Secondary Logo

Journal Logo

2018 BERNESE HIP SYMPOSIUM

Does Cartilage Degenerate in Asymptomatic Hips With Cam Morphology?

Grammatopoulos, George BSc, MBBS, DPhil, FRCSC (Tr&Orth); Melkus, Gerd PhD; Rakhra, Kawan MD, FRCPC; Beaulé, Paul E. MD, FRCSC

Author Information
Clinical Orthopaedics and Related Research: May 2019 - Volume 477 - Issue 5 - p 962-971
doi: 10.1097/CORR.0000000000000629

Abstract

Introduction

Femoroacetabular impingement (FAI) is a dynamic process, which leads to abutment of the femoral head-neck junction against the acetabulum [33]. Variant morphologic features of the proximal femur (such as cam morphology [17, 26]) and/or acetabulum (pincer morphology) [16] are considered the principal factors contributing to FAI. Other factors such as spinal morphology [24] and pelvic motion [35] patterns also are believed to contribute. FAI can predispose people to osteoarthritis (OA) development; however, not all hips with radiographic features consistent with FAI are symptomatic or go on to develop degenerative changes [1, 22].

The therapeutic goal in symptomatic FAI is to relieve pain, improve pain-free ROM, and halt the progression of cartilage degeneration [12]. Identifying hips in the early phases of chondrolabral damage aids timely surgical management before irreversible chondral degeneration and improves outcome (pain reduction and joint preservation) after treatment [14, 15]. Conversely, the management of asymptomatic individuals with abnormal bony features suggestive of FAI has received less attention. In recent studies [37], it has been shown that these asymptomatic patients may have compromised cartilage in a pattern similar to patients with symptomatic FAI despite the lack of symptoms [5]. Whether the cartilage damage will progress is unknown but is important because this knowledge could help determine the natural history of cam morphology and guide the management of such individuals.

Traditional imaging modalities have limited value in detecting early degenerative changes [18]. Advanced MRI techniques such as delayed gadolinium-enhanced MRI of cartilage (dGEMRIC ) [39, 45], T1ρ [40, 41], T2, and T2* [25] mapping allow probing of the biochemical content of cartilage tissue in vivo and have been shown to be sensitive to molecular changes seen in early OA. An inverse relation has been found between T1ρ relaxation time and proteoglycan content (an early marker of OA) [2, 47] in bovine and human cartilage samples of the knee [20, 38] and hip [40, 41].

The aims of this longitudinal, T1ρ MRI study were to determine whether (1) asymptomatic hips with cam morphology are at risk for further cartilage degeneration; (2) T1ρ changes are predictive of symptom onset; and (3) bony (acetabular, femoral, or spinal) morphologic parameters are associated with any of the T1ρ signal changes.

Patients and Methods

This is a prospective, single-center, institutional review board-approved study. Participants were recruited from a previous cross-sectional study of 200 asymptomatic hips [21] and have been described in previous reports [5, 6]. Of these hips, 28 (20 males) had a cam deformity and were asymptomatic. All were invited to participate in a study comparing the T1ρ signal between asymptomatic hips with cam morphology and controls [5]; 20 (71%) accepted the invitation. Inclusion criteria for this study were no previous hip pathology or surgery, no signs of OA based on radiologic (MRI) assessments at the time of the cross-sectional study, WOMAC score (> 90) [10] at initial MRI, and the presence of a cam deformity based on oblique axial imaging. The findings of the initial T1ρ imaging study compared with controls were previously reported [5]. Participants were mailed an Addendum to the Research Consent Form; those who agreed to further participation presented for a followup T1ρ MRI scan and functional outcome assessment at a minimum 2-year interval. Eighteen of the 20 hips, who volunteered for the initial study [5], presented for the second assessment at a mean interval of 4 years (range, 2–6 years). Motion artifacts were present in one hip, which could not be processed; the remaining 17 formed the study’s cohort. A minimum scan interval of 2 years was deemed necessary. Most participants were men (16 of the 17) and the mean age was 33 years old (range, 27–45 years) at the time of the initial T1ρ (Table 1). The patients’ mean body mass index was 25 kg/m2 (range, 19–29 kg/m2).

