Patients with Cam-Type Femoroacetabular Impingement Demonstrate Increased Change in Bone-to-Bone Distance during Walking: A Dual Fluoroscopy Study

Abstract

Cam-type femoroacetabular impingement (FAI) syndrome is a painful, structural hip disorder. Herein, we investigated hip joint mechanics through in vivo, dynamic measurement of the bone-to-bone distance between the femoral head and acetabulum in patients with cam FAI syndrome and morphologically screened controls. We hypothesized that individuals with cam FAI syndrome would have larger changes in bone-to-bone distance compared to the control group, which we would interpret as altered joint mechanics as signified by greater movement of the femoral head as it articulates within the acetabulum. Seven patients with cam FAI syndrome and eleven asymptomatic individuals with typical morphology underwent dual fluoroscopy imaging during level and inclined walking (upward slope). The change in bone-to-bone distance between femoral and acetabular bone surfaces was evaluated for five anatomical regions of the acetabulum at each timepoint of gait. Linear regression analysis of the bone-to-bone distance considered two within-subject factors (activity, region) and one between-subjects factor (group). Across activities, the change in minimum bone-to-bone distance was 1.38-2.54mm for the cam FAI group and 1.16-1.84mm for controls. In all regions except the anterior-superior region, the change in bone-to-bone distance was larger in the cam group than the control group (p≤.024). An effect of activity was detected only in the posterior-superior region where larger changes were noted during level walking than incline walking.

Statement of Clinical Significance:

Patients with cam FAI syndrome exhibit altered hip joint mechanics during the low-demand activity of walking; these alterations could affect load transmission, and contribute to pain, tissue damage, and osteoarthritis.

Level of Evidence:

Cross-sectional; 3.

Introduction:

Femoroacetabular impingement (FAI) syndrome is a motion-related structural hip disorder.¹ Individuals who present clinically with hip pain that is both aggravated by movement and reproduced with clinical tests, including the hip flexion, adduction and internal rotation (FADIR) test, and who have specific hip morphological features on imaging are diagnosed with FAI syndrome consistent with the Warwick agreement.¹ Patients with cam-type morphology exhibit a loss of sphericity of the femoral head and/or reduced femoral head neck offset. Rotation of the aspherical femoral head within the acetabulum may cause the femoral head to lever- or cam-out,^2,3 which may be observed as larger variability in the distance between the femur and the acetabulum (i.e., bone-to-bone distance) throughout the motion as compared to individuals without deformity. Abnormal motion of the femur in the acetabulum may disrupt normal load transmission, leading to injuries of the acetabular labrum and articular cartilage that increase the risk of hip osteoarthritis (OA).^4-6

The initially proposed pathomechanics of cam morphology suggested that impingement occurred in activities with substantial hip flexion such as deep squats. However, whole body biomechanical studies indicate movement patterns are altered in individuals with FAIS during daily activities which do not require end range hip positions.^7-9 Still, the role cam morphology has on in vivo articulation of the hip joint during daily activities such as walking is not well understood. Notably, most studies investigating this clinical population have been based on skin marker motion capture, which is prone to kinematic measurement errors due to soft tissue artefact and inaccuracies in the estimate of the hip joint center location.^10,11 More recent research has applied dual fluoroscopy (DF) to study the kinematics of patients with FAIS. The advantage of DF is that it provides direct imaging and tracking of in vivo motion of the femur and acetabulum with submillimeter accuracy.¹² The motion quantified by DF is displayed relative to patient- or subject-specific bone anatomy provided by three-dimensional (3D) reconstructions of segmented medical image data, thereby enabling investigation of the role of morphology on the mechanics of motion.

