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SELECTED PROCEEDINGS FROM THE 2020 BERNESE HIP SYMPOSIUM GUEST EDITOR: KLAUS-ARNO SIEBENROCK MD

Does the Capital Femoral Physis Bony MorphologyDiffer in Children with Symptomatic Cam-type Femoroacetabular Impingement

Hosseinzadeh, Shayan MD; Novais, Eduardo N. MD; Emami, Alireza MD; Portilla, Gabriela BA; Maranho, Daniel A. MD, PhD; Kim, Young-Jo MD, PhD, MHCM; Kiapour, Ata M. PhD, MMSc

Author Information
Clinical Orthopaedics and Related Research: May 2021 - Volume 479 - Issue 5 - p 922-931
doi: 10.1097/CORR.0000000000001602

Abstract

Introduction

A cam-type morphology is an aspherical contour of the femoral head-neck junction that may lead to abnormal contact with the acetabular rim and symptomatic femoroacetabular impingement (FAI) syndrome [4]. Cam morphology may develop during rapid adolescent growth and has immediate and long-term implications, including pain, reduced hip function, and increased likelihood of hip osteoarthritis [5, 40]. Although the pathogenesis of cam-type FAI is most likely multifactorial, mechanical factors—mainly early participation in high-impact sports—seem to play a role [1, 22, 29, 30]. A greater prevalence of cam morphology was found in adolescent athletes practicing at the elite level in soccer [1, 37], football [13], basketball [30, 31], and ice hockey [26, 29] than in nonathletic individuals. The adaptive response of the growth plate under increased loads may lead to asymmetric supraphysiologic extension of the epiphysis on the femoral neck around the time of growth plate closure [1, 23, 30, 32]. Based on these observations, during normal growth of the epiphysis, supraphysiological physeal stress may lead to abnormal growth of epiphyseal extension in adolescents involved in sports activities [1, 28].

The epiphyseal tubercle, which is an eccentric, posterosuperior, beak-like inner projection into its metaphyseal fossa, along with peripheral growth of the epiphysis around the metaphysis (peripheral cupping), has been shown to play a major role in epiphyseal stability [2, 12, 14, 15, 25, 28-30, 34, 35]. These anatomic structures undergo developmental changes during skeletal growth, with the greatest changes occurring between 11 and 13 years [10, 22], which corresponds to the onset of cam morphology [5, 24]. Considering the important role these morphologic features play in stabilizing the epiphysis, any abnormalities of these features may lead to microinstability [18, 19] under high shear or impulsive loads (for example, loads that occur during sports activity) and result in the development of a cam morphology. Based on this theory, the development of high-risk morphology in the capital femoral epiphysis may explain why some children with early participation in high-impact sports will develop a cam morphology while others do not. Although most previous studies on cam-type FAI have mainly focused on overgrowth of the peripheral cupping with abnormal extension of the epiphysis [1, 21, 23, 25, 29-32], little is known about the detailed morphologic changes to the epiphyseal and metaphyseal surfaces in patients with cam deformities.

Therefore, we asked: (1) Does the CT-based bony morphology of the peripheral epiphyseal cupping differ between patients with a cam-type morphology and asymptomatic controls (individuals who did not have hip pain)? (2) Does the CT-based bony morphology of the epiphyseal tubercle differ between patients with a cam-type morphology and asymptomatic controls? (3) Does the CT-based bony morphology of the metaphyseal fossa differ between patients with a cam-type morphology and asymptomatic controls?

Patients and Methods

Participants

After obtaining institutional review board approval for this study, we retrospectively searched our institutional database for patients 8 to 15 years old with a diagnosis of an idiopathic cam morphology who underwent a preoperative CT evaluation of the affected hip between 2005 and 2018. Patients with slipped capital femoral epiphysis, developmental dysplasia of the hip, Perthes disease, previous fractures of the hip, or infection were not included in the search. Of 152 eligible patients, we excluded 136 due to lack of imaging data or prior disease history (Fig. 1). The choice of CT scanning versus MRI was solely based on the treating physicians’ preference.

F1
Fig. 1:
Search strategy and patient selection process in the FAI cohort.