Table 1.
Table 1.:
Cohort demographics, interval between MRI scans, and WOMAC scores

Bony Morphology

The alpha angle was measured on CT images of the radial series at the 1:30 and 3:00 positions. An alpha angle > 60° at 1:30 and/or > 50.5° at 3:00 was defined as having a cam morphology [36]. The average alpha angle anterosuperiorly was 66° (range, 49°–77°) and the average alpha angle anteriorly was 56° (range, 37°–65°) [7, 36]. There were two hips with anterior cam lesions (3:00 location only), six hips with cam lesions located anterosuperiorly (1:30 location only), whereas nine hips had cam morphology at both the 1:30 and 3:00 locations.

Other parameters measured from CT, using validated software and methods [19], included the femoral neck-shaft angle [35], acetabular version and inclination, acetabular depth, acetabular subtended angles (measure of how much femoral head coverage the acetabulum provides along different points of its “clockface”) [13, 29], pelvic incidence, sacral slope, and pelvic tilt [30-32, 42] (Table 2). Subtended angles were measured around the weightbearing acetabular clockface starting anteriorly, at right angles to the anterior pelvic plane, equating to the 0° orientation. Thereafter, the superior acetabular aspect is at the 90° orientation and posterior acetabular rim is at 180° [19]. Subtended measurements were made at 30° increments around the acetabulum. Femoral version was measured according to Murphy et al. [34] using transverse slices at three different femoral locations: the center of the femoral head, the base of the femoral neck, and the condylar axis. Two observers (GG, GN) blinded to patient identity performed all measurements. Excellent interobserver coefficients (ICCs) were identified (ICC, 0.9-0.95; p < 0.001). Furthermore, one observer repeated the measurements for 10 participants and excellent ICCs (0.93-0.98) were identified.

Table 2.
Table 2.:
Bony parameters for the whole cohort

Functional Outcome

The WOMAC osteoarthritis score [11] was obtained for all patients at the time of the first and second scans. There was no difference with the numbers available in the WOMAC score between initial (100; range, 95–100) and followup assessments (98; 87–100; p = 0.534). The difference between the two WOMAC scores was established (ΔWOMAC):

MRI Protocol

Each participant underwent a hip MRI that was performed on a 1.5-T MRI scanner (Magnetom Symphone; Siemens Medical Solutions, Erlangen, Germany) using a body coil for signal transmission and a flexible four-channel surface coil for signal reception. Participants were positioned in a similar fashion for both scans: supine with the leg fixed in neutral rotation. T1ρ-weighted data sets were obtained in the sagittal oblique plane, parallel to the acetabular fossa (see Appendix, Supplemental Digital Content, http://links.lww.com/CORR/A134).

Image Postprocessing and Data Analysis

The MR images were segmented and analyzed using an in-house, custom-written software program developed in MATLAB® (MathWorks Inc, Natick, MA, USA). A musculoskeletal imaging scientist (GM) performed the segmentation analysis of the MRI scans. The T1ρ mapping and analysis protocol used in this study were evaluated in a recent publication, which showed strong interobserver, intraobserver, and inter-MR scan reliability [6]. The ICC and root mean square coefficient of variation were 0.965 and 4% (intraobserver), 0.953 and 4% (interobserver), and 0.988 (all p < 0.001) and 9% (inter-MR scan), respectively [6].

We used an oblique coronal localizer sequence to establish the transverse coverage of the hip that included the superior weightbearing acetabular surface. Seven or eight (depending on joint size) sagittal T1ρ image slices were analyzed, starting from the lateral sourcil margin and extending medially. The hyaline cartilage was segmented as one layer (acetabulum and femoral head together) using the first T1ρ-weighted data set (spin lock time = 12 ms). The matched, anatomic intermediate-weight image was used to facilitate delineation of the hyaline cartilage margins for segmentation, ensuring that the labrum and subchondral compact bone were excluded from the region of interest.