An improved understanding of the influence of cam morphology on the mechanics of articulation between the femur and acetabulum of patients with cam FAI syndrome could improve diagnosis, treatment planning, and evaluation of the efficacy of clinical interventions, such as rehabilitation and/or surgery. The primary objective of this DF imaging study was to investigate hip joint mechanics through in vivo, dynamic measurement of the bone-to-bone distance between the femoral head and acetabulum during walking in patients with cam FAI syndrome and morphologically normal controls. Walking was selected as it is one of the most frequent activities of daily living; incline walking was selected because it requires increased hip flexion and because recent research has demonstrated that hip kinematics are different between patients with cam FAI syndrome and control participants during this activity.¹³ We chose to use bone-to-bone distance as a measure of joint mechanics since it reflects the dynamic interaction between the femur and acetabulum and inherently includes the collective stabilizing effects of the surrounding soft tissue; furthermore, the change in bone-to-bone distance may be more appropriate than measuring femoral head translations since the latter method relies on fitting a sphere to a femoral head which is, in the case of cam morphology, non-spherical. We hypothesized that individuals with cam FAI syndrome would have larger changes in bone-to-bone distance when compared to the control group, which we would interpret as altered joint mechanics as signified by greater movement of the femoral head as it articulates within the acetabulum.

Methods:

Study Design:

This is a cross sectional study with convenience sample.

Participants:

Seven participants with cam morphology and a diagnosis of FAI syndrome (5 males, 2 females; age, 29±7 years; height, 179.1±10.1 cm; mass, 78.9±15.2 kg) and eleven asymptomatic individuals with typical morphology (6 males, 5 females; age, 23±2 years; height, 173.3±10.4 cm; mass, 63.8±10.9 kg) participated in this study between March 2013 and January 2016 from the University of Utah Orthopaedic Center. During the period of recruitment, all eligible patients seen in the clinic were consulted for participation in our study. Individuals in the patient group needed to have imaging findings of cam morphology (i.e., alpha angle greater than 55.5°)¹⁴, symptoms, and clinical signs consistent with FAI syndrome.¹ All patients were planning to undergo surgery to treat their symptoms. Individuals in the control group were recruited via word of mouth and also needed to have an alpha angle less than 55.5°¹⁴ and no history of hip pain, and thus were different from the patients in both morphology and pain status. For both patients and control participants, alpha angles were measured from oblique-axial reformatted magnetic resonance images (MRI);¹⁵ as previously published,¹³ patients had larger alpha angles than asymptomatic control participants (61±5° compared to 40±5°, p<.001). All participants also had to have a lateral center edge angle between 20° and 45° indicating no acetabular dysplasia or pincer morphology and Kellgren-Lawrence (KL) grade < 2 indicating little or no evidence of hip OA. Individuals with evidence of other anatomical abnormalities were excluded. Additionally, to participate in the study, both patients and control participants needed to be recreationally active with a body mass index (BMI) less than 30 kg/m² and have no previous history of lower limb surgery. All participants provided written informed consent as approved by the University of Utah Institutional Review Board and the research was conducted according to the Declaration of Helsinki.

Computed Tomography Scan:

Computed tomography (CT) arthrography images were obtained according to a published protocol¹⁵; the same protocol was used for patients and controls. Briefly, CT images were acquired using a 128-section single-source CT machine (SOMATOM Definition™, Siemens Healthcare, Munich, Bavaria, Germany). Images of the proximal femur and pelvis were acquired at 120 kVp, 1.0 mm slice thickness, and 200-400 mAs. The acquisition matrix was 512x512, while the field of view varied slightly based on the width of the participant’s pelvis, resulting in a spatial resolution of approximately 0.7x0.7mm (range: 0.61 - 0.77mm). The hip that was to be treated with surgery was segmented for patients, whereas a randomly selected side was segmented for control participants to have a balanced number of left and right hips.

Motion Capture:

Dual fluoroscopy images were acquired of the selected hip at 100 frames per second during two activities¹³, including treadmill walking on a level surface and 5° incline (corresponding to a 1:12 upward slope similar to a wheelchair-accessible ramp). The same protocol was used for patients and controls. All data were collected at the participant’s self-selected speed, which was determined with a timed walk overground prior to imaging. For direct comparisons across participants, each gait cycle was normalized to 100 time points.

