HIP
Three-dimensional morphology and bony range of movement in hip joints in patients with hip dysplasia I. Nakahara, M. Takao, T. Sakai, H. Miki, T. Nishii, N. Sugano From Department of Orthopaedic Medical Engineering, Osaka University Graduate School of Medicine, 2-2, Yamadaoka, Suita, 565-0871, Japan
To confirm whether developmental dysplasia of the hip has a risk of hip impingement, we analysed maximum ranges of movement to the point of bony impingement, and impingement location using three-dimensional (3D) surface models of the pelvis and femur in combination with 3D morphology of the hip joint using computer-assisted methods. Results of computed tomography were examined for 52 hip joints with DDH and 73 normal healthy hip joints. DDH shows larger maximum extension (p = 0.001) and internal rotation at 90° flexion (p < 0.001). Similar maximum flexion (p = 0.835) and external rotation (p = 0.713) were observed between groups, while high rates of extra-articular impingement were noticed in these directions in DDH (p < 0.001). Smaller cranial acetabular anteversion (p = 0.048), centre-edge angles (p < 0.001), a circumferentially shallower acetabulum, larger femoral neck anteversion (p < 0.001), and larger alpha angle were identified in DDH. Risk of anterior impingement in retroverted DDH hips is similar to that in retroverted normal hips in excessive adduction but minimal in less adduction. These findings might be borne in mind when considering the possibility of extra-articular posterior impingement in DDH being a source of pain, particularly for patients with a highly anteverted femoral neck. Cite this article: Bone Joint J 2014;96-B:580–9.
I. Nakahara, MD, PhD, Orthopaedic Surgeon H. Miki, MD, PhD, Orthopaedic Surgeon Osaka National Hospital, Department of Orthopaedic Surgery, 2-1-14 Hoenzaka Chuoku, Osaka, 540-0006, Japan. M. Takao, MD, PhD, Orthopaedic Surgeon, Assistant Professor T. Sakai, MD, PhD, Orthopaedic Surgeon, Lecturer Osaka University Graduate School of Medicine, Department of Orthopaedic Surgery, 2-2, Yamadaoka, Suita, 565-0871, Japan. T. Nishii, MD, PhD, Orthopaedic Surgeon, Assistant Professor Osaka University Graduate School of Medicine, Department of Orthopaedic Medical Engineering, 2-2, Yamadaoka, Suita, 565-0871, Japan. N. Sugano, MD, PhD, Orthopaedic Surgeon, Professor Osaka University Graduate School of Medicine, Department of Orthopaedic Medical Engineering, 2-2, Yamadaoka, Suita, 565-0871, Japan. Correspondence should be sent to Dr N. Sugano; e-mail: [email protected] ©2014 The British Editorial Society of Bone & Joint Surgery doi:10.1302/0301-620X.96B5. 32503 $2.00 Bone Joint J 2014;96-B:580–9. Received 27 May 2013; Accepted after revision 31 January 2014
580
Developmental dysplasia of the hip (DDH) is a major cause of secondary osteoarthritis (OA).1,2 DDH shows characteristic anatomical abnormalities, including a shallow acetabulum, acetabular mal-orientation, and a highly anteverted femoral neck.3-5 These abnormalities cause hip instability and increased joint contact pressure,6 leading to cartilage damage and subsequent OA.7 In the contemporary literature, hip pain induced by femoro-acetabular impingement (FAI)8,9 and ischiofemoral impingement10,11 has been attracting attention. Symptomatic hips with FAI display characteristic morphological features such as over-coverage of the anterior acetabulum, a deep acetabular socket, a non-spherical femoral head, or reduced head–neck offset.8,12-15 Among patients with DDH, the cross-over sign on plain radiographs is considered suggestive of anterior impingement and is reportedly present in 18% of cases.16 Patients with DDH show the morphological features of a highly anteverted femoral neck, which has been reported as a risk factor for posterior impingement.11,17 These findings have led us to question whether some patients with DDH have symptoms due to anterior or posterior impingement.