After segmentation, the joint was divided and subdivided into two 90° regions defined using a line drawn through the center and superior apex of the femoral head, creating an anterior and posterior zone. In each hip, the T1ρ relaxation zones were calculated for the whole surface analyzed (T1ρcomplete), the anterior (T1ρanterior) and posterior (T1ρposterior) halves, and six principal regions of interest (ROIs) as previously described [6]. To determine T1ρ in the six ROIs, sagittal slices were divided into lateral (slices 1-3), intermediate (slices 4-6), or medial (slices 7-8) zones. Thereafter, the ROI could be subdivided into six areas (anterolateral, anterointermediate, anteromedial, posterolateral, posterointermediate, and posteromedial; Fig. 1).

Fig. 1 A-D
Fig. 1 A-D:
Three-dimensional reconstructed femoral acetabular joint showing the six cartilage regions analyzed in the study as color-coded overlays from different views. (A) AP oblique view. (B) AP oblique view with 75% acetabulum opacity. (C) Posteroanterior oblique view. (D) Posteroanterior oblique view with 75% acetabulum opacity.

When the initial T1ρ signal changes were reported in this cohort [5], higher values were detected anterolaterally in asymptomatic hips with cam FAI (33 ± 6 ms) compared with controls (29 ± 4 ms).

Because two MR scans were available for each patient in this study, we measured interpatient variability by calculating the individual patient’s T1ρ signal differences and relative differences. The absolute differences in T1ρ values (ΔT1ρ) were determined and were calculated as: ΔT1ρ = T1ρInitial – T1ρFollowup.

The relative differences (%ΔT1ρ) = ΔT1ρ/ T1ρInitial were calculated as:

A negative %ΔT1ρ denotes a greater T1ρ value at followup, indicating a smaller proteoglycan content at followup (ie, further degeneration).

Outcome Measures

The T1ρ, ΔT1ρ, and %ΔT1ρ values were determined for all zones. It has been shown that the variability within the different regions in the joint is < 10% [40] and similarly the T1ρ difference from MR scans performed within a period of 2 weeks in the same individual can be up to 9% [6]. Therefore, 17.6% (1.96% x 9%) was considered clinically important.

Onset of symptoms was determined from the WOMAC score and if the score had deteriorated in the followup review. We tested the WOMAC score difference for correlation with the %ΔT1ρ; furthermore, we assessed whether participants with a clinically important reduction or increase in %ΔT1ρ had greater ΔWOMAC compared with the rest of the group at followup.

Lastly, we tested whether the hips with a clinically important alteration in %ΔT1ρ had different morphologic femoral, acetabular, or spinopelvic parameters compared with the rest of the hips. Whether ΔT1ρ and/or %ΔT1ρ were associated with any of the bone morphologic parameters was tested using correlation coefficients.

Sample Size Calculation

A power analysis based on published hip cartilage T1ρ values of cam participants and healthy controls was performed to calculate the minimal number of hips needed for this study. In the anterolateral region, the area where cam impingement occurs, participants with a cam deformity showed significant higher cartilage T1ρ values (33 ± 5 ms) compared with the control group (29 ± 4 ms) (p = 0.039) [6]. Based on these differences, using a power of 0.8 and alpha error (p) of 0.05, we estimated a minimum of 15 participants was needed for this study.

Statistical Analysis

Statistical analysis was performed with SPSS (Version 23; IBM Corp, Armonk, NY, USA). Nonparametric tests were used for analysis. Statistical significance was set at < 0.05. The Mann-Whitney U and Kruskal-Wallis tests were used for scale data, whereas the chi-square and Fisher’s exact tests were used for categorical data. Spearman’s (ρ) correlation was used to determine whether any correlations existed for scale data. The Mann-Whitney U and Kruskal-Wallis tests were used for research question 1; Spearman’s (ρ) correlation and Mann-Whitney U were used for research question 2, whereas Spearman’s (ρ) correlation was used for research question 3.