Image Analysis:

The time-varying position of the femur and pelvis were determined using model-based tracking (MBT)¹⁶ as previously described; the same protocol was used for patients and controls.^12,13 A CT-based model of each bone and the dual fluoroscopic images were input into MBT software. MBT software generated digitally-reconstructed radiographs (DRRs) from the CT-based model, which were semi-automatically aligned with the two fluoroscopic images. Alignment of the DRRs with the fluoroscopic images in two views determined the 3D position of each bone over time. Previous research has demonstrated that DF and MBT of the hip produces kinematic positional errors of less than 0.48 mm and rotational errors of less than 0.58°, with average errors for bone-to-bone distance of 0.52 mm.¹²

Bone Surface Files and Acetabular Regions:

Subchondral bone of the femur and acetabulum was semi-automatically segmented to obtain 3D reconstructions using the Amira software (6.1, ThermoFisher Scientific, Waltham, MA).^12,17 Surfaces were decimated and smoothed according to a published protocol to remove small surface irregularities.¹² The region of the acetabulum was isolated using the second principle surface curvature (smoothing, 5; cutoff, 0.0; PostView software, v2.0, University of Utah, Salt Lake City, UT), then divided into superior, anterior-superior, anterior-inferior, inferior, posterior-inferior, and posterior-superior regions. Regions were defined by dividing the surface of the acetabulum into equal, 60° increments where the inferior region was centered over the acetabular notch (Figure 1). Owed to an absence of articular cartilage and subchondral bone, the inferior region of the acetabulum was not analyzed.

Figure 1.

The acetabulum was divided into six 60° radial segments for analysis. A plane was fit to the rim of the acetabulum; the anterior and posterior inferior edges of the lunate surface (dashed line) were transected by a line originating at the projected center of the acetabulum (dotted line) to define the inferior direction. The region split by this inferiorly pointed vector defined the orientation of the six regions but was omitted from analysis of bone-to-bone distance as contact is minimal in this region due to the absence of acetabular bone. Sup, superior; Ant, anterior; Int, inferior, Post, posterior.

Bone-to-bone Distance:

For each time point of the gait cycle, bone-to-bone distance between the subchondral surface reconstructions of the acetabulum and the femoral head was calculated for each node on the surface of the joint, such that it was spatially-varying (PostView). This algorithm measures the minimum distance between the two surfaces at each vertex of the surface of interest. We used mesh densities for the pelvis and femur surface reconstructions that were of sufficient resolution to yield converged measurements of bone-to-bone distance.¹⁸ At each normalized time point of the gait cycle, the minimum bone-to-bone distance within each region was determined. The change in the minimum distance was used to measure joint mechanics and was quantified as the difference between the largest minimum value and smallest minimum value recorded during the gait cycle.

Statistical Methods:

Linear regression analyses of the minimum distance (smallest and largest) and the change in minimum distance were performed with two within-subject factors (activity and region) and one between-subjects factor (group) using IBM SPSS Statistics (Version 24). The activity was either level or inclined gait, the region was one of the five analyzed acetabular regions, and group was either cam FAI syndrome or control. We modeled the main effects of activity, region, and group, and each interaction term; a generalized estimating equation (GEE) was applied to correct for repeated measures (activity and region). Least significant difference (LSD) pairwise comparisons were performed if a main effect was found. Statistical significance for all tests was set at p<0.05.

Results:

Across activities and groups, the mean regional smallest minimum bone-to-bone distance ranged from 0.7 to 2.1 mm while the mean regional largest minimum bone-to-bone distance ranged from 2.5 to 3.8 mm (Table 1). There was a three-way interaction of activity, region, and group (p<.001) for each main analysis. Therefore, each of the five acetabular regions was analyzed separately. A main effect of group was noted for the largest minimum distance in the anterior-inferior (p=.019; mean difference: 0.5, 95% CI: 0.1, 0.9) and the posterior-superior (p=.019; mean difference: 0.5, 95% CI: 0.1, 0.8) regions, where the cam FAI group had the greater largest minimum distance (Figure 2). A main effect of activity for the largest minimum distance was noted in the posterior-superior region (p=.009; mean difference: 0.2, 95% CI: 0.1, 0.4) with distances being less during incline walking compared to level walking. Main effects of activity were also noted for the smallest minimum value in the superior (p=.041; mean difference: 0.2, 95% CI: 0.0, 0.3) and anterior-superior (p=.013; mean difference: 0.2, 95% CI: 0.0, 0.4) regions, with the smallest minimum values being less during incline walking compared to level walking (Figure 3).

