Secondary Logo

Journal Logo

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

A Cam Morphology Develops in the Early Phase of the Final Growth Spurt in Adolescent Ice Hockey Players: Results of a Prospective MRI-based Study

Hanke, Markus S. MD; Schmaranzer, Florian MD, PhD; Steppacher, Simon D. MD; Reichenbach, Stephan MD; Werlen, Stefan F. MD; Siebenrock, Klaus A. MD

Author Information
Clinical Orthopaedics and Related Research: May 2021 - Volume 479 - Issue 5 - p 906-918
doi: 10.1097/CORR.0000000000001603

Abstract

Introduction

Cam morphologies of the proximal femur may arise secondary to childhood diseases, including slipped capital epiphysis or Perthes disease, or secondary to previous trauma [4, 9, 14, 37, 50, 53]. The etiology of primary or so-called idiopathic cam morphologies remains unclear. Males have been reported to carry a fourfold increased risk for developing a cam morphology compared with females [16, 23, 32, 54]. Several studies have shown that high-impact sports during adolescence increase the prevalence of cam morphologies in young adults [1, 2, 7, 8, 26, 41, 42]. Most of these cross-sectional studies were performed in male adolescents and young men and included age-matched control groups. Typical sports activities with reported higher risks of cam morphologies include soccer, ice hockey, basketball, and, skiing [1, 28, 33, 41, 43]. The reported risk of cam morphologies ranged from 26% to 89% in athletes [1, 2, 15, 17, 19, 27, 32, 41–43]. It has been theorized that there might be a dose-response relationship between the amount of practice per week and later cam morphologies in adolescents [8]. Practicing soccer more than three times per week in patients younger than 12 years was associated with a higher risk of developing a cam morphology later when compared with players practicing less [49].

Because of the cross-sectional study design of most of the abovementioned reports, an accurately defined time period for appearance of the cam morphology is lacking. A cam morphology before the age of 12 to 13 years in male adolescents has seldom been reported on [1, 52]. Agricola et al. [2] re-examined the hips of adolescent soccer players with plain radiographs 2.4 years after the initial examination. There was a rather large age variation of the participants at time of inclusion with a mean (range) age of the soccer players of 14.5 years (12 to 19 years). These authors found a small increase of the alpha angle during adolescence [2], and identify adolescence as the time of morphological changes of the proximal femur. Regarding potential prophylactic measurements or early detection of clinically important cam morphologies leading to cartilage damage, there is a need to more accurately frame the vulnerable time span for the development of primary cam morphologies. Ideally, a longitudinal prospective study should start before any cam morphology has occurred, which typically seems to be up to 13 years of age in males [1, 52]. For this reason, we designed a prospective, longitudinal MRI study to monitor morphological changes during growth. Noncontrast MRI scans with radial cuts on the proximal femur have the advantage that they can detect the morphology in a more three-dimensional (3-D) way and the lesions can be detected more easily than on plain radiographs [20, 39, 47]. In addition, MRI can differentiate open from closed physes [13, 38] and can detect alterations in the shape of the physeal scar at the area of the cam morphologies [41, 44]. An increased epiphyseal extension toward the neck has been described in association with a cam morphology in patients with idiopathic cam lesions and in adolescents playing basketball or soccer [2, 41, 44]. The association of an extended physis and cam morphology may be a hint for underlying physeal damage as cause of the cam morphology.

We therefore asked the following questions: (1) What is the frequency of cam morphologies in adolescent ice hockey players, and when do they appear? (2) Is there an association between an extension of the physeal growth plate and the development of a cam morphology? (3) How often do these players demonstrate clinical findings like pain and lack of internal rotation?

Patients and Methods

We performed a prospective cohort study on adolescent male ice hockey players who were recruited on a voluntary basis at the local ice hockey club. They were all members of the local competitive ice hockey team up to the age of 13 years. The mean (range) age at enrollment was 12 ± 0.5 years (11 to 13 years). Inclusion criteria consisted of uninterrupted participation in the club’s program of ice hockey training sessions and games since the age of 8 years. Typical athletic activities were three training sessions or games per week for 9- to 12-year-old players, four or five games or training sessions per week for 13- to 15-year-old players, and up to eight training sessions or games per week for players 16 years and older. The study protocol assigned the right hip for examination in participants with an even-numbered birthday and the left hip in participants with an odd-numbered birthday. Because the morphology of the femur and pelvis in girls is clearly distinct from the morphology in boys, and therefore the mechanism of femoroacetabular impingement differs, only male volunteers were included in the current study [6]. Thirty-five players fulfilled the study inclusion criteria, but 10 players declined to participate (Fig. 1). Twenty-five players were included in the study and none had previous hip surgery or a history of hip disease (such as slipped capital femoral epiphysis or Perthes disease). There were 13 left hips and 12 right hips. Two participants (two hips) refused the latest follow-up; both participants had stopped playing ice hockey for reasons unassociated with hip problems (for example, groin pain). One participant (one hip) became symptomatic and developed anterior hip pain with a cam morphology at the 1.5-year follow-up interval. This participant was included in the statistical analysis of the overall prevalence of cam morphologies at 3-year follow-up. This individual underwent hip arthroscopy with bilateral femoral osteochondroplasty (Fig. 2). The remaining 22 players (22 hips) completed clinical and radiologic follow-up at 3 years.