Results

No difference in T1ρ values was seen in these asymptomatic hips with cam morphology on the baseline MRI in the anterolateral (34 ± 6 ms) and posterolateral (33 ± 4 ms) ROIs (p = 0.734); however, at followup, the T1 value was higher in the posterolateral (36 ± 5 ms) ROI compared with the anterolateral (32 ± 3 ms) ROI (p = 0.031). The global T1ρ remained unchanged between the initial (mean, 35 ± 5 ms) and followup scans (mean, 34 ± 3 ms) (p = 0.518). For the whole cohort, there were no differences in the T1ρ obtained between the initial and followup MRIs for any of the six ROIs (Table 3). The mean global ΔT1ρ was 1 ± 5 ms (95% confidence interval [CI], -1 to +3 ms). Interval time between scans (ρ = 0.24, p = 0.36) and age at initial scan (ρ = 0.13, p = 0.610) did not correlate with global ΔT1ρ. Similarly, body mass index did not correlate (ρ = -0.10, p = 0.721) with global ΔT1ρ. The mean global %ΔT1ρ was 2% ± 13%. The %ΔT1ρ showed an overall reduction in T1ρ value (at followup) over the anterior half of the joint (9%; 95% CI, 2%–17%), which is contrary to an overall increase in the T1ρ over the posterior half (-5%; 95% CI, -14% to 4%) at followup.

Table 3.
Table 3.:
T1ρ measurements for the whole cohort including the global and ROIs measurements

We observed a clinically important change in the anterolateral %ΔT1ρ (≥ 18%) in four hips; in two of these hips, the T1ρ value increased at followup, whereas in the other two hips, the T1ρ value was reduced at followup. The patient with the largest %ΔT1ρ (-26%) was one of the two patients who reported a WOMAC score reduction (from 100 to 92; Fig. 2). We found that %ΔT1ρ in the anterolateral ROI strongly and positively correlated (ρ = 0.73; p < 0.001) with the T1ρ value in the anterolateral ROI of the baseline MR scan (Fig. 3).

Fig. 2
Fig. 2:
Scatter box of %ΔT1ρ seen in the anterolateral ROI (y-axis, plotted against ΔWOMAC). Dashed lines represent boundaries of significance (± 17.6% of change between scans).
Fig. 3
Fig. 3:
Scatterplot of baseline T1p in the anterolateral ROI plotted against the percentage change in T1p in the anterolateral ROI.

The only bony morphologic parameter that correlated with T1ρ value was the acetabular subtended angle. The anterior and superior acetabular subtended angles (ρ = 0.59–0.61; p = 0.002; Table 4) positively and moderately correlated with the %ΔT1ρ seen over the corresponding ROIs (anterolaterally); the smaller the degree of coverage, the more negative the %ΔT1ρ (ie, greater T1ρ signal at followup scan; Fig. 4).

Table 4.
Table 4.:
Correlations tested for the different bony parameters and the %ΔT1ρ in the anterolateral ROI
Fig. 4
Fig. 4:
Scatterplot of %ΔT1ρ seen in the anterolateral ROI (y-axis) plotted against subtended angle of acetabulum anterosuperiorly. Dashed line represented correlation detected.

Discussion

Proximal femoral cam morphology has a prevalence of approximately 15% among all comers [21]. It can be associated with an increased risk of pain [27] and development of OA within 5 years of detection [46] in some volunteers, yet not all hips with a cam deformity will develop OA or symptoms [1, 22]. Recent studies have identified static/bony and dynamic parameters that increase the risk of a hip with a cam deformity being symptomatic [35, 43]. Identifying which hips are at risk of degeneration and intervening in a timely manner are paramount in the quest of joint preservation. Using patient symptomatology (in particular hip pain) certainly would be an obvious choice, but because this can be nonspecific with regard to disease state [8], evaluating biomarkers such as cartilage degenerative markers in the blood or advanced cartilage imaging with MRI might help identify at-risk hips. In this small, longitudinal study, we found little progression of degenerative changes as measured by T1ρ; only two of 17 individuals with previously asymptomatic cam morphology of the proximal femur developed a clinically important degree of articular cartilage degeneration as measured by T1ρ, and of those, only one developed symptoms. In addition, we were able to demonstrate that biomechanical parameters other than the size of the cam morphology may be of importance; decreasing acetabular coverage anteriorly and laterally was associated with a decrease in T1ρ value content change in individuals with asymptomatic cam morphology.