Table 1.

Mean (standard deviation) of smallest, largest, and change in minimum bone-to-bone distance within each region across the gait cycle (mm).

Activity	Group		Acetabular Region
			Superior	Anterior- Superior	Anterior- Inferior	Posterior- Inferior	Posterior- Superior
Minimum bone-to-bone distance
Walk	Cam	Smallest	2.0 (0.7)	1.5 (0.3)	1.7 (0.3)	0.7 (0.4)	0.9 (0.6)
		Largest	3.6 (0.4)	3.4 (0.5)	3.7 (0.5)	2.8 (0.8)	3.4 (0.5)
		Change	1.6 (0.5)	1.9 (0.4)	2.1 (0.5)	2.2 (0.6)	2.5 (0.6)
	Control	Smallest	2.1 (0.5)	1.8 (0.7)	1.7 (0.7)	0.8 (0.4)	1.1 (0.5)
		Largest	3.2 (0.6)	3.5 (0.5)	3.3 (0.5)	2.6 (0.3)	2.9 (0.4)
		Change	1.2 (0.5)	1.7 (0.7)	1.6 (0.7)	1.7 (0.5)	1.8 (0.4)
Incline	Cam	Smallest	1.8 (0.7)	1.2 (0.2)	1.5 (0.4)	0.8 (0.5)	1.2 (0.5)
		Largest	3.5 (0.7)	3.4 (0.7)	3.8 (0.7)	2.8 (0.6)	3.1 (0.4)
		Change	1.7 (0.2)	2.1 (0.7)	2.2 (0.8)	2.0 (0.5)	2.0 (0.5)
	Control	Smallest	1.9 (0.5)	1.7 (0.6)	1.8 (0.7)	0.9 (0.5)	1.2 (0.6)
		Largest	3.2 (0.6)	3.4 (0.7)	3.2 (0.6)	2.5 (0.4)	2.8 (0.6)
		Change	1.2 (0.5)	1.7 (0.6)	1.4 (0.6)	1.6 (0.5)	1.6 (0.6)

Figure 2:

Box plots (and outliers labeled with subject identifiers) for largest minimum bone-to-bone distance during incline and level walking in patients with cam morphology and control participants. The largest minimum bone-to-bone distances were greater for the cam group than the control group with significant effects of either group (†) or activity (‡) from the regression analysis indicated. FAIS, femoroacetabular impingement syndrome.

Figure 3.

Box plots (and outliers labeled with subject identifiers) for smallest minimum bone-to-bone distance during incline and level walking in patients with cam morphology and control participants. Minimum bone-to-bone distances were smaller when walking on an incline than when walking on level surface with significant effects of activity (‡) from the regression analysis indicated. FAIS, femoroacetabular impingement syndrome.

The mean change (largest – smallest) in minimum bone-to-bone distance over the gait cycle ranged from 1.2 to 2.5 mm (Table 1). Similar to the minimum bone-to-bone distances, there was a three-way interaction of activity, region, and group (p<.001). Main effects of group were noted for the superior (p=.017; mean difference: 0.4, 95% CI: 0.1, 0.8), anterior-inferior (p=.003; mean difference: 0.7, 95% CI: 0.2, 1.1), posterior-inferior (p=.005; mean difference: 0.5, 95% CI: 0.2, 0.9), and posterior-superior (p=.024; mean difference: 0.4, 95% CI: 0.1, 0.8) regions (Figure 4). In each of these regions, the cam FAI group had a greater change in the minimum distance than the control group, which was observed at discrete positions (Figure 5) and throughout gait (Supplemental Video 1). In the posterior-superior region, there was also a main effect of activity; the change in minimum distance was less during incline walking than during level walking (p=.004; mean difference: 0.4, 95% CI: 0.1, 0.7). The only region without any differences was the anterior-superior region (p≥.184).