We found 16 patients with a diagnosis of an idiopathic cam morphology in the setting of FAI syndrome who underwent preoperative pelvic CT. The median (range) age was 14 years (8 to 15), and 9 of 16 patients were boys. Six of 16 patients had a diagnosis of bilateral FAI syndrome, for whom we randomly selected one side to be included in the study, leading to a total of 11 right hips and five left hips. The diagnosis was made based on clinical symptoms of pain aggravated by sports in addition to clinical signs of FAI with a positive impingement test result (Flexion Adduction Internal Rotation [FADIR]), as well as radiographic confirmation of reduced femoral head-neck offset and/or an increased alpha angle. The mean ± SD alpha angle, which was assessed using sagittal or axial oblique sequences on MRI, was 59° ± 8°. All hips had chondral-labral lesions on MRI, with the exception of one hip with an evident cam lesion but no labral lesion. The mean tilt angle was 5° ± 7°, and no hip had signs of slipped capital femoral epiphysis on radiographs. Thirteen of 16 hips underwent surgical treatment of FAI through an arthroscopic or open (surgical hip dislocation) approach, and surgical findings confirmed the presence of a cam morphology and varying degrees of FAI-related injuries of the labrum and cartilage. Two hips with alpha angles less than 50° had FAI symptoms, and the surgical findings confirmed unequivocal cam morphology with labral and acetabular chondral FAI abnormalities. Three hips were treated nonoperatively until the date of data collection, as a decision was made to adjust sports activities to be less intense to minimize symptoms or postpone surgery. For the 10 participants with unilateral FAI, the uninvolved contralateral hips were also analyzed and used as internal controls.

Pelvic CT images of 80 participants with asymptomatic hips (50% female, 40 patients; mean age 11.5 ± 2.3 years), obtained in our institution from 2008 to 2010 because of suspected appendicitis, comprised the control group. This cohort was previously used in a study investigating age- and sex-related changes in epiphyseal morphology in normal hips [22]. We confirmed that the hips of participants in the control group were asymptomatic and normal in radiographic appearance by confirming the absence of hip pain through the medical records and by measuring the epiphyseal tilt angle, alpha angle, and acetabular index angle and comparing the measurements to the normative values [3, 21, 36]. None of the patients in either group had a history of systemic arthropathy, metabolic disorder, or hip injury.

Description of Experiment

CT images of each patient were segmented to generate a three-dimensional (3-D) model of the proximal femur using commercially available software (Mimics version 17.0, Materialise, Belgium). Segmented masks were used to create 3-D models of the proximal femoral epiphysis and metaphysis (Fig. 2A). An orthopaedic surgeon with 10 years of experience (DAM) segmented the CT images in a blinded manner. The reconstructed 3-D models were analyzed for alignment and anatomic measurements (3-matics software package version 9.0, Materialise, Belgium). A second-year orthopaedic surgery resident (SH) performed all measurements. An experienced orthopaedic surgeon (AE) and an experienced biomechanical researcher (AMK) independently reevaluated the segmented images, the reconstructed 3-D models, and the measurements to highlight any inconsistencies. No disagreements on segmentation and measurements were found between the observers.

F2
Fig. 2:
A-B (A) This image shows 3-D segmentation of CT images to reconstruct the proximal femur. (B) This image shows alignment of the segmented structures in 3-D. Images are adapted and modified with permission from Sage Publishing from Novais EN, Maranho DA, Kim YJ, Kiapour A. Age- and sex-specific morphologic variations of capital femoral epiphysis growth in children and adolescents without hip disorders. Orthop J Sports Med. 2018;6:2325967118781579, and from John Wiley and Sons from Hosseinzadeh S, Novais EN, Maranho DA, et al. Age- and sex-specific morphologic changes in the metaphyseal fossa adjacent to epiphyseal tubercle in children and adolescents without hip disorders. J Orthop Res. 2020;38:2213-2219.