Limitations to this study include the small sample size, which was predetermined by the number of volunteers who had a cam deformity in the prevalence study (n = 28) and the number that presented for the initial scans (n = 20). Such a small cohort raises the possibility of selection biases. Second, we did not obtain activity data for any volunteers; such data would have allowed us to determine whether any activity modification could be responsible for the %ΔT1ρ detected. Third, the majority of volunteers were male (16 of 17) and therefore the findings of this study may not apply to female hips; nevertheless, cam-type FAI is more prevalent among males. Fourth, the bony morphologic assessments were made based on CT-based analysis and not per radiographic analysis, which is most commonly performed in clinical practice. However, this was performed to improve accuracy of the three-dimensional anatomic assessments. Lastly, a mean 4-year interval between MRI scans is not a long interval in the lifetime of the native hip, and therefore, longer surveillance and longitudinal studies are necessary. However, this work establishes key parameters in further determining what represents a pre- versus a clinical disease state in patients with cam morphology. Previous work has shown that the degenerative process in patients with cam morphology is complex with a variety of biomechanical and biologic processes involved [28, 35, 44].

Considering the whole cohort, the mean global %ΔT1ρ was 1%, demonstrating that on average very little change in the overall articular cartilage health took place, although we did detect regional differences (reduction in T1ρ value anteriorly, increase in T1ρ value posteriorly). In two cross-sectional, observational studies of asymptomatic hips, nonuniform T1ρ values have been described with increasing T1ρ values detected from anterior to posterior [40, 45]. In this longitudinal cohort, similar T1ρ values were seen at the baseline scan between the anterolateral (34 ms) and posterolateral (33 ms) ROIs; however, at followup, the T1ρ values were higher for posterolateral (36 ms) compared with anterolateral (32 ms). This positive change (increased T1ρ signal) in the posterolateral zone would suggest arthritis progression within regions other than the anterolateral zone. The cause of these findings calls for further studies; for example, it could represent arthritis progression secondary to (1) impingement in the superoposterior region, which would typically occur in 90° of flexion in a hip with a cam anterosuperiorly; or (2) microinstability--anterior impingement could lead to counter-coup injury posteriorly, a mechanism precipitated by lesser degrees of acetabular cover or lastly secondary to the action of the inflammatory mediators within the hip with cam FAI [23]. It is evident that further (in vitro and in vivo) studies are needed that would address these mechanical and molecular hypotheses. Such studies would study the areas of hip impingement with three-dimensional modeling work and identify potential microinstability of the hip, correlating the findings with cartilaginous mapping. Additionally, an animal model of the disease could help us determine what contributes to the changes and in what topographic order. To study the contribution of inflammation, histologic and immunologic analysis from the synovial fluid and other regions of the joint from patients in the various stages of the pathologic process would be necessary.

With only two patients who developed symptoms over the relatively short followup interval (2-6 years) in this study, we were not able to determine whether T1ρ changes were predictive of symptom onset. Whether asymptomatic individuals with cam morphology should be under surveillance is a matter of debate. However, this group of patients already exhibited signs of degeneration compared with normal individuals [5], and it would appear that for the most part they still remain asymptomatic within 5 years. This is consistent with other reports showing that certain patients with cam morphology can remain free of arthritic symptoms [3]. The findings of this cohort would argue that surveillance with the newest generation MRI modalities is not currently indicated in patients within 5 years of followup. One of the two volunteers with a clinically important reduction in the proteoglycan content (as per %ΔT1ρ) was a patient with a decreased WOMAC score. In this cohort, there were two volunteers with a reduction in WOMAC score by followup, and only one showed a clinically important increase in T1ρ (%ΔT1ρ of -26% in anterolateral ROI). What factors might cause the onset of hip pain is unclear, and certainly one could argue that patient symptomatology probably is the most effective way to monitor those patients. For the asymptomatic individual with cam morphology, our current understanding of the clinical relevance of the observed T1ρ signal changes and their relationship with patient-reported outcome measures necessitates further investigation. Furthermore, such studies should include and compare the various advanced MR techniques (dGEMRIC, T2, T1ρ) as part of crossvalidation because they probe different biologic changes that occur in cartilage degeneration.

The only morphologic parameter that showed a positive correlation with T1ρ was the degree of acetabular coverage when there was greater coverage anteriorly; we detected a smaller increase in %ΔT1ρ. Two cohort studies [4, 9] reported a protective role of acetabular coverage reflected through the center-edge angle (a radiographic measure of the degree of femoral head coverage the acetabulum provides) on the degree of cartilage damage in cam-type FAI.