F1
Fig. 1:
This image shows the selection of participants, including the association of the examinations and the growth spurt.
F2
Fig. 2.:
A-C (A) At the baseline examination, no cam morphology was visible on MRI. At 1.5 years of follow-up, the participant complained about anterior groin pain and limited internal rotation, and (B) MR arthrography (because of clinical presentation) showed a cam morphology with an extended proximal femoral epiphysis (arrow). (C) This MR image was taken after arthroscopic anterosuperior femoral osteochondroplasty (double arrow).

All study participants completed a questionnaire and underwent a clinical examination and MRI at the time of enrollment and each follow-up examination. Follow-up MRI and examinations were performed 1.5 and 3 years after enrollment (Fig. 1). The questionnaire focused on the start of ice hockey training, the frequency of training per week, and the location and severity of pain in the hip, groin, greater trochanter, buttocks, or lower back within the past 6 months.

The physical examination focused on (1) a limited internal rotation with the hip and knee flexed to 90° and (2) the anterior impingement test [35, 36, 51], which is performed with combined hip flexion, adduction, and internal rotation. The anterior impingement test was considered positive when a sharp pain in the groin or anterolateral hip area was produced with more than 60° hip flexion. One of the authors (MSH) performed the clinical examination.

MR Techniques and Image Analysis

All participants underwent repeated noncontrast MRI of the hip on the same 3T scanner (Siemens Skyra, Siemens, Erlangen, Germany). The imaging protocol included axial sequences of the pelvis and distal femoral condyles. To assess the proximal femoral anatomy, radial two-dimensional (2-D) proton density-weighted turbo spin-echo images were acquired, which were aligned with the femoral neck axis and included the following sequence parameters: repetition time/echo time 1800/14 ms, 4-mm slice thickness, 150° flip angle, 16-cm field of view, 403 x 448 matrix size, and acquisition time of 04:24 minutes for 14 images.

The clockface system was applied for orientation around the femoral-neck axis [21]. The center of the greater trochanter identified the 12 o’clock position of the femoral head-neck junction. Anterior was defined as 3 o’clock in both right and left hips (Fig. 3). The subsequent radial slices were defined in clockwise directions around the femoral head-neck axis for right hips and counterclockwise for left hips. All MRI measurements were performed with the commercially available DICOM viewer OSIRIX (Pixmeo SARL, Bernex, Switzerland).

F3
Fig. 3.:
This image shows the 3-D morphology of the femoral head, proximal femoral epiphysis, and head-neck junction, which were assessed using hip radial images. The clockface system was applied for orientation around the femoral-neck axis [21]. The center of the greater trochanter served to determine the 12 o’clock position of the femoral head-neck junction. Anterior was defined as 3 o’clock in the right and left hips. Reprinted with permission from Steppacher SD, Tannast M, Werlen S, Siebenrock KA. Femoral morphology differs between deficient and excessive acetabular coverage. Clin Orthop Relat Res. 2008;466:782-790. Available at https://journals.lww.com/clinorthop/pages/articleviewer.aspx?year=2008&issue=04000&article=00005&type=Fulltext.

The 3-D morphology of the femoral head, proximal femoral epiphysis, and head-neck junction was assessed using radial images of the hip and two previously published and validated radiographic parameters: alpha angle [31] (validated by Steppacher et al. [46] with an intraclass correlation coefficient [ICC] of 0.86 for intraobserver reliability and 0.81 for interobserver reliability) and epiphyseal extension [44] (validated by Agricola et al. [2] with an ICC of 0.97 for intraobserver reliability and 0.97 for interobserver reliability) (Fig. 4). All radiographic parameters were assessed circumferentially around the femoral-neck axis for all three examinations for each participant. The alpha angle was used to quantify head-neck sphericity (Fig. 4A) [31]. Based on the midpoint of the two neck diameters and independently from the center of the femoral head, the true femoral-neck axis was determined [25]. An alpha angle threshold of 60° according to Agricola et al. [3] was used to define the presence of a cam morphology. The growth pattern and the tilt of the epiphysis was evaluated by measuring the epiphyseal extension (Fig. 4B) [44].

F4
Fig. 4.:
A-B (A) The alpha angle was defined by the femoral head-neck axis and a line passing through the center of the femoral head and the point where the anterior head-neck contour exceeded the head radius. (B) The epiphyseal extension was formed according to the initial description of Siebenrock et al. [41]: (1) the head-neck axis was drawn through the center of the femoral head to the medial femoral head; (2) a line orthogonal to this axis was drawn starting at the medial femoral head toward the clock position being measured; (3) the distance between this line and the physeal extension was measured, parallel with the head-neck axis; and (4) (e) this distance was divided by (d) the femoral head diameter to express the epiphyseal extension as a ratio.

The status of the capital growth plate (open versus closed) was evaluated for all three examinations for each participant. The capital growth plate was considered closed on proton-weighted sequences when it was represented only by a complete black line similar to the cortical or sclerotic bone and lack of increased signal on the T2 or Trufisp sequences [42]. An open physis typically presents with a bright signal on T2 or Trufisp sequences, indicating a higher water content and/or cartilage [12, 13, 38].