Variables, Outcome Measures, Data Sources, and Bias

Our primary outcomes were the extent (height) of peripheral growth of the epiphysis around the metaphysis (peripheral cupping), the height of the epiphyseal tubercle (a beak-like prominence in the posterosuperior aspect of the epiphysis), and the depth of the metaphyseal fossa (a groove on the metaphyseal surface corresponding to the epiphyseal tubercle). Secondary outcomes included the length and width of epiphyseal tubercle and metaphyseal fossa. All the measurements were conducted on the 3-D models reconstructed from the CT scans based on the following techniques.

A best-fit sphere matching the curvature of the epiphyseal surface was used to determine the center and diameter of the epiphysis. We then established a plane parallel to the longitudinal axis of the femoral neck passing through the greater trochanter. The intersection of this plane and the epiphysis was defined as the superior aspect of the epiphysis. This point was used as the origin to establish a local coordinate system to conduct the epiphyseal measurements (Fig. 2B).

To quantify the peripheral cupping, the coronal and sagittal cross-sectional views through the center of the epiphysis were established. Epiphyseal cupping was defined as the distance between the highest peripheral point of the epiphysis in the superior, inferior, anterior, and posterior locations and the plane of the epiphyseal center (Fig. 3A). The average epiphyseal cupping was calculated as the mean of the peripheral cupping measured across the four anatomic locations. Epiphyseal tubercle dimensions were measured from coronal and sagittal cross-sectional views through the tubercle peak. Tubercle height was defined as the distance between the tubercle peak and the plane of the epiphyseal center (Fig. 3B). The metaphyseal fossa was defined as a depression on the metaphyseal surface corresponding to the epiphyseal tubercle on the epiphyseal surface (Fig. 3C).

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Fig. 3:
A-C These images show 3-D measurements of the morphology of (A) peripheral cupping, (B) epiphyseal tubercle, and (C) metaphyseal fossa. Images are adapted and modified with permission from Sage Publishing from Novais EN, Maranho DA, Kim YJ, Kiapour A. Age- and sex-specific morphologic variations of capital femoral epiphysis growth in children and adolescents without hip disorders. Orthop J Sports Med. 2018;6:2325967118781579, and from John Wiley and Sons from Hosseinzadeh S, Novais EN, Maranho DA, et al. Age- and sex-specific morphologic changes in the metaphyseal fossa adjacent to epiphyseal tubercle in children and adolescents without hip disorders. J Orthop Res. 2020;38:2213-2219.

Sagittal and coronal views through the deepest point of the fossa were selected to measure the fossa length (sagittal plane) and width (coronal plane). We measured the fossa depth as the distance between the deepest point of the fossa and the plane through the nadir points adjacent to the fossa (Fig. 3C). All measurements are presented as proportions because of normalization to the epiphyseal diameter, neutralizing the effects of individual variability in anatomic dimensions.

To assess within- and between-observer reliability and avoid recall bias, the same investigator (SH) and an independent investigator (AE) measured a random subset of 30 hips 4 weeks later. Variance estimates were used to compute the intraclass and interclass correlation coefficients. For all measurements, the intraclass correlation coefficient values for intraobserver and interobserver reliability were between 0.82 and 0.96 (Table 1).

Table 1. - Intraobserver and interobserver agreement, assessed by intraclass correlation coefficients, for quantified anatomic features (with 95% confidence intervals)
Anatomic feature Intraobserver reliability Interobserver reliability
Tubercle height 0.92 (0.84-0.96) 0.85 (0.73-0.90)
Tubercle width 0.95 (0.90-0.97) 0.90 (0.83-0.95)
Tubercle length 0.94 (0.89-0.97) 0.91 (0.84-0.95)
Fossa depth 0.89 (0.78-0.90) 0.82 (0.70-0.91)
Fossa width 0.94 (0.88-0.96) 0.91 (0.83-0.95)
Fossa length 0.95 (0.89-0.98) 0.90 (0.82-0.95)
Anterior cupping 0.96 (0.92-0.98) 0.88 (0.81-0.93)
Posterior cupping 0.92 (0.83-0.95) 0.89 (0.83-0.96)
Superior cupping 0.89 (0.80-0.91) 0.86 (0.75-0.92)
Inferior cupping 0.93 (0.89-0.95) 0.92 (0.83-0.96)