In conclusion, in this small longitudinal study, we found that only two of 17 individuals with asymptomatic cam morphologies developed clinically important progression of cartilage degeneration as measured by T1ρ, and of those, only one developed symptoms. By studying several bony parameters, we found that decreasing acetabular coverage, particularly anterosuperiorly, was associated with increased articular cartilage degeneration as measured by T1ρ. Reduced acetabular coverage may increase the likelihood that preclinical cartilage degeneration will arise within 2 to 6 years. Future longitudinal studies should include larger cohorts and the study of subclinical degeneration should perhaps include histologic and immunologic assessments of the hip’s structures.

Acknowledgments

We thank Andrew Speirs and Geoff Ng for their contributions to the study methodology. We also acknowledge The Hans K. Uhthoff Scholarship Program for providing financial support to graduate students involved in this work.

References

1. Agricola R, Reijman M, Bierma-Zeinstra SM, Verhaar JA, Weinans H, Waarsing JH. Total hip replacement but not clinical osteoarthritis can be predicted by the shape of the hip: a prospective cohort study (CHECK). Osteoarthritis Cartilage. 2013;21:559-564.
2. Akella SV, Regatte RR, Gougoutas AJ, Borthakur A, Shapiro EM, Kneeland JB, Leigh JS, Reddy R. Proteoglycan-induced changes in T1rho-relaxation of articular cartilage at 4T. Magn Reson Med. 2001;46:419-423.
3. Anderson LA, Anderson MB, Kapron A, Aoki SK, Erickson JA, Chrastil J, Grijalva R, Peters C. The 2015 Frank Stinchfield Award: Radiographic abnormalities common in senior athletes with well-functioning hips but not associated with osteoarthritis. Clin Orthop Relat Res. 2016;474:342-352.
4. Anderson LA, Peters CL, Park BB, Stoddard GJ, Erickson JA, Crim JR. Acetabular cartilage delamination in femoroacetabular impingement. Risk factors and magnetic resonance imaging diagnosis. J Bone Joint Surg Am. 2009;91:305-313.
5. Anwander H, Melkus G, Rakhra KS, Beaule PE. T1rho MRI detects cartilage damage in asymptomatic individuals with a cam deformity. J Orthop Res. 2016;34:1004-1009.
6. Anwander H, Rakhra KS, Melkus G, Beaulé PE. T1ρ hip cartilage mapping in assessing patients with cam morphology: how can we optimize the regions of interest? Clin Orthop Relat Res. 2017;475:1066-1075.
7. Barton C, Salineros MJ, Rakhra KS, Beaule PE. Validity of the alpha angle measurement on plain radiographs in the evaluation of cam-type femoroacetabular impingement. Clin Orthop Relat Res. 2011;469:464-469.
8. Beaule P, Belzile E, Clohisy J, Ryu J-J. Outcomes of joint preservation surgery: comparison of patients with developmental dysplasia of the hip and femoroacetabular impingement. J Hip Preserv Surg. 2016;3:270-277.
9. Beaule 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.
10. Bellamy N, Buchanan WW, Goldsmith CH. Validation study of WOMAC: a health status instrument for measuring clinically important patient relevant outcomes following total or knee arthroplasty in osteoarthritis. J Orthop Rheumatol. 1988;1:95-108.
11. Bellamy N, Buchanan WW, Goldsmith CH, Campbell J, Stitt LW. Validation study of WOMAC: a health status instrument for measuring clinically important patient relevant outcomes to antirheumatic drug therapy in patients with osteoarthritis of the hip or knee. J Rheumatol. 1988;15:1833-1840.
12. Clohisy JC, St John LC, Schutz AL. Surgical treatment of femoroacetabular impingement: a systematic review of the literature. Clin Orthop Relat Res. 2010;468:555-564.