Ethical Approval

We obtained ethical approval for this study from the local ethical committee, Kantonale Ethikommission Bern (KEK-Gesuchs-Nr.:205/12). We also acquired written consent from each participant and from one of the parents (for legal reasons).

Statistical Analysis

Normal distribution was confirmed with the Kolmogorov-Smirnov test. For comparison between the three time points, we used paired t-tests. We used Bonferroni correction for multiple comparisons to compare the three time points (p = 0.05/3 = 0.017 as adjusted level of significance). Binominal data were assessed with the Fisher exact test. To correlate values of the epiphyseal extension and alpha angle at each measurement time point, we used the Spearman rank correlation test.

Results

Frequency and Timing of Appearance of Cam Morphologies

At the baseline examination, none of the 25 players showed evidence of a cam morphology (defined as an alpha angle greater than 60° [3, 47]) at any measured location. Cam morphologies were most apparent at the 1.5-year follow-up interval (10 of 25; baseline versus 1.5-year follow-up: p = 0.007) and a few more occurred between 1.5 and 3 years (12 of 23; 1.5-year follow-up versus 3-year follow-up: p = 0.14; baseline versus 3-year follow-up: p = 0.003).

Physis Changes Associated with Cam Morphologies

During the study period, the alpha angle (Table 1) increased predominantly within the anterosuperior quadrant (most pronounced at the 2 o’clock position: baseline 45° ± 7°, 1.5-year follow-up 52° ± 7°, 3-year follow-up 59° ± 10°; baseline versus 1.5-year follow-up: p < 0.001; baseline versus 3-year follow-up: p < 0.001; 1.5-year versus 3-year follow-up: p = 0.004) (Fig. 5A). The epiphyseal extension toward the neck also increased predominantly in the anterosuperior quadrant (1 o’clock position: baseline 0.68 ± 0.07, 1.5-year follow-up 0.70 ± 0.05, 3-year follow-up 0.74 ± 0.08; baseline versus 1.5-year follow-up: p = 0.10; baseline versus 3-year follow-up: p = 0.01; 1.5-year versus 3-year follow-up: p = 0.03) (Fig. 5B). When evaluating the hips at 3-year follow-up, there was a positive correlation between increased epiphyseal extension and a high alpha angle at the anterosuperior quadrant (1 o’clock to 3 o’clock) (Spearman correlation coefficient = 0.341; p < 0.003) (Fig. 6).

Table 1. - Mean difference between the time points per clock position of the alpha angles
Time points Position
12 o’clock 1 o’clock 2 o’clock 3 o’clock 4 o’clock 5 o’clock 6 o’clock 7 o’clock 8 o’clock 9 o’clock 10 o’clock 11 o’clock
Baseline versus 1.5-year follow-up 1 ± 2 (95% CI -2 to 5; 0.43) 5 ± 2 (95% CI 2 to 9; 0.003) 6 ± 1 (95% CI 4 to 9; < 0.001) 7 ± 2 (95% CI 3 to 1 0; < 0.001) 4 ± 2 (95% CI 1 to 7; 0.02) 4 ± 1 (95% CI 2 to 7; 0.002) 4 ± 1 (95% CI 2 to 7; 0.004) 4 ± 1 (95% CI 2 to 6; < 0.001) 0 ± 2 (95% CI -3 to 4; 0.86) -1 ± 1 (95% CI -3 to 1; 0.55) -3 ± 3 (95% CI -9 to 2; 0.56) 0 ± 2 (95% CI -3 to 2; 0.72)
Baseline versus 3-year follow-up 1 ± 1 (95% CI -1 to 4; 0.34) 9 ± 2 (95% CI 4 to 14; 0.001) 13 ± 2 (95% CI 8 to 18; < 0.001) 9 ± 1 (95% CI 5 to 12; < 0.001) 4 ± 1 (95% CI 2 to 6; < 0.001) 2 ± 1 (95% CI -1 to 5; 0.34) 2 ± 1 (95% CI 0 to 5; 0.09) 4 ± 1 (95% CI 2 to 7; < 0.001) -1 ± 2 (95% CI -4 to 3; 0.58) -2 ± 1 (95% CI -4 to 0; 0.26) -4 ± 2 (95% CI -9 to 1; 0.06) 0 ± 1 (95% CI -2 to 3; 0.77)
1.5-year versus 3-year follow-up 1 ± 1 (95% CI -1 to 3; 0.48) 3 ± 2 (95% CI -2 to 8; 0.30) 7 ± 3 (95% CI 1 to 12; 0.004) 1 ± 1 (95% CI -2 to 4; 0.38) 0 ± 2 (95% CI -4 to 4; 0.90) -3 ± 1 (95% CI -6 to 0; 0.04) -2 ± 2 (95% CI -6 to 1; 0.16) 0 ± 1 (95% CI -2 to 3; 0.95) -2 ± 2 (95% CI -5 to 2; 0.33) -2 ± 1 (95% CI -3 to 0; 0.09) -1 ± 2 (95% CI -5 to 3; 0.17) 2 ± 1 (95% CI -1 to 4; 0.19)
Data are presented as the mean ± SD (95% CI; p value).