Although proper diagnosis and early intervention may relieve hip pain and possibly prevent development of hip OA in impingement-related disorders,18 the range of movement (ROM) to the point of bony impingement could be better understood in order to clarify the rationale of such interventions. Computer-assisted measurement of the ROM using three-dimensional (3D) models of the pelvis and femur provides an assessment of relative movement between the pelvis and femur to the point of impingement, and allows identification of the site of impingement. Applying this methodology, the maximum range of hip movement in symptomatic hip joints due to FAI,19,20 with Legg–Calvé–Perthes disease,21 coxa valga and highly anteverted femoral necks,20 and normal healthy hip joints,22 have been reported; however, the maximum ROM in DDH patients has not. The primary purpose of this study was to investigate the ROM to the point of bony impingement and its location in DDH. The secondary purpose was to measure the 3D morphology of the acetabulum and proximal femur in order to clarify which morphological parameters influence the ROM. Finally the effects of acetabular retroversion and a highly anteverted femoral neck on anterior and posterior impingement, respectively, were studied. THE BONE & JOINT JOURNAL
THREE-DIMENSIONAL MORPHOLOGY AND BONY RANGE OF MOVEMENT IN HIP JOINTS IN PATIENTS WITH HIP DYSPLASIA
581
Table I. Demographic data of subjects. Data are shown as mean (range) (DDH, developmental dysplasia of the hip) Subjects
DDH n = 29 (52 joints)
Normal n = 49 (73 joints)
p-value*
Age (years) (range) Height (cm) (range) Weight (kg) (range) BMI (kg/m2) (range)
33.0 (16 to 48) 158.1 (147 to 171) 54.0 (46 to 77) 21.6 (18.6 to 31.6)
71.7 (63 to 80) 151.7 (140 to 165) 49.9 (35 to 69) 21.7 (13.7 to 28.4)
< 0.001 < 0.001 0.019 0.930
* Mixed-model ANOVA
Materials and Methods The present investigation used a database of CT images which had been obtained for pre-operative surgical planning for pelvic osteotomies due to DDH from 2006 to 2012. Inclusion criteria were Crowe Group-I DDH23 with a centre-edge (CE) angle ≤ 20°2 on plain anteroposterior (AP) radiography, that had neither signs of advanced or terminal OA (Tönnis classification ≥ grade 2)24 nor Perthes-like femoral head deformity. The DDH group comprised 52 hip joints in 29 women with a mean age of 33.0 years (16 to 48). As controls, CT images of 73 normal hip joints from 49 healthy female volunteers with a mean age of 71.7 years (63 to 80) were obtained from the normal CT image database which was developed for research according to the following criteria: no hip symptoms, no signs of OA (Tönnis classification ≥ grade 1) nor acetabular dysplasia (CE angle ≤ 20°) and no previous hip surgery (Table I). The entire pelvis and bilateral femora were scanned using a helical CT scanner (HiSpeed Advantage, GE Medical Systems, Milwaukee, Wisconsin) with a slice pitch of 1 mm and 1.25 mm thickness. All study protocols were approved by the institutional review board. Both ROM and morphological measurements were performed on standard pelvic and femoral co-ordinate systems. The pelvic reference co-ordinates were defined by sagittal pelvic tilt in the supine position and bilateral anterior superior iliac spines. The femoral reference co-ordinates were defined by the posterior femoral plane, including the most posterior point of the greater trochanter and the posterior femoral condyles, the centre of the femoral head, and the knee centre.22 3D surface models of the pelvis and femur were reconstructed from CT data using an algorithm of marching cubes25 published in the Visualization Toolkit.26 The centre of the femoral head as determined by a best-fit sphere technique was set to be the centre of rotation of the femur, and neutral position of the hip joint was determined when both pelvic and femoral co-ordinates were parallel. Collision of the pelvic and femoral models was automatically checked by rotating the femoral models 0.5° at a time until overlapping of the polygons occurred. The V-Collide library developed at the University of North Carolina, Chapel Hill was used for collision detection.27 Maximum flexion, extension, external rotation, and internal rotation at VOL. 96-B, No. 5, MAY 2014
90° flexion were calculated in each patient model. Additionally, two movement patterns corresponding to the anterior and posterior impingement test9,10 were evaluated. For the anterior impingement test, maximum internal rotation was measured in 10° increments between 80° and 110° of flexion and 0° and 20° of adduction. For the posterior impingement test, maximum external rotation was measured in 10° increments between 0° and 30° of extension and 0° and 20° of adduction. The locations of impingement on both the pelvic and femoral sides were determined for every movement in each patient model. Possible pelvic impingement areas were defined as the acetabular rim, ischium, posterior acetabular wall surface, around the anterior inferior iliac spine, and around the anterior superior iliac spine. The areas of possible femoral impingement were divided into the femoral neck, greater and lesser trochanters, intertrochanteric crest, distal side of the femoral neck, and the femoral shaft. Locations of the rim were further divided in a clock system by defining the locations of the anterior rim, deepest acetabular notch, and posterior rim as three, six, and nine o’clock, respectively. Locations of the femoral neck were also further divided in a clock system by defining the anterior location, the most prominent point of Adam’s arch,28 which shows the thickened medial cortex at the femoral neck, and the posterior location as three, six, and nine o’clock, respectively. Impingement type was specified as intra- or extraarticular impingement according to the location of the impingement zone. Impingement between the rim and neck was defined as intra-articular impingement, and that between all other anatomical areas was defined as extraarticular impingement. Using 3D-viewer software (3D Template; Japan Medical Materials, Osaka, Japan), three orthogonal planes (coronal, sagittal, and axial) were reconstructed. On the axial views, at the femoral head centre level (level 0), and onethird (level 1) and two-thirds (level 2) of femoral head radius from the femoral head centre, the acetabular anteversion was measured. When the anteversion angle was negative at any level, the acetabulum was defined as retroverted. Lateral and anterior CE angles were measured on coronal and sagittal views through the femoral head centre, respectively. When the lateral CE angle was less than 0°, the
582
I. NAKAHARA, M. TAKAO, T. SAKAI, H. MIKI, T. NISHII, N. SUGANO
Fig. 1 3D image showing multiple radial planes through the acetabular axis reconstructed at increments of 15° from the deepest part of the acetabular notch. Acetabular edge angle was defined as the angle between the acetabular axis and a line between the centre of the femoral head and the acetabular edge point in each radial plane.