Figure 4:

Box plots (and outliers labeled with subject identifiers) for change (largest-smallest) in minimum bone-to-bone distance during incline and level walking in patients with cam morphology and control participants. The cam group had greater change in minimum bone-to-bone distance for all regions except the Anterior-Superior region with significant effects of either group (†) or activity (‡) from the regression analysis indicated. FAIS, femoroacetabular impingement syndrome.

Figure 5.

Color fringe plot of bone-to-bone distance (A) and minimum bone-to-bone distance in each region (B) from heel strike (0) to ipsilateral heel strike (100) for a representative patient with cam FAI syndrome (FAIS) and a control participant. The change in bone-to-bone distance (largest – smallest) was calculated for the five regions of interest.

Discussion:

We found that individuals with cam morphology and FAI syndrome demonstrated a greater change in the minimum bone-to-bone distance within all regions of the acetabulum except the anterior-superior region when compared to pain-free individuals with typical morphology. Further, bone-to-bone distance varied more dramatically during gait in the patient group than in individuals without deformity or pain, which may indicate that cam morphology and pain contribute to instability as the femur rotates within the acetabulum. We observed group differences in bone-to-bone distance during walking, which is a submaximal activity wherein direct impingement would not be expected between the femoral neck and acetabulum. Our findings challenge the original presumption that mechanics in hips with cam morphology are altered as a result of direct impingement at end range hip positions. Notably, our results build upon recent studies^8,13 that suggest cam morphology affects hip joint biomechanics during activities of daily living, even when the demand for flexion, internal rotation, and adduction is minimal.

Our study is the first to quantify changes in bone-to-bone distance in individuals with FAI syndrome during functional tasks. One prior study using CT evaluated the translation of the femoral head between neutral and combined hip flexion, abduction, and external rotation (FABER) in individuals with FAI syndrome.¹⁹ In their evaluation of two static positions, 29% of patients had total translations greater than 1 mm, with the average translation of all patients being 0.84 mm. While joint translations are not equivalent with bone-to-bone distances, we noted larger changes during dynamic activities. As measured by DF during walking, we found mean changes in bone-to-bone distance of 2.54 mm in patients with cam morphology compared to 1.84 mm in the control group. Larger changes in bone-to-bone distance suggest greater movement of the femoral head within the acetabulum, supporting the assertion of decreased stability in symptomatic patients with cam morphology.^2,3,20,21

Although present in many individuals without pain,²² cam morphology is a recognized risk factor for future hip OA.^4-6 While physical impingement of the femur and acetabulum is the presumed mechanism for increased OA risk, altered hip joint mechanics, including decreased stability may also be a factor as theorized by Eijer and Hogervorst.²⁰ Altered mechanics may modify the loading environment, such as through increased compressive and shear stresses,²³ and contribute to the elevated risk of OA in hips with cam morphology.^4-6 The lack of significant difference in the anterior-superior region was surprising given that this region is where cartilage damage is most commonly observed in hips with cam morphology.^24-26 However, it should be noted that the force from the femur onto the acetabulum is directed anteriorly and superiorly for most of the gait cycle.²⁷ The anteriorly directed force may contribute to a consistent bone-to-bone position shifting the center of rotation toward the anterior-superior region while allowing the distance to vary more in other regions.

In addition to contributing to the understanding of how cam morphology and pain alters hip joint mechanics, our study also emphasized the need for advancements in computerized surgical planning and impingement evaluation tools. These tools traditionally use a fixed center of rotation.²⁸ As demonstrated here and by Cvetanovich and colleagues,¹⁹ it is unlikely that femurs with cam morphology maintain a single point of rotation within the acetabulum. Further, studies have also shown that regions of minimum bone-to-bone distance do not necessarily correlate with the regions of femur-labrum contact.^28,29 As such, incorporating dynamic joint translation and soft-tissue structures into these models could substantially improve the validity and value of surgical planning and impingement evaluation tools.