F5
Fig. 5.:
A-B (A) This graph shows the alpha angle around the femoral-neck axis. Anterosuperiorly, the alpha angle increased the most and mainly between baseline and 1.5 years of follow-up. At the 2 o’clock position, the alpha angle further increased until 3 years of follow-up. (B) This graph shows the epiphyseal extension around the femoral-neck axis. Anterosuperiorly, the epiphyseal extension increased the most. *p < 0.005.
F6
Fig. 6.:
This scatterplot with a linear regression line shows the relationship between the alpha angle and the epiphyseal extension in the anterosuperior quadrant at 3 years of follow-up (1 o’clock through 3 o’clock positions).

At the baseline examination, all 25 players presented with an open capital femoral physis. Complete capital femoral physis closure occurred most often in the interval between the 1.5-year follow-up (1 of 25) and the 3-year follow-up (18 of 22; p < 0.001). Four players had incomplete closure of the capital femoral physis. Two of these four individuals with a partially open physis presented with an alpha angle greater than 60°.

Clinical Findings: Pain and Restricted Internal Rotation

Internal rotation and flexion decreased during the study period. At the baseline examination, no individual demonstrated pain on any impingement test or had internal rotation of less than 20° (Table 2). The prevalence of pain on the impingement test and/or restricted internal rotation less than 20° increased most between 1.5-year (1 of 25) and the 3-year follow-up (6 of 22; p = 0.02). Five individuals with an alpha angle greater than 60° at the last follow-up examination had internal rotation less than 20°, whereas none of the players with normal alpha angles showed restricted internal rotation. Two individuals with an alpha angle greater than 60° at the last follow-up interval had a positive anterior impingement test result, compared with only negative impingement test results in the hips with a normal alpha angle. The mean internal rotation was 17° ± 9° in players with an abnormal alpha angle compared with a mean internal rotation of 28° ± 8° in hips with a normal alpha angle (p = 0.01).

Table 2. - Demographic and clinical data
Parameter Baseline 1.5-year follow-up 3-year follow-up p value (baseline versus 1.5-year follow-up) p value (baseline versus 3-year follow-up) p value (1.5-year versus 3-year follow-up)
Age in years 12.4 ± 0.5 14 ± 0.5 15.5 ± 0.6
Height in m 1.5 ± 0.1 1.6 ± 0.1 1.7 ± 0.1
Weight in kg 40 ± 7 50 ± 9 61 ± 8
BMI in kg/m2 18 ± 2 19 ± 2 21 ± 2
Complete capital femoral physis closure, percent positive 0 4 (1 of 25) 82 (18 of 26) 0.32 <0.001 <0.001
Anterior impingement test result and/or IR < 20°, percentage positive 0 4 (1 of 25) 27 (6 of 22) 0.33 0.01 0.02
ROM 42 ± 11 45 ± 16 23 ± 10 0.25 <0.001 <0.001
 Internal rotation in 90° of flexion in °
Continuous values are expressed as the mean ± SD.

Discussion

High-impact sports such as soccer, basketball, and ice hockey during adolescence are a risk factor for the development of cam morphology of the proximal femur [1, 27, 32, 41, 43]. So far, it has remained unclear at which age the cam morphology actually develops. The present study demonstrated that a cam morphology develops during the early phase of the growth spurt. At the final examination, at a mean age of 16 ± 0.6 years, a cam morphology was present in 12 of 23 hips. A local extension of the epiphyseal portion in the same area was associated with the appearance of a cam morphology at the anterosuperior head-neck junction. This finding may indicate an underlying alteration of the capital physis. At final clinical examination, six players with a cam morphology had an abnormal clinical finding in terms of a painful impingement test or a limited internal rotation of the hip of less than 20°. The daily practice now includes further MRI imaging in ice hockey players with a positive impingement test or restricted IR.

Limitations

There are several limitations to this study. First, we were not able to recruit an age- and sex-matched control group. This was because of parental refusal to have their asymptomatic children undergo repeated technical imaging examinations. The reported prevalence of cam morphologies in nonathletic control groups of a similar age group is distinctly lower (8%-17%) than found in the present study [1, 20, 42]. However, the question of when cam morphologies do appear in control groups remains unanswered. Second, this study only examined ice hockey players who were boys (or young men). This is because males are more prone to develop cam morphologies than females [16, 23, 32, 54]. Thus, the study results do not apply to adolescent girls performing high-level sports. Third, because of the study design, 4 of 22 participants did not show complete closure of the physeal growth plate at latest follow-up. In theory, cam morphologies still might evolve until complete growth plate closure. Thus, the study might have underestimated the number of relevant cam morphologies. However, the high prevalence of cam morphologies at the latest examination is two to three times higher when compared with reported rates in control groups [8, 20]. Fourth, because of concerns of our ethical board about radiation exposure of these adolescent individuals, we were unable to perform conventional radiographic examinations and calculate the biological instead of the chronological bone age in this study. However, in daily practice, the knowledge about the most vulnerable phase for cam development during the chronological period between 13 to 16 years of age is the most important information. Early screening and further diagnostic tests for cam morphologies, if necessary, should focus on this life period. Fifth, most previously published studies were based on conventional radiographs and comparison of their results with MRI-based imaging may be limited [1, 2, 15, 19]. Radial MRI scan sections can depict a cam morphology circumferentially at the femoral head-neck junction, which conventional radiographs in two planes may miss and underestimate [10, 11, 20, 39, 47]. Thus, radial MRI scans seem to be the more accurate method for depicting a cam morphology. In addition, MRI may depict abnormalities in shape before ossification is complete (Fig. 7A-C) [22].