Fig. 2 3D image showing multiple planes including the femoral neck axis reconstructed at increments of 15° from the most prominent part of Adam’s arch. On each plane, the alpha angle was measured.
anterior CE angle was considered to be 0°. To examine acetabular rim coverage three-dimensionally, a plane including the anterior and posterior acetabular edges on the axial plane and the superior acetabular edge on the coronal plane was defined as the acetabular opening plane, while the line perpendicular to this plane and passing through the centre of the femoral head was defined as the acetabular axis. Multiple radial planes through the acetabular axis were reconstructed by rotating planes around the axis in 15° increments from the deepest acetabular notch. On each plane, the angle between the acetabular axis and a line connecting the femoral head centre and acetabular edge was measured (Fig. 1). Locations of the rim were given using the same clock system used for impingement location. On the femoral side, femoral neck anteversion and neck shaft angle were measured according to the previously reported method.29 To investigate the alpha angle15 of the
femoral neck three-dimensionally, multiple radial planes through the femoral neck axis were reconstructed at 15° increments from the most prominent part of Adam’s arch. In each plane, the alpha angle was measured (Fig. 2).15 Locations were again given using the same clock system used for the location of impingement. Statistical analysis. Statistical comparisons of demographic data, ROM, and morphological parameters between the DDH and normal groups were made using a mixed-model analysis of variance (ANOVA) regarding each subject as a random effect and each group as a fixed effect. When each group was further divided into subgroups based on impingement location (extra- or intra-articular impingement), acetabular anteversion (with or without retroversion), and femoral neck anteversion (regularly or highly anteverted), we used a Kruskal–Wallis test to compare subgroups; if significant, we used the Mann–Whitney U test to THE BONE & JOINT JOURNAL
THREE-DIMENSIONAL MORPHOLOGY AND BONY RANGE OF MOVEMENT IN HIP JOINTS IN PATIENTS WITH HIP DYSPLASIA
583
Table II. Range of movement (ROM) and impingement locations in both groups
Mean flexion (°) (range) No. of intra-articular impingements (n, %) No. of extra-articular impingements (n, %) Mean extension in degrees (range) No. of intra-articular impingements (n, %) No. of extra-articular impingements (n, %) Mean external rotation in degrees (range) No. of intra-articular impingements (n, %) No. of extra-articular impingements (n, %) Mean internal rotation at 90° flexion (°) (range) No. of intra-articular impingements (n, %) No. of extra-articular impingements (n, %)
DDH
Normal
p-value
130.3 (105.5 to 153.0) 18 (34.6) 34 (65.4) 66.3 (17.5 to 146.0) 52 (100) 0 (0) 34.5 (7.5 to 68.0) 0 (0) 52 (100) 70.8 (34.5 to 107.5) 49 (94.2) 3 (5.8)
129.2 (113.5 to 146.5) 58 (79.5) 15 (20.5) 50.6 (0.5 to 95.0) 73 (100) 0 (0) 35.3 (0.5 to 67.5) 44 (60.3) 29 (39.7) 49.6 (27.5 to 80.5) 71 (97.3) 2 (2.7)
0.835* < 0.001† 0.001* 0.713* < 0.001‡ < 0.001* 0.648‡
* Mixed-model ANOVA † Chi-squared test ‡ Fisher’s exact test
P < 0.001 0.005
0.032
< 0.001
100
50
< 0.001 0.004
100
60 Degrees
40
50
20
ar ul
ul
ic
ic
rt tr Ex
In
tr
aa
aa
rt
aa
aa tr Ex
tr In
rt
ic
ic
ul
ul
ar
ar External rotation
rt
ul ic rt aa
Ex
In
tr
tr
tr
aa
aa
rt
rt
ic
ic
ul
ar
ar
ar ul
ul ic rt
aa tr
aa tr In Flexion
Ex
aa
rt
rt
ic
ic
ul
ar
ar
ar ul
ar ul ic tr
aa
rt
Ex
tr In
0
ar
0
0
Ex
Degrees
150
P < 0.001
P = 0.026
0.246 < 0.001 0.001 0.182
Degrees
DDH Normal
Internal rotation
Fig. 3 Detailed range of movement (ROM) analysis (mean with range) in directions of flexion, external rotation, and internal rotation at 90° flexion according to impingement locations (Overall p-values (top) measured using the Kruskal–Wallis test; all other p-values used the Mann–Whitney U test).
compare each group. Mann–Whitney U tests were conducted to detect differences in location of impingement zones on the acetabular rim and femoral neck. The chisquared test or Fisher’s exact test were applied to detect differences in the prevalence of intra- and extra-articular impingement. A correlation analysis was performed to examine the relationship between morphological parameters and ROM for both the DDH and normal groups using the Pearson linear correlation coefficient (r). Differences were defined as statistically significant for probability values less than 5%.