13. Cobb J, Logishetty K, Davda K, Iranpour F. Cams and pincer impingement are distinct, not mixed: the acetabular pathomorphology of femoroacetabular impingement. Clin Orthop Relat Res. 2010;468:2143-2151.
14. Domb BG, Gui C, Lodhia P. How much arthritis is too much for hip arthroscopy: a systematic review. Arthroscopy. 2015;31:520-529.
15. Egerton T, Hinman RS, Takla A, Bennell KL, O'Donnell J. Intraoperative cartilage degeneration predicts outcome 12 months after hip arthroscopy. Clin Orthop Relat Res. 2013;471:593-599.
16. Ganz R, Leunig M, Leunig-Ganz K, Harris WH. The etiology of osteoarthritis of the hip: an integrated mechanical concept. Clin Orthop Relat Res. 2008;466:264-272.
17. Ganz R, Parvizi J, Leunig M, Siebenrock KA. Femoroacetabular impingement: a cause for osteoarthritis of the hip. Clin Orthop Relat Res. 2003;417:112-120.
18. Gold SL, Burge AJ, Potter HG. MRI of hip cartilage: joint morphology, structure, and composition. Clin Orthop Relat Res. 2012;470:3321-3331.
19. Grammatopoulos G, Speirs AD, Ng KCG, Riviere C, Rakhra KS, Lamontagne M, Beaule PE. Acetabular and spino-pelvic morphologies are different in subjects with symptomatic cam femoro-acetabular impingement. J Orthop Res. 2018;36:1840-1848.
20. Gupta R, Virayavanich W, Kuo D, Su F, Link T, Ma B, Li X. MR T(1)ρ quantification of cartilage focal lesions in acutely injured knees: correlation with arthroscopic evaluation. Magn Reson Imaging. 2014;32:1290-1296.
21. Hack K, Di Primio G, Rakhra K, Beaule PE. Prevalence of cam-type femoroacetabular impingement morphology in asymptomatic volunteers. J Bone Joint Surg Am. 2010;92:2436-2444.
22. Hartofilakidis G, Bardakos NV, Babis GC, Georgiades G. An examination of the association between different morphotypes of femoroacetabular impingement in asymptomatic subjects and the development of osteoarthritis of the hip. J Bone Joint Surg Br. 2011 2011;93:580-586.
23. Hashimoto S, Rai MF, Gill CS, Zhang Z, Sandell LJ, Clohisy JC. Molecular characterization of articular cartilage from young adults with femoroacetabular impingement. J Bone Joint Surg Am. 2013;95:1457-1464.
24. Hellman MD, Haughom BD, Brown NM, Fillingham YA, Philippon MJ, Nho SJ. Femoroacetabular impingement and pelvic incidence: radiographic comparison to an asymptomatic control. Arthroscopy. 2017;33:545-550.
25. Hesper T, Bulat E, Bixby S, Akhondi-Asl A, Afacan O, Miller P, Bowen G, Warfield S, Kim YJ. Both 3-T dGEMRIC and acetabular-femoral T2 difference may detect cartilage damage at the chondrolabral junction. Clin Orthop Relat Res. 2017;475:1058-1065.
26. Ito K, Minka MA, Leunig M, Werlen S, Ganz R. Femoroacetabular impingement and the cam-effect. A MRI-based quantitative anatomical study of the femoral head-neck offset. J Bone Joint Surg Br. 2001;83:171-176.
27. Khanna V, Caragianis A, Diprimio G, Rakhra K, Beaule PE. Incidence of hip pain in a prospective cohort of asymptomatic volunteers: is the cam deformity a risk factor for hip pain? Am J Sports Med. 2014;42:793-797.
28. Lamontagne M, Kennedy MJ, Beaulé PE. The effect of cam FAI on hip and pelvic motion during maximum squat. Clin Orthop Relat Res. 2009;467:645-650.
29. Larson CM, Moreau-Gaudry A, Kelly BT, Byrd JW, Tonetti J, Lavallee S, Chabanas L, Barrier G, Bedi A. Are normal hips being labeled as pathologic? A CT-based method for defining normal acetabular coverage. Clin Orthop Relat Res. 2015;473:1247.