F7
Fig. 7.:
A-C (A) At the baseline examination, at the age of 12 years, no evidence of a cam morphology was apparent. (B) At 1.5 years of follow-up, soft-tissue apposition at the anterosuperior head-neck junction was visible, creating a cam morphology (arrow). The epiphysis showed no clear extension (*). (C) At the 3-year follow-up examination, clear extension of the anterosuperior proximal epiphysis (*) was visible, leading to a cam morphology (double arrow).

Another limitation is that acetabular morphology and its potential influence have not been evaluated. To the authors, noncontrast MRI scans alone without plain radiographs of the hip and pelvis are not sufficient to reliably determine dysplasia or acetabular version. The study only answered the questions about timing and frequency of morphological changes within the femur. Morphological influences from the acetabular side cannot be excluded but would need an extended study protocol. In addition, intraarticular damage like cartilage and labral lesions were not reported in the current study. A reliable evaluation of intraarticular damage should be done using contrast MRI [40, 45, 48] as a gold standard, which the local ethical committee would not have permitted in asymptomatic volunteers.

Frequency and Timing of Appearance of Cam Morphologies

Cam morphologies predominantly developed during the early phase of the final growth spurt. An abnormally high alpha angle has seldom been described in previous studies in athletes before the age of 13 years [1, 42, 43]. This finding was confirmed by the present study, where none of the young ice hockey players had an abnormally high alpha angle (> 60°) at a mean age of 12 ± 0.5 years. At the baseline examination, all femoral capital physes were open as represented by a thorough bright enhancement line on T2-weighted and a black line on proton density MRI images [13, 38]. Agricola et al. [2] found the highest increase in flattening of the head-neck junction (rise from 14% to 50%) in a subgroup of 12- to 13-year-old preprofessional soccer players (n = 63) with an open growth plate at the basic examination. The findings were based on a prospective cohort study with a 2.4-year follow-up radiographic examination of the hip in soccer players ranging from 12 to 19 years. Agricola et al. [2] reported a mean progression of the alpha angle of 2° with no further progression after complete growth plate closure. The present study and the findings from other authors [1, 2, 52] suggest an early vulnerable phase for the development of a cam morphology when the growth plate starts to close in boys around 13 years of age.

In the present study, the frequency of a cam morphology was 12 of 23 at the most recent examination. In four hips (18%), the growth plate was not completely closed, which might underestimate the ultimate rate of cam morphologies. However, the findings are consistent with a previous reported frequency of 56% cam morphologies in a different ice hockey player cohort from the same club measured with the same MRI technique [43]. In predominantly cross-sectional studies, the prevalence of cam morphologies in high-impact sports such as soccer, football, basketball, ice hockey, and skiing range from 26% to 89% [1, 27, 32, 41, 43, 49]. The large variation in reported frequencies partially is due to the use of different thresholds for an abnormal alpha angle (50°-60°) and the use of different techniques for detecting cam morphologies (MRI versus plain radiographs) (Table 3) [1, 10, 11, 27, 32, 42, 43, 43, 49]. However, one may assume that the type of sports and training exercises also might play an important role in the appearance and frequency of cam morphologies [29].

Table 3. - Selected literature on the association of sport and cam morphology
Author Study design Imaging modality Type of sport Threshold alpha angle Number of hips (number of patients) Follow-up, months Results
Siebenrock et al. [42] Case-control MRI Basketball/no sport > 55° 72 (37)/76 (38) NA Overall, the athletes had a 10-fold increased likelihood of having a cam morphology. After physeal closure 89% of the basketball players showed cam morphologies versus 9% in the control group.
Nepple et al. [27] Retrospective review Radiograph American football > 50° 123 (107) NA Radiographic evidence of cam FAI (abnormal alpha angle or decreased head-neck offset) was present in 72% of hips.
Agricola et al. [1] Cross-sectional Radiograph Soccer > 60° 178 (89) NA Cam morphologies were recognizable and present from the age of 13 years and were more prevalent in soccer players than in their nonathletic peers. A cam morphology tended to be more prevalent in soccer players (26%) than in controls (17%).
Philippon et al. [32] Cohort study MRI Ice hockey/ski ≥ 55° 61 (61)/27 (27) NA Cam morphology present in the ice hockey group in 75% compared with 42% in the skier group.
Siebenrock et al. [43] Cross-sectional MRI Ice hockey > 55° 77 (77) NA After physeal closure, a cam morphology at any measurement position was found in 56% of hips. In hips with an open physis, a cam morphology was found in 6%.
Siebenrock et al. [41] Case-control MRI Basketball/no sport > 55° 72 (37)/76 (38) 12 Correlation between a cam morphology and greater epiphyseal extension in the anterosuperior femoral head quadrant.
Carsen et al. [8] Cross-sectional MRI NA > 50° 88 (44) NA Cam morphology was present exclusively in the closed physeal group. Daily activity level was higher for patients with cam morphology.
Agricola et al. [2] Cohort study Radiograph Soccer > 60° 126 (63) 24 In boys aged 12 and 13 years at baseline, the prevalence of a flattened head-neck junction increased significantly during follow-up (13.6% to 50%). The amount of growth plate extension was significantly associated with the alpha angle.
Tak et al. [49] Cross-sectional Radiograph Soccer > 60° 126 (63) NA The prevalence of a cam morphology was 40% in players who started playing football from the age of 12 years or older, and 64% in those playing football before the age of 12 years.
Van Klij et al. [52] Cohort study Radiograph Soccer ≥ 60° 98 (49) 60 Cam morphology developed from 12 to 13 years of age until growth plate closure around 18 years.
Polat et al. [33] Cohort study Radiograph Soccer > 55° 214 (214) NA The prevalence of FAI was higher in players who had been playing football for 3 years or more and who had been training for 12.5 hours/week or more.
NA = not applicable; FAI = femoroacetabular impingement.