Results Maximum extension and internal rotation at 90° flexion was significantly larger in the DDH group than in the normal group. No significant differences were seen in maximum flexion and external rotation. The rate of extraarticular impingement was significantly higher in these directions in the DDH group (Table II). The maximum flexVOL. 96-B, No. 5, MAY 2014
ion until extra-articular impingement was significantly larger than that until intra-articular impingement in both the DDH and normal groups. However, ROM, until either intra- or extra-articular impingement, did not differ significantly between DDH and normal groups. The range of internal rotation at 90° flexion until intra-articular impingement in the normal group was significantly smaller than that in the DDH group, regardless of impingement location. There was no difference in maximum external rotation among the subgroups based on impingement location (Fig. 3). For the anterior impingement simulation, significantly larger maximum internal rotation angles were observed in the DDH group, except for 100° and 110° of flexion with 20° of adduction (Fig. 4). For the posterior impingement simulation, maximum external rotation decreased in the DDH group for the composite movement in 30° of extension with 10° of adduction (Fig. 5). From the analysis of impingement locations, the anterior impingement zones on
I. NAKAHARA, M. TAKAO, T. SAKAI, H. MIKI, T. NISHII, N. SUGANO
40 20 0
80
90
100
20° adduction
10° adduction 80
< 0.001
0.002
60
0.012
40 20 0
110
< 0.001
80
90
Flexion
100
Internal rotation
DDH 0° adduction Normal < 0.001 80 < 0.001 < 0.001 < 0.001 60
Internal rotation
Internal rotation
584
80 0.001 0.008
60
0.053 40 0.124 20 0
110
80
Flexion
90
100
110
Flexion
Fig. 4 Graph showing the results of anterior impingement tests for the developmental dysplasia of the hip (DDH) and normal groups in 0°, 10°, and 20° adduction. The solid line indicates the mean for dysplasia; the dotted line indicates the normal mean with error bars showing the 95% confidence interval (p-values shown above each result used the mixed-model ANOVA).
0.833 0.252
10 0 10
20
Extension
30
30
0.948 0.842
20
0.507 10 0
0.012
External rotation
30
0
40
40
0.870
20
20° adduction
10° adduction
External rotation
External rotation
DDH 0° adduction Normal 0.877 40
30 20
0.720 0.283
10
0.985 0.062 0
0
10
20
Extension
30
0
10
20
30
Extension
Fig. 5 Graph showing results of posterior impingement tests for the developmental dysplasia of the hip (DDH) and normal groups in 0°, 10°, and 20° adduction. The solid line indicates the mean for dysplasia, the dotted line indicates the normal mean with error bars showing the 95% confidence interval (p-values shown above each result use the mixed-model ANOVA).
the femoral neck and posterior impingement zones on the acetabular rim were located more inferiorly in the DDHgroup. A higher prevalence of extra-articular impingement was observed for both anterior and posterior impingement tests in the DDH group (Fig. 6). The DDH group showed significantly smaller cranial acetabular anteversion and CE angles and larger femoral neck anteversion compared with the normal group (Table III). In 3D analysis of acetabular rim coverage, the DDH group also showed lower coverage at all locations compared with the normal group. In both groups, three prominences and three depressions were identified at consistent locations; these prominences were seen generally at clock positions between 1 o’clock and 2 o’clock, between 4 o’clock and 5 o’clock, and between 7 o’clock and 8 o’clock, and the depressions were seen commonly at 11 o’clock, 3 o’clock, and 6 o’clock (Fig. 7). Analysis of the alpha angle, also revealed a significantly larger alpha angle at clock positions from 2 o’clock to 3 o’clock and from 6 to 9 o’clock in the DDH group (Fig. 8).