Statistical Analysis

A general linear model was used to compare the quantified anatomic features between hips with FAI and normal hips (controls) after adjusting for age and sex, which were entered into the model as covariates. The Wilcoxon matched-pairs signed rank test was used to compare the FAI hips with uninvolved contralateral hips in subjects with unilateral FAI (n = 10). All variables were defined as continuous, except sex, which was defined as a dichotomous variable in the model. All measurements are reported as percentages (normalized to epiphyseal diameter). The group differences in morphological measurements are presented as fold change (FAI/control) along with mean differences (FAI – Control) and 95% confidence interval in normalized measurements. All data in the graphs are shown as mean ± SD. All p values were two-sided and considered statistically significant at α = 0.05.

Results

Representative 3-D models of the epiphysis and metaphysis highlight distinct differences in peripheral cupping, epiphyseal tubercle, and metaphyseal fossa between asymptomatic controls and FAI cohorts (Fig. 4).

F4
Fig. 4:
A-B Representative 3-D models of the epiphysis and metaphysis of a (A) normal asymptomatic hip and (B) cam-type FAI hip. The white arrows indicate the peripheral cupping, black arrows indicate the epiphyseal tubercle, and blue arrows indicate the metaphyseal fossa. A color image accompanies the online version of this article.

Extent of Peripheral Cupping

After adjusting for age and sex, we found that hips with FAI had a 1.3-fold larger anterior cupping (adjusted mean difference 3.9% [95% CI 1% to 7%]; p = 0.003), 1.3-fold larger posterior cupping (adjusted mean difference 3.6% [95% CI 1% to 6%]; p = 0.007), 1.7-fold larger superior cupping (adjusted mean difference 5.9% [95% CI 3% to 9%]; p < 0.001), and 1.6-fold larger inferior cupping (adjusted mean difference 4.8% [95% CI 2% to 8%]; p = 0.001). The average peripheral cupping (mean of cupping measurements across all four regions) was 1.4-fold larger in the FAI group compared with controls (adjusted mean difference 4.6% [95% CI 2% to 7%]; p < 0.001; Fig. 5). There were no differences in any of the quantified aspects of peripheral cupping between the indexed and uninvolved contralateral sides in patients with unilateral FAI (see Fig. 1; Supplemental Digital Content 1, https://links.lww.com/CORR/A484).

F5
Fig. 5:
These graphs show age- and sex-adjusted comparisons of patients with normal hips and those with FAI in terms of (A) anterior cupping, (B) posterior cupping, (C) superior cupping, (D) inferior cupping, and (E) average cupping heights.

Epiphyseal Tubercle Size

After adjusting for age and sex, we found that hips with FAI had a 0.3-fold smaller tubercle height (adjusted mean difference -2.9% [95% CI -5% to 1%]; p = 0.01) and a 0.6-fold smaller tubercle length (adjusted mean difference -18.7% [95% CI -23% to -15%]; p < 0.001) than control hips. There was no difference in tubercle width between the groups (Fig. 6). In patients with unilateral FAI, the indexed hips had a smaller tubercle height and smaller tubercle length compared with the uninvolved contralateral side. There was no side-to-side difference in tubercle width in patients with unilateral FAI (see Fig. 2; Supplemental Digital Content 2, https://links.lww.com/CORR/A485).

F6
Fig. 6:
These graphs show age- and sex-adjusted comparisons between patients with normal hips and those with FAI in terms of (A) tubercle height, (B) tubercle length, and (C) tubercle width. Significant differences are highlighted in bold; p < 0.05.

Morphology of Metaphyseal Fossa

After adjusting for age and sex, we found that hips with FAI had a 1.9-fold larger fossa depth (adjusted mean difference 3.8% [95% CI 3% to 5%]; p < 0.001), 1.8-fold larger fossa length (adjusted mean difference 17.3% [95% CI 12% to 22%]; p < 0.001), and a 2.3-fold larger fossa width (adjusted mean difference 26.9% [95% CI 23% to 32%]; p < 0.001) than control hips (Fig. 7). In patients with unilateral FAI, the indexed hips had a larger fossa depth compared with the uninvolved contralateral side. There were no side-to-side differences in fossa width and length in patients with unilateral FAI (see Fig. 3; Supplemental Digital Content 3, https://links.lww.com/CORR/A486).