Physis Changes Associated with Cam Morphologies

The extension of the epiphysis toward the neck during the final growth spurt increased most distinctly in the anterosuperior head-neck quadrant (Fig. 5B). This head-neck quadrant represents the area where the cam morphology developed and a moderate positive correlation between cam and epiphyseal extension could be found (Fig. 6). The data confirm previous studies in young athletes showing a correlation between an increase in epiphyseal extension and cam development on MRI or plain radiographs [41, 44]. In contrast to a previous assumption that epiphyseal extension may precede the cam morphology, the present and a previously published prospective study [2] suggest that the two findings rather occur simultaneously during growth plate closure. The open question remains whether there is a causative link between the two observations. Theoretically, a cam morphology may be triggered by an abnormal physiological stimulus leading to a growth plate alteration or vice versa.

Clinical Findings: Pain and Restricted Internal Rotation

Pain on an anterior impingement test and/or an internal rotation of the hip of less than 20° at final examination was seen in 6 of 22 hips. In hips with a proven cam morphology, clinical findings were seen in 5 of 11 participants, one of whom underwent surgery for symptomatic cam impingement with cartilage damage. A positive anterior impingement test in hips with a relevant cam morphology (alpha angle > 60°) is suspicious for symptomatic impingement with potential cartilage damage and needs further adequate diagnostic imaging and potential surgery [5, 18, 24, 28, 35, 36, 42, 51]. Similarly, a restricted internal rotation (< 20°) with the hip flexed to 90° often has been associated with a cam morphology [30, 43]. In a large study in 244 asymptomatic young males, Reichenbach et al. [34] reported a prevalence of a cam morphology in 48% when internal rotation was less than 30°. We believe that the four hips without pain on an impingement test but with a restricted internal rotation (< 20°) must be considered hips at risk for developing symptomatic cam impingement.

Conclusion

Our data suggest that a cam morphology develops during the early phase of the final growth spurt of the femoral head in adolescent ice hockey players. Ten of 25 players already showed a relevant cam morphology at a mean age of 14 years. At the site of the cam morphology, we found a correlation with an increased extension of the physeal growth plate toward the femoral neck. Further high-resolution or biochemical MRI imaging studies might help to determine whether there is a causal link between a growth plate alteration and the appearance of a cam morphology based on vigorous sports activities. Clinical findings (pain on impingement test, restricted internal rotation < 20°) in 6 of 22 participants at the age of 16 years are a concern. These hips seem at risk for developing early cartilage damage. As a consequence, we now perform routine screening of young ice hockey players, with further diagnostic imaging in painful hips and yearly clinical controls in hips with a restricted internal rotation (< 20°).