Correlation analysis identified that the maximum flexion showed a positive correlation with acetabular anteversion, as well as weak negative correlations with anterior CE angle and neck–shaft angle. Acetabular anteversion, CE angles, and mean acetabular rim coverage all correlated negatively with maximum extension. In external rotation, negative correlations were indicated with both acetabular anteversion and femoral neck anteversion. The maximum internal rotation at 90° flexion correlated negatively with CE angles and mean acetabular rim coverage and positively with femoral neck anteversion and neck–shaft angle. The alpha angle did not show correlations with any direction of the ROM (Table IV). The retroverted acetabulum was observed only at the cranial level in eight hips (15.3%) in the DDH group and in five hips (6.8%) in the normal group. No significant difference in prevalence was seen between groups (p = 0.214, chi-squared test). The retroverted DDH hips showed smaller ranges until anterior impingement than the remaining DDH cases in excessive flexion and adduction. THE BONE & JOINT JOURNAL
THREE-DIMENSIONAL MORPHOLOGY AND BONY RANGE OF MOVEMENT IN HIP JOINTS IN PATIENTS WITH HIP DYSPLASIA
585
Table III. Morphological measurements for both groups
Acetabular anteversion (level 0) Acetabular anteversion (level 1) Acetabular anteversion (level 2) Lateral CE angle Anterior CE angle Femoral anteversion Neck–shaft angle
DDH
Normal
p-value*
22.1 (0.2 to 36.4) 18.9 (-3.2 to 37.4) 12.9 (-9.5 to 34.1) 4.6 (-15.5 to 17.9) 23.1 (0 to 53.8) 38.9 (8.3 to 66.0) 126.9 (119.1 to 140.0)
23.3 (12.8 to 37.4) 22.4 (0.2 to 39.3) 16.8 (-3.4 to 38.0) 35.6 (21.4 to 59.2) 58.6 (34.6 to 73.9) 25.1 (1.0 to 47.5) 125.6 (113.1 to 137)
0.251 0.053 0.048 < 0.001 < 0.001 < 0.001 0.230
* Mixed-model ANOVA test
Anterior impingement pelvic side
Anterior impingement femoral side
100
100
80
DDH Normal
DDH Normal
P = 0.054
60
40
P < 0.001
60
Rate (%)
Rate (%)
80
40
P < 0.001 20
20
0
0
P < 0.001
Intraarticular Posterior impingement pelvic side
P < 0.001
100
DDH Normal
80 P < 0.001
60
Rate (%)
Rate (%)
80
100
40
Posterior impingement femoral side P < 0.001
DDH Normal
P = 0.371
60
40
20
20
0
0
Intraarticular
Intraarticular Fig. 6
Histograms showing the impingement zones for anterior impingement tests and posterior impingement tests in developmental dysplasia of the hip (DDH) and normal hips
Compared with the retroverted normal hips, ranges until anterior impingement were significantly larger in less flexion and adduction and were not restricted in any hip positions. The comparison with the non-retroverted normal hips, revealed ranges until anterior impingement that were also significantly larger in less flexion and adduction but in excessive flexion and adduction, they were restricted (Fig. 9). A highly anteverted femoral neck over 50° was observed in only 13 hips of the DDH group (25%) VOL. 96-B, No. 5, MAY 2014
and the prevalence was significantly different (p < 0.001, Fisher’s exact test). Significantly smaller ranges until posterior impingement were frequently observed compared with DDH and normal hips with regular anteversion (Fig. 10).
Discussion We have demonstrated maximum extension and internal rotation at 90° flexion in DDH which were significantly larger when compared to normal hip joints. In flexion and
586
I. NAKAHARA, M. TAKAO, T. SAKAI, H. MIKI, T. NISHII, N. SUGANO
DDH Normal
Angle (º)
100 90 80 70 60 0:00 1:30 3:00 4:30 6:00 7:30 9:00 10:30 Acetabular location Fig. 7 Graph showing the result of circumferential acetabular edge angle. The solid line indicates the mean for developmentally dysplastic hips (DDH); the dotted line indicates the normal mean with error bars showing the 95% confidence interval. Significant differences in acetabular edge angle existed in all locations (p < 0.001; mixed-model ANOVA).
DDH Normal
Angle (º)
50 45 40 35 30 0:00 1:30 3:00 4:30 6:00 7:30 9:00 10:30 Femoral neck location
Location
p-value
0.00 0.30 1.00 1.30 2.00 2.30 3.00 3.30 4.00 4.30 5.00 5.30 6.00 6.30 7.00 7.30 8.00 8.30 9.00 9.30 10.00 10.30 11.00 11.30
0.885 0.153 0.936 0.054 0.034 0.005 0.003 0.531 0.329 0.054 0.458 0.444 0.026 0.005 < 0.001 0.006 0.010 0.039 0.413 0.942 0.453 0.722 0.392 0.566
Fig. 8 Graph showing the result of circumferential alpha angle. The solid line indicates the mean for the developmentally dysplastic hips (DDH) group; the dotted line indicates the mean for the normal group with error bars showing the 95% confidence interval (p-values were assessed using the mixed-model ANOVA).