30. Lazennec JY, Brusson A, Rousseau MA. Hip-spine relations and sagittal balance clinical consequences. Eur Spine J. 2011;20(Suppl 5):686-698.
31. Le Huec J, Saddiki R, Franke J, Rigal J, Aunoble S. Equilibrium of the human body and the gravity line: the basics. Eur Spine J. 2011;20:558-563.
32. Legaye J, Duval-Beaupere G, Hecquet J, Marty C. Pelvic incidence: a fundamental pelvic parameter for three-dimensional regulation of spinal sagittal curves. Eur Spine J. 1998;7:99-103.
33. Leunig M, Beaule PE, Ganz R. The concept of femoroacetabular impingement: current status and future perspectives. Clin Orthop Relat Res. 2009;467:616-622.
34. Murphy SB, Simon SR, Kijewski PK, Wilkinson RH, Griscom NT. Femoral anteversion. J Bone Joint Surg Am. 1987;69:1169-1176.
35. Ng KC, Lamontagne M, Adamczyk AP, Rakhra KS, Beaule PE. Patient-specific anatomical and functional parameters provide new insights into the pathomechanism of cam FAI. Clin Orthop Relat Res. 2015;473:1289-1296.
36. Notzli 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.
37. Palmer A, Fernquest S, Rombach I, Park D, Pollard T, Broomfield J, Bangerter N, Carr A, Glyn-Jones S. Diagnostic and prognostic value of delayed gadolinium enhanced magnetic resonance imaging of cartilage (dGEMRIC) in early osteoarthritis of the hip. Osteoarthritis Cartilage. 2017;25:1468-1477.
38. Peers SC, Maerz T, Baker EA, Shetty A, Xia Y, Puwal S, Marcantonio D, Keyes D, Guettler J. T1ρ magnetic resonance imaging for detection of early cartilage changes in knees of asymptomatic collegiate female impact and nonimpact athletes. Clin J Sports Med. 2014;24:218-225.
39. Pollard T, Gwilym S, Carr A. The assessment of early osteoarthritis. Bone Joint J. 2008;90:411-421.
40. Rakhra KS, Cardenas-Blanco A, Melkus G, Schweitzer ME, Cameron IG, Beaule PE. Is the T1rho MRI profile of hyaline cartilage in the normal hip uniform? Clin Orthop Relat Res. 2015;473:1325-1332.
41. Rakhra KS, Lattanzio PJ, Cardenas-Blanco A, Cameron IG, Beaule PE. Can T1-rho MRI detect acetabular cartilage degeneration in femoroacetabular impingement? A pilot study. J Bone Joint Surg Br. 2012;94:1187-1192.
42. Ross JR, Nepple JJ, Philippon MJ, Kelly BT, Larson CM, Bedi A. Effect of changes in pelvic tilt on range of motion to impingement and radiographic parameters of acetabular morphologic characteristics. Am J Sports Med. 2014;42:2402-2409.
43. Rylander J, Shu B, Favre J, Safran M, Andriacchi T. Functional testing provides unique insights into the pathomechanics of femoroacetabular impingement and an objective basis for evaluating treatment outcome. J Orthop Res. 2013;31:1461-1468.
44. Speirs A, Beaule PE, Rakhra KS, Schweitzer ME, Frei H. Bone density is higher in cam-type femoroacetabular impingement deformities compared to normal subchondral bone. Osteoarthritis Cartilage. 2013;21:1068-1073.
45. Subburaj K, Valentinitsch A, Dillon AB, Joseph GB, Li X, Link TM, Vail TP, Majumdar S. Regional variations in MR relaxation of hip joint cartilage in subjects with and without femoralacetabular impingement. Magn Reson Imaging. 2013;31:1129-1136.
46. Waarsing JH, Arden NK, Carr AJ, Bierma-Zeinstra SM, Thomas GE, Weinans H, Glyn-Jones S. Cam impingement of the hip—a risk factor for hip osteoarthritis. Nat Rev Rheumatol. 2013;9:630-634.
47. Wheaton AJ, Casey FL, Gougoutas AJ, Dodge GR, Borthakur A, Lonner JH, Schumacher HR, Reddy R. Correlation of T1ρ with fixed charge density in cartilage. J Magn Reson Imaging. 2004;20:519-525.

Supplemental Digital Content

© 2019 by the Association of Bone and Joint Surgeons