References

1. Agricola R, Bessems JHJM, Ginai AZ, et al. The development of cam-type deformity in adolescent and young male soccer players. Am J Sports Med. 2012;40:1099-1106.
2. Agricola R, Heijboer MP, Ginai AZ, et al. A cam deformity is gradually acquired during skeletal maturation in adolescent and young male soccer players: a prospective study with minimum 2-year follow-up. Am J Sports Med. 2014;42:798-806.
3. Agricola R, Waarsing JH, Thomas GE, et al. Cam impingement: defining the presence of a cam deformity by the alpha angle: data from the CHECK cohort and Chingford cohort. Osteoarthritis Cartilage. 2014;22:218-225.
4. Albers CE, Steppacher SD, Haefeli PC, et al. Twelve percent of hips with a primary cam deformity exhibit a slip-like morphology resembling sequelae of slipped capital femoral epiphysis. Clin Orthop Relat Res. 2015;473:1212-1223.
5. Beaulé PE, Hynes K, Parker G, Kemp KA. Can the alpha angle assessment of cam impingement predict acetabular cartilage delamination? Clin Orthop Relat Res. 2012;470:3361-3367.
6. Bixby SD, Kienle K-P, Nasreddine A, Zurakowski D, Kim Y-J, Yen Y-M. Reference values for proximal femoral anatomy in adolescents based on sex, physis, and imaging plane. Am J Sports Med. 2013;41:2074-2082.
7. Bizzini M, Notzli HP, Maffiuletti NA. Femoroacetabular impingement in professional ice hockey players: a case series of 5 athletes after open surgical decompression of the hip. Am J Sports Med. 2007;35:1955-1959.
8. Carsen S, Moroz PJ, Rakhra K, et al. The Otto Aufranc Award. On the etiology of the cam deformity: a cross-sectional pediatric MRI study. Clin Orthop Relat Res. 2014;472:430-436.
9. Castañeda P, Ponce C, Villareal G, Vidal C. The natural history of osteoarthritis after a slipped capital femoral epiphysis/the pistol grip deformity. J Pediatr Orthop. 2013;33(suppl 1):S76-82.
10. Domayer SE, Ziebarth K, Chan J, Bixby S, Mamisch TC, Kim YJ. Femoroacetabular cam-type impingement: diagnostic sensitivity and specificity of radiographic views compared to radial MRI. Eur J Radiol. 2011;80:805-810.
11. Dudda M, Albers C, Mamisch TC, Werlen S, Beck M. Do normal radiographs exclude asphericity of the femoral head-neck junction? Clin Orthop Relat Res. 2009;467:651-659.
12. Dvorak J, George J, Junge A, Hodler J. Age determination by magnetic resonance imaging of the wrist in adolescent male football players. Br J Sports Med. 2007;41:45-52.
13. Ecklund K, Jaramillo D. Patterns of premature physeal arrest: MR imaging of 111 children. AJR Am J Roentgenol. 2002;178:967-972.
14. Eijer H, Myers SR, Ganz R. Anterior femoroacetabular impingement after femoral neck fractures. J Orthop Trauma. 2001;15:475-481.
15. Gerhardt MB, Romero AA, Silvers HJ, Harris DJ, Watanabe D, Mandelbaum BR. The prevalence of radiographic hip abnormalities in elite soccer players. Am J Sports Med. 2012;40:584-588.
16. Gosvig KK, Jacobsen S, Sonne-Holm S, Palm H, Troelsen A. Prevalence of malformations of the hip joint and their relationship to sex, groin pain, and risk of osteoarthritis: a population-based survey. J Bone Joint Surg Am. 2010;92:1162-1169.
17. Johnson AC, Shaman MA, Ryan TG. Femoroacetabular impingement in former high-level youth soccer players. Am J Sports Med. 2012;40:1342-1346.
18. Johnston TL, Schenker ML, Briggs KK, Philippon MJ. Relationship between offset angle alpha and hip chondral injury in femoroacetabular impingement. Arthroscopy. 2008;24:669-675.
19. Kapron AL, Anderson AE, Aoki SK, et al. Radiographic prevalence of femoroacetabular impingement in collegiate football players: AAOS exhibit selection. J Bone Joint Surg Am. 2011;93:e111(1-10).
20. Kienle K-P, Keck J, Werlen S, Kim Y-J, Siebenrock K-A, Mamisch TC. Femoral morphology and epiphyseal growth plate changes of the hip during maturation: MR assessments in a 1-year follow-up on a cross-sectional asymptomatic cohort in the age range of 9-17 years. Skeletal Radiol. 2012;41:1381-1390.
21. Klenke FM, Hoffmann DB, Cross BJ, Siebenrock KA. Validation of a standardized mapping system of the hip joint for radial MRA sequencing. Skeletal Radiol. 2015;44:339-343.
22. Kushdilian MV, Ladd LM, Gunderman RB. Radiology in the study of bone physiology. Acad Radiol. 2016;23:1298-1308.
23. Laborie LB, Lehmann TG, Engesæter IØ, Eastwood DM, Engesæter LB, Rosendahl K. Prevalence of radiographic findings thought to be associated with femoroacetabular impingement in a population-based cohort of 2081 healthy young adults. Radiology. 2011;260:494-502.
24. Mullins K, Hanlon M, Carton P. Differences in athletic performance between sportsmen with symptomatic femoroacetabular impingement and healthy controls. Clin J Sport Med. 2018;28:370-376.
25. Murgier J, Espié A, Bayle-Iniguez X, Cavaignac E, Chiron P. Frequency of radiographic signs of slipped capital femoral epiphysiolysis sequelae in hip arthroplasty candidates for coxarthrosis. Orthop Traumatol Surg Res. 2013;99:791-797.
26. Murray RO, Duncan C. Athletic activity in adolescence as an etiological factor in degenerative hip disease. J Bone Joint Surg Br. 1971;53:406-419.
27. Nepple JJ, Brophy RH, Matava MJ, Wright RW, Clohisy JC. Radiographic findings of femoroacetabular impingement in National Football League Combine athletes undergoing radiographs for previous hip or groin pain. Arthroscopy. 2012;28:1396-1403.
28. Nepple JJ, Carlisle JC, Nunley RM, Clohisy JC. Clinical and radiographic predictors of intra-articular hip disease in arthroscopy. Am J Sports Med. 2011;39:296-303.