external rotation, we identified no significant differences in maximum ROM. In the present study, smaller CE angles and a more anteverted femoral neck were confirmed in DDH. These findings mirror previous reports.3-5,30,31 The 3D analysis of the acetabular rim demonstrated that its coverage in DDH was significantly lower in each location but the wave-
shaped pattern of the rim was similar to that of normal hips, although the acetabulum is shallower overall. Circumferential alpha-angle analysis of hips with DDH showed larger alpha angles in the anterosuperior and postero-inferior aspects compared to normal hips. Some of these differences in morphology correlated with the ROM. Maximum extension and internal rotation at THE BONE & JOINT JOURNAL
THREE-DIMENSIONAL MORPHOLOGY AND BONY RANGE OF MOVEMENT IN HIP JOINTS IN PATIENTS WITH HIP DYSPLASIA
587
Table IV. Coefficients of correlation (r) (with p-value) between range of movement (ROM) and morphological parameters
Acetabular anteversion (level 0) Acetabular anteversion (level 1) Acetabular anteversion (level 2) Lateral CE angle Anterior CE angle Mean acetabular rim coverage Femoral neck anteversion Neck–shaft angle Mean alpha angle
Flexion
Extension
External rotation
Internal rotation at 90° flexion
0.491* (< 0.001) 0.461* (< 0.001) 0.507* (< 0.001) -0.171 (0.056) -0.298* (< 0.001) -0.139 (0.121) 0.108 (0.230) -0.241† (0.007) -0.097 (0.280)
-0.516* (< 0.001) -0.504* (< 0.001) -0.464* (< 0.001) -0.457* (< 0.001) -0.384* (< 0.001) -0.459* (< 0.001) -0.145 (0.108) 0.110 (0.221) 0.164 (0.069)
-0.324* (< 0.001) -0.254† (0.004) -0.249† (0.005) -0.012 (0.896) 0.061 (0.498) -0.060 (0.506) -0.619* (< 0.001) 0.037 (0.676) 0.025 (0.781)
0.043 (0.636) -0.096 (0.289) -0.037 (0.679) -0.704* (< 0.001) -0.675* (< 0.001) -0.679* (< 0.001) 0.775* (< 0.001) 0.209‡ (0.019) 0.038 (0.670)
* p < 0.001 † p < 0.01 ‡ p < 0.05
DDH with retroverted DDH with non-retroverted Normal with retroverted Normal with non-retroverted 10º adduction
20º adduction
100
100
80
80
80
60 40 20
Internal rotation
100 Internal rotation
Internal rotation
0º adduction
60 40
0
0 80
90
100
110
40 20
20
0
60
80
90
Flexion
100
80
110
90
100
110
Flexion
Flexion 80° flexion
90° flexion
100° flexion
110° flexion
0° adduction
vs DDH without retroverted vs non-retroverted normal hips vs retroverted normal hips
0.277 0.001 < 0.001
0.423 0.003 < 0.001
0.723 0.087 0.024
0.429 0.462 0.091
10° adduction
vs DDH without retroverted vs non-retroverted normal hips vs retroverted normal hips
0.703 0.007 0.001
0.437 0.173 0.029
0.094 0.824 0.365
0.009 0.244 0.242
20° adduction
vs DDH without retroverted vs non-retroverted normal hips vs retroverted normal hips
0.135 0.779 0.174
0.024 0.329 0.620
< 0.001 0.007 0.724
< 0.001 < 0.001 -
Fig. 9 Graph showing the results of anterior impingement tests for the developmentally dysplastic (DDH) and normal groups with and without acetabular retroversion in 0°, 10°, and 20° adduction (table shows p-values at each result).
90° flexion increased with decreasing acetabular rim coverage. The significantly larger ROM in these directions depend on the shallow acetabulum. Maximum internal rotation at 90° flexion also increased with greater femoral neck anteversion. The larger femoral neck anteversion in DDH contributed to the increased ROM as well. In contrast, increasing femoral anteversion reduced maximum external rotation due to a reduced distance until impingement. Increasing acetabular anteversion increased maximum flexion and reduced maximum extension. Significant VOL. 96-B, No. 5, MAY 2014
differences in cranial anteversion and femoral neck anteversion between groups might make the maximum ROM different but the differences in the location of impingement between groups resulted in no significant differences in maximum flexion and external rotation. Although larger alpha angles were noticed in DDH, the lack of correlation between alpha angle and ROM in any direction suggested that the effect of the difference was negligible. FAI is often caused by impingement between the acetabular rim and femoral neck in a combination of flexion,
588
I. NAKAHARA, M. TAKAO, T. SAKAI, H. MIKI, T. NISHII, N. SUGANO
DDH with high anteversion DDH with regular anteversion Normal with regular anteversion 0º adduction
10º adduction
40
30 20 10
External rotation
40 External rotation
External rotation
40
20º adduction
30 20
0
0 0
10 20 30 Extension
20 10
10
0
30
0
0
10 20 30 Extension
10 20 30 Extension
0° extension
10° extension
20° extension
30° extension
0° adduction
vs DDH with regular anteversion vs normal with regular anteversion
< 0.001 < 0.001
0.005 0.017
0.098 0.090
0.007 0.003
10° adduction
vs DDH with regular anteversion vs normal with regular anteversion
< 0.001 0.002
0.050 0.034
0.134 0.033
0.028 < 0.001
20° adduction
vs DDH with regular anteversion vs normal with regular anteversion
< 0.001 0.002
0.030 0.148
0.040 0.002
0.006
Fig. 10 Graph showing the results of posterior impingement tests for the developmental dysplastic hip group (DDH) with regular and high femoral neck anteversion and normal with regular femoral neck anteversion in 0°, 10°, and 20° adduction (p-values shown in table).
