) (11,24). That being said, the modeling approach used in the current study was based on the assumption that the cartilage material was homogeneously distributed and that the effects of anisotropy and viscoelasticity were not considered. Given that articular cartilage has been modeled previously as a single-phase, linear, elastic continuum material (9,10,24), this simplification was deemed acceptable to assess the fundamental aspects of cartilage loading (31).
SUMMARY Internal rotation of the femur resulted in elevated patella cartilage stress during a squatting task. Our results support the premise that females with PFP who exhibit excessive hip internal rotation may be exposed to abnormal patellofemoral joint loading. As increased patellofemoral joint stress has been shown to result in higher subchondral bone strain and pain (19), clinicians may consider screening for altered hip kinematics in this population.
There was no external funding provided for this study, and the authors declared that there were no conflicts of interest. The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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