29. Nepple JJ, Vigdorchik JM, Clohisy JC. What is the association between sports participation and the development of proximal femoral cam deformity? A systematic review and meta-analysis. Am J Sports Med. 2015;43:2833-2840.
30. Neumann M, Cui Q, Siebenrock KA, Beck M. Impingement-free hip motion: the “normal” angle alpha after osteochondroplasty. Clin Orthop Relat Res. 2009;467:699-703.
31. Nötzli HP, Wyss TF, Stoecklin CH, Schmid MR, Treiber K, Hodler J. The contour of the femoral head-neck junction as a predictor for the risk of anterior impingement. J Bone Joint Surg Br. 2002;84:556-560.
32. Philippon MJ, Ho CP, Briggs KK, Stull J, LaPrade RF. Prevalence of increased alpha angles as a measure of cam-type femoroacetabular impingement in youth ice hockey players. Am J Sports Med. 2013;41:1357-1362.
33. Polat G, Arzu U, Dinç E, Bayraktar B. Prevalence of femoroacetabular impingement and effect of training frequency on aetiology in paediatric football players. Hip Int. 2019;29:204-208.
34. Reichenbach S, Jüni P, Nüesch E, Frey F, Ganz R, Leunig M. An examination chair to measure internal rotation of the hip in routine settings: a validation study. Osteoarthritis Cartilage. 2010;18:365-371.
35. Reiman MP, Goode AP, Cook CE, Hölmich P, Thorborg K. Diagnostic accuracy of clinical tests for the diagnosis of hip femoroacetabular impingement/labral tear: a systematic review with meta-analysis. Br J Sports Med. 2015;49:811.
36. Reiman MP, Mather RC, Cook CE. Physical examination tests for hip dysfunction and injury. Br J Sports Med. 2015;49:357-361.
37. Saisu T, Kamegaya M, Segawa Y, Kakizaki J, Takahashi K. Postoperative improvement of femoroacetabular impingement after intertrochanteric flexion osteotomy for SCFE. Clin Orthop Relat Res. 2013;471:2183-2191.
38. Sasaki T, Ishibashi Y, Okamura Y, Toh S, Sasaki T. MRI evaluation of growth plate closure rate and pattern in the normal knee joint. J Knee Surg. 2002;15:72-76.
39. Schmaranzer F, Cerezal L, Llopis E. Conventional and arthrographic magnetic resonance techniques for hip evaluation: what the radiologist should know. Semin Musculoskelet Radiol. 2019;23:227-251.
40. Schmaranzer F, Todorski IAS, Lerch TD, Schwab J, Cullmann-Bastian J, Tannast M. Intra-articular lesions: imaging and surgical correlation. Semin Musculoskelet Radiol. 2017;21:487-506.
41. Siebenrock KA, Behning A, Mamisch TC, Schwab JM. Growth plate alteration precedes cam-type deformity in elite basketball players. Clin Orthop Relat Res. 2013;471:1084-1091.
42. Siebenrock KA, Ferner F, Noble PC, Santore RF, Werlen S, Mamisch TC. The cam-type deformity of the proximal femur arises in childhood in response to vigorous sporting activity. Clin Orthop Relat Res. 2011;469:3229-3240.
43. Siebenrock KA, Kaschka I, Frauchiger L, Werlen S, Schwab JM. Prevalence of cam-type deformity and hip pain in elite ice hockey players before and after the end of growth. Am J Sports Med. 2013;41:2308-2313.
44. Siebenrock KA, Wahab KHA, Werlen S, Kalhor M, Leunig M, Ganz R. Abnormal extension of the femoral head epiphysis as a cause of cam impingement. Clin Orthop Relat Res. 2004;(418):54-60.
45. Smith TO, Hilton G, Toms AP, Donell ST, Hing CB. The diagnostic accuracy of acetabular labral tears using magnetic resonance imaging and magnetic resonance arthrography: a meta-analysis. Eur Radiol. 2011;21:863-874.
46. Steppacher SD, Tannast M, Werlen S, Siebenrock KA. Femoral morphology differs between deficient and excessive acetabular coverage. Clin Orthop Relat Res. 2008;466:782-790.
47. Sutter R, Dietrich TJ, Zingg PO, Pfirrmann CWA. How useful is the alpha angle for discriminating between symptomatic patients with cam-type femoroacetabular impingement and asymptomatic volunteers? Radiology. 2012;264:514-521.
48. Sutter R, Zubler V, Hoffmann A, et al. Hip MRI: how useful is intraarticular contrast material for evaluating surgically proven lesions of the labrum and articular cartilage? AJR Am J Roentgenol. 2014;202:160-169.
49. Tak I, Weir A, Langhout R, et al. The relationship between the frequency of football practice during skeletal growth and the presence of a cam deformity in adult elite football players. Br J Sports Med. 2015;49:630-634.
50. Tannast M, Hanke M, Ecker TM, Murphy SB, Albers CE, Puls M. LCPD: reduced range of motion resulting from extra- and intraarticular impingement. Clin Orthop Relat Res. 2012;470:2431-2440.
51. Tannast M, Siebenrock KA, Anderson SE. Femoroacetabular impingement: radiographic diagnosis - what the radiologist should know. AJR Am J Roentgenol. 2007;188:1540-1552.
52. Van Klij P, Heijboer MP, Ginai AZ, Verhaar JAN, Waarsing JH, Agricola R. Cam morphology in young male football players mostly develops before proximal femoral growth plate closure: a prospective study with 5-yearfollow-up. Br J Sports Med. 2019;53:532-538.
53. Wensaas A, Gunderson RB, Svenningsen S, Terjesen T. Femoroacetabular impingement after slipped upper femoral epiphysis: the radiological diagnosis and clinical outcome at long-term follow-up. J Bone Joint Surg Br. 2012;94:1487-1493.
54. Yanke AB, Khair MM, Stanley R, et al. Sex differences in patients with cam deformities with femoroacetabular impingement: 3-dimensional computed tomographic quantification. Arthroscopy. 2015;31:2301-2306.
© 2021 by the Association of Bone and Joint Surgeons