adduction, and internal rotation.8,9 Acetabular retroversion is one of the risk factors of FAI8,12-15 and is sometimes observed even in patients with DDH.16 In our study, larger ranges until anterior impingement were observed and the rate of extra-articular impingement was higher in DDH. Furthermore, maximum internal rotation at 90° flexion in DDH with acetabular retroversion was much larger than that in previous reports on FAI patients, which described mean values of 11°.18,19 Even when the acetabulum was retroverted, ranges were not restricted at all in adduction 0° and 10° in DDH compared to normal hips. However, in 20° abduction the ranges until anterior impingement decreased. Inferior areas of the acetabular rim and femoral neck come into contact with increased adduction, where ranges until impingement tend to be restricted in comparison with less adduction. The anterior impingement which occurs at inferior areas in DDH might have been responsible for the restricted ranges seen in excessive adduction in the retroverted pattern in DDH. Despite the restriction, the ranges were at least of a similar level compared to the retroverted normal hips. These results suggest that anterior intraarticular impingement seldom occurs in DDH during daily activities, even in the presence of a retroverted acetabulum. Ischiofemoral impingement is caused by impingement between the ischium and lesser trochanter in a combination
of extension, adduction, and external rotation.10,11 In the present study, the range until posterior impingement in DDH was limited when the hip was positioned with excessive extension with adduction and the prevalence of extraarticular impingement was much higher. DDH with a highly anteverted femoral neck notably restricted the ROM. These findings indicate that posterior extra-articular impingement will frequently occur in DDH, especially for hips with a highly anteverted femoral neck. As femoral offset in the AP view was reduced when the femoral neck anteversion was higher, the proximity of the ischium to the femur would influence the reduction in the ROM. Some limitations need to be considered in this study. First, control subjects were much older than DDH subjects. In older individuals, the pelvis tends to tilt backward with degenerative changes in the spine,32 which may influence the results of the analysis of the hip ROM. However, no normal subjects showed atypical backward tilt of the pelvis. Furthermore, because control subjects had neither symptoms nor osteoarthritic changes, despite their old age, selection of this elderly population as a control group was of value in representing normal hip joints in the true sense. Second, hips with severe subluxation such as Crowe Groups II, III, and IV23 DDH and hips with Perthes-like deformities were excluded from the present study. Since THE BONE & JOINT JOURNAL
THREE-DIMENSIONAL MORPHOLOGY AND BONY RANGE OF MOVEMENT IN HIP JOINTS IN PATIENTS WITH HIP DYSPLASIA
previous reports have shown that hip morphology differs according to the Crowe classification5,31 and hips with Perthes-like deformities display unique morphological characteristics,33 the ROM until bony impingement would differ in each subgroup due to morphological differences. We therefore focused solely on Crowe Group I DDH without any marked OA present, therefore allowing the present study to analyse range of hip movement and morphology based on the original acetabulum. In conclusion, significant differences in the ROM until bony impingement (including larger maximum extension and internal rotation at 90° flexion) were seen in DDH compared with normal hip joints. Although maximum flexion and external rotation were similar between groups, extra-articular impingement more frequently acted as the endpoint of the ROM in DDH. The shallower acetabulum and larger femoral neck anteversion contributed to the increased maximum ROM in DDH. Prevalence of cranial retroversion in DDH is similar to normal hips and the risk of anterior impingement in retroverted DDH is similar to that in retroverted normal hips in excessive adduction but minimal in less adduction. However, consideration should be given to extra-articular posterior impingement in DDH being one of the sources of hip pain, particularly in the presence of a highly anteverted femoral neck. No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. This article was primary edited by G. Scott and first proof edited by D. Rowley.
References 1. Rosendahl K, Markestad T, Lie RT. Developmental dysplasia of the hip: prevalence based on ultrasound diagnosis. Pediatr Radiol 1996;26:635–639. 2. Wiberg G. Studies on dysplastic acetabula and congenital subluxation of the hip joint, with special reference to the complication of osteo-arthritis. Acta Chir Scand Suppl 1939;83(Suppl 58):29–38. 3. Dandachli W, Kannan V, Richards R, et al. Analysis of cover of the femoral head in normal and dysplastic hips: new CT-based technique. J Bone Joint Surg [Br] 2008;90-B:1428–1434. 4. Murphy SB, Kijewski PK, Millis MB, Harless A. Acetabular dysplasia in the adolescent and young adult. Clin Orthop Relat Res 1990;(261):214–223. 5. Sugano N, Noble PC, Kamaric E, et al. The morphology of the femur in developmental dysplasia of the hip. J Bone Joint Surg [Br] 1998;80-B:711–719. 6. Chegini S, Beck M, Ferguson SJ. The effects of impingement and dysplasia on stress distributions in the hip joint during sitting and walking: a finite element analysis. J Orthop Res 2009;27:195–201. 7. Murphy SB, Ganz R, Müller ME. The prognosis in untreated dysplasia of the hip. A study of radiographic factors that predict the outcome. J Bone Joint Surg [Am] 1995;77-A:985–989. 8. Beck M, Kalhor M, Leunig M, Ganz R. Hip morphology influences the pattern of damage to the acetabular cartilage: femoroacetabular impingement as a cause of early osteoarthritis of the hip. J Bone Joint Surg [Br] 2005;87-B:1012–1018.