F7
Fig. 7:
These graphs show age- and sex-adjusted comparisons between patients with normal hips and those with FAI in terms of (A) fossa depth, (B) fossa length, and (C) fossa width.

Discussion

Cam-type FAI morphology of the proximal femur is believed to occur mostly during adolescence [8]. Excessive extension of the capital femoral epiphysis over the superior and anterior aspects of the metaphysis was described as a precursor of cam-type FAI morphology and is associated with vigorous sports participation by adolescent athletes [1, 16, 19, 29, 30, 39]. However, the anatomy of the inner surface of the capital femoral epiphysis has not been studied as well as the peripheral morphology in adolescents with cam-type FAI. We found that compared with normal asymptomatic controls, hips with cam-type FAI had larger peripheral cupping, smaller epiphyseal tubercle, and larger metaphyseal fossa after adjusting for age and sex. Interestingly, in patients with unilateral FAI, there were no side-to-side differences in peripheral cupping but smaller epiphyseal tubercle and larger metaphyseal fossa in the FAI side compared with the uninvolved contralateral side. Although preliminary, these findings suggest that the epiphyseal tubercle and its corresponding metaphyseal fossa, which have been shown to be major stabilizers of the epiphysis at early ages, may also be involved in the pathomechanism of cam-type FAI. Thus, further research and clinical observations on epiphyseal morphology in addition to the measurements of alpha angle may help identify the mechanisms and risk factors for cam-type FAI.

Limitations

We acknowledge there are several limitations to this study. First, small numbers in the FAI group precluded direct matching of patients who had FAI with patients without FAI based on sex and age. We tried to overcome this limitation by implementing appropriate statistical techniques to adjust the analysis by age and sex. We also conducted an additional analysis comparing the FAI side to the uninvolved contralateral side in patients with unilateral FAI. Even though our results suggest differences in the epiphyseal tubercle and the metaphyseal fossa between hips with cam-type FAI and asymptomatic controls, future prospective studies with larger sample size are essential to confirm these findings. Second, our control cohort (80 patients with asymptomatic, normal-looking hips who were imaged for suspected appendicitis) was retrospectively selected, which may have introduced some bias into the analysis. We tried to minimize the potential bias by randomly selecting the subjects and by performing a comprehensive review of the medical records and imaging data to ensure that the hips are normal and asymptomatic [22]. Third, segmentation of CT images was limited to the bony morphology, and our assessment of the cartilaginous morphology of the capital femoral epiphysis was limited. Although MRI would allow for a more comprehensive analysis of the cartilaginous morphology, establishing a control group would be challenging. Therefore, we compared CT images. It should be noted that a pelvic CT scan is not a routine modality to assess FAI in children due to its high radiation exposure, which is also another reason for the small sample size in the FAI cohort. Further studies with advanced MRI would be worthwhile for a better understanding of the anatomic surface of the capital epiphysis. The lack of physical activity data prohibited us from investigating the effect of physical activity levels on the development of cam-type morphology in our cohort. Finally, the study was cross-sectional; as such, we can only show association, but we have little ability to confirm our speculations regarding whether these morphological features cause the development of cam-type FAI. Although the side-to-side differences in epiphyseal tubercle and metaphyseal fossa size seen in patients with unilateral FAI may suggest that smaller tubercle and larger fossa possibly lead to development of cam morphology, further longitudinal studies with larger sample sizes are required to confirm the current findings and provide further details about the interplay between mechanical loading, epiphyseal morphology, and the development of cam morphology.

Extent of Peripheral Cupping

Our findings showed that patients with cam-type FAI deformities have larger peripheral cupping than control patients who did not have hip symptoms or radiographic signs of FAI, after adjusting for age and sex. These current findings are in agreement with prior reports on overgrowth of the epiphyseal extension around metaphysis in cam-type FAI [1, 21, 23, 25, 29-32]. With aging, peripheral cupping increases [15, 22, 35]. This impacts the mechanical stability of the epiphysis, and epiphysis stability progressively depends on peripheral cupping with increasing age, suggesting that this could be a compensatory mechanism. However, the response of increasing peripheral cupping in the superior and anterior aspects becomes pathologic as it leads to the development of cam morphology. The potential of capital epiphysis overgrowth as an epiphyseal stabilizer has been described as protective against slipped capital femoral epiphysis [20].