Although we found that painful hips with cam morphology had greater change in bone-to-bone distance, the origin of the alteration is unclear. A levering effect of cam morphology has been proposed whereby the femur and acetabulum impinge anteriorly causing joint separation posteriorly. This levering was originally theorized at end range hip positions to explain the mechanism of injury for cartilage damage observed in the posterior aspect of the hip in patients with pincer-type FAI morphology (i.e., acetabular overcoverage).²⁵ While the full levering effect is unlikely during walking, it is plausible that an aspherical femoral head articulating within a relatively spherical acetabulum, as is the case in patients with cam FAI syndrome, could alter mechanics of the femoral head within the acetabulum. Furthermore, repetitive levering during activities requiring end range positions could produce capsular laxity, allowing for altered movement of the femoral head.^30-32 In a cadaveric study of hips without cam morphology, with the hip in 90° of flexion and applied internal and external rotation torques, translations as large as 4 mm have been measured,³⁰ twice the size of what we observed in vivo during walking. However, the cadaveric study represented an end range-of-motion activity unlike walking.

Alterations in muscle strength or neuromuscular control may also contribute to altered hip mechanics.⁹ Individuals with cam morphology and pain (and hence, FAI syndrome) have documented hip muscle weakness.^33-35 The activation patterns and coordination of hip muscles also appear to be altered.^36,37 Observed alterations could be related to the underlying morphology or to the symptoms of FAI syndrome as pain is known to affect movement patterns.³⁸ Additionally, Lawrenson and colleagues found that, among individuals with cam morphology, differences in muscle activation increased with increased severity of symptoms³⁹ suggesting that pain as well as morphology may affect joint mechanics. However, it is unclear if these alterations are positively adaptive or maladaptive – that is, if they are beneficial for the patient or contribute to the problem. As proposed by Radin for the knee,⁴⁰ altered neuromuscular coordination could contribute to altered loading, and ultimately contribute to pain and OA. Our study did not directly measure strength or muscle activation assessment; however, our measure of bone-to-bone distance directly quantified the bone movement which resulted from the individual’s muscle activation patterns. Future research should include measures of muscle function as recommended in a recent consensus statement.⁴¹

Limitations

As we measured bone-to-bone distance without consideration for the cartilage, it is possible that heterogeneity in the cartilage thickness may have contributed to the observed differences in the change in bone-to-bone distance.⁴² Additionally, owed to the fact that DF requires demanding and laborious processing, we included only a small number of participants. While DF and MBT provide accurate kinematics, it is possible that small errors in tracking could influence the measurements of bone-to-bone distance, and thus, results reported herein should be interpreted with caution. To reduce the likelihood of errors affecting our results, we used the same imaging, tracking, and post-processing procedures for patients and control participants. Patients were recruited from a single orthopaedic surgeon’s office and thus may not generalize to all patients with cam morphology. Our groups differed in both morphology and pain status; we cannot, therefore, disentangle the effect of morphology from the effect of other clinical symptoms including pain. To address these limitations, we are actively developing patient-specific finite element models that include cartilage and labrum anatomy and are driven from DF data; these models should clarify what effect larger changes in bone-to-bone distance over gait have on chondrolabral stresses and strains. As part of these studies, we plan to recruit asymptomatic individuals with cam morphology to better understand the influence of morphology on hip joint mechanics.

Conclusion

We measured the change in minimum bone-to-bone distance during level ground and 5° incline walking. During walking, hips with cam morphology exhibited altered hip joint articulation when compared to control hips, as evidenced by larger changes in minimum bone-to-bone distance. Additional research is needed to determine how altered mechanics in hips with cam FAI syndrome change load transmission of the hip, and contribute to pain, soft tissue damage, and osteoarthritis.

Supplementary Material

vS1

Supplemental Video 1. Bone-to-bone distance in a representative cam FAI syndrome patient and in a control participant throughout gait during level treadmill walking.