Epiphyseal Tubercle Size

Our findings showed that patients with a cam-type FAI morphology had a smaller tubercle than controls, after adjusting for age and sex. Interestingly, we also saw side-to-side differences in tubercle size in patients with unilateral FAI with a smaller tubercle in the FAI side compared with uninvolved contralateral side. The role of the tubercle as a stabilizer is directly related to its size [14]. During the first years of adolescence in patients younger than 12 years, the tubercle is a large, prominent structure and the stability of the epiphysis mainly depends on the tubercle, but the tubercle’s dimensions decrease with age [15, 22, 35]. During this transitional time (that is, from a tubercle-dependent stability model to a peripheral cupping–dependent stability model), a cam-type morphology develops. Vigorous sports participation during this transition period may suppress physiologic resistance to stress because of an interlocking mechanism between the epiphyseal tubercle and metaphyseal fossa. The relatively smaller epiphyseal tubercle observed in our study would further limit resistance to stress and contribute to potential microinstability at the growth plate. In this setting, an increase in peripheral cupping could be a compensatory response to maintain stability at the cost of increased epiphyseal extension into the metaphysis, leading to a cam-type morphology [14, 15, 22].

Morphology of Metaphyseal Fossa

Our findings also showed that patients with cam-type FAI deformities have a larger fossa than controls do, after adjusting for age and sex. Interestingly, we also saw side-to-side differences in fossa size in patients with unilateral FAI with larger fossa in the FAI side compared with the uninvolved contralateral side. The epiphyseal tubercle is close to its corresponding metaphyseal fossa and both act as an interlocking mechanism to stabilize the epiphysis [6, 7, 12, 27, 33, 38]. A previous study using a pig model showed that loads applied through the epiphysis force the tubercle to abut the medial aspect of the metaphyseal fossa [12]. A subsequent study showed that the tubercle and its fossa play a crucial role in the stability of the capital femoral epiphysis [11]. A larger fossa and smaller tubercle will lead to increased mismatch that may compromise the stability of the physis.

Clinical Relevance

These observations, at minimum, highlight the need for further longitudinal studies and comparative biomechanical models to investigate the cause-effect relationship between tubercle and fossa morphology with cam-type FAI pathogenesis. Those findings may lead to the development of new imaging biomarkers to predict the risk of FAI or to monitor its progression. Such tools are essential for more accurate risk prediction and to improve the decision-making process in the treatment of patients with cam-type FAI. Our findings also suggest pathogenic similarities of FAI with SCFE, in which the epiphyseal tubercle is smaller and the peripheral cupping is larger [9, 23]. Possibly, the supraphysiological stress across the growth plate in SCFE leading to potential microinstability [17-19] would also occur in FAI hips but with different deformity progression.

Conclusion

Hips with cam-type FAI have a smaller epiphyseal tubercle along with a larger metaphyseal fossa and larger peripheral cupping than controls without hip symptoms or radiographic signs of FAI. Because cam-type FAI develops during transitional stability of the capital femoral epiphysis from the epiphyseal tubercle to the peripheral cupping, the increased peripheral cupping observed in patients with FAI may be a response to insufficient stability provided by a small tubercle and a relatively large fossa. Adolescents participating in vigorous sports activities who have a smaller tubercle or larger metaphyseal fossa may be at higher risk of developing a cam-type morphology. Although future longitudinal prospective studies are needed to confirm these findings, this study suggests that detailed analysis of the physeal morphology, in addition to peripheral cupping overgrowth, can help understand cam-type FAI pathology and help better identify at-risk individuals who may benefit from surgical interventions or conservative treatments to lower the risk of FAI and associated joint degeneration.

Acknowledgments

We thank Roya Dastjerdi MD and Amishi Vairagade BS at Boston Children’s Hospital for assistance with data collection.

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