VOL. 96-B, No. 5, MAY 2014
589
9. Ganz R, Parvizi J, Beck M, et al. Femoroacetabular impingement: a cause for osteoarthritis of the hip. Clin Orthop Relat Res 2003;417:112–120. 10. Stafford GH, Villar RN. Ischiofemoral impingement. J Bone Joint Surg [Br] 2011;93-B:1300–1302. 11. Sutter R, Pfirrmann CW. Atypical hip impingement. AJR Am J Roentgenol 2013;201:W437–W442. 12. Banerjee P, McLean CR. Femoroacetabular impingement: a review of diagnosis and management. Curr Rev Musculoskelet Med 2011;4:23–32. 13. Tannast M, Siebenrock KA, Anderson SE. Femoroacetabular impingement: radiographic diagnosis--what the radiologist should know. AJR Am J Roentgenol 2007;188:1540–1552. 14. Jamali AA, Mladenov K, Meyer DC, et al. Anteroposterior pelvic radiographs to assess acetabular retroversion: high validity of the "cross-over-sign". J Orthop Res 2007;25:758–765. 15. Nötzli HP, Wyss TF, Stoecklin CH, et al. The contour of the femoral head-neck junction as a predictor for the risk of anterior impingement. J Bone Joint Surg [Br] 2002;84-B:556–560. 16. Fujii M, Nakashima Y, Yamamoto T, et al. Acetabular retroversion in developmental dysplasia of the hip. J Bone Joint Surg [Am] 2010;92-A:895–903. 17. Siebenrock KA, Steppacher SD, Haefeli PC, Schwab JM, Tannast M. Valgus hip with high antetorsion causes pain through posterior extraarticular FAI. Clin Orthop Relat Res 2013;471:3774–3780. 18. Beck M, Leunig M, Parvizi J, et al. Anterior femoroacetabular impingement: part II. Midterm results of surgical treatment. Clin Orthop Relat Res 2004;418:67–73. 19. Kubiak-Langer M, Tannast M, Murphy SB, Siebenrock KA, Langlotz F. Range of motion in anterior femoroacetabular impingement. Clin Orthop Relat Res 2007;458:117–124. 20. Tannast M, Kubiak-Langer M, Langlotz F, et al. Noninvasive three-dimensional assessment of femoroacetabular impingement. J Orthop Res 2007;25:122–131. 21. Tannast M, Hanke M, Ecker TM, et al. LCPD: reduced range of motion resulting from extra- and intraarticular impingement. Clin Orthop Relat Res 2012;470:2431– 2440. 22. Nakahara I, Takao M, Sakai T, et al. Gender differences in 3D morphology and bony impingement of human hips. J Orthop Res 2011;29:333–339. 23. Crowe JF, Mani VJ, Ranawat CS. Total hip replacement in congenital dislocation and dysplasia of the hip. J Bone Joint Surg [Am] 1979;61-A:15–23. 24. Tönnis D. Normal values of the hip joint for the evaluation of X-rays in children and adults. Clin Orthop Relat Res 1976;119:39–47. 25. Lorensen W, Cline H. Marching cubes: a high resolution 3D surface construction algorithm. Computer Graphics 1987;21:163–170. 26. Schroeder W, Martin K, Lorensen W. The Visualization Toolkit: An Object Orient Approach to Computer Graphics. Second ed. New Jersey: Prentice Hall, 1997. 27. Jiménez P, Thomas F, Torras C. 3D collision detection: a survey. Comp Graph 2001;25:269–285. 28. Lohfert H, Schmelzeisen H. Biomechanics of the femoral neck. Calculation of pressure and tension distribution in the human femoral neck, applying principles of the theory of elasticity and strength of materials. Arch Orthop Trauma Surg 1980;96:31– 33. 29. Sugano N, Noble PC, Kamaric E. A comparison of alternative methods of measuring femoral anteversion. J Comput Assist Tomogr 1998;22:610–614. 30. Fujii M, Nakashima Y, Sato T, Akiyama M, Iwamoto Y. Pelvic deformity influences acetabular version and coverage in hip dysplasia. Clin Orthop Relat Res 2011;469:1735–1742. 31. Noble PC, Kamaric E, Sugano N, et al. Three-dimensional shape of the dysplastic femur: implications for THR. Clin Orthop Relat Res 2003;417:27–40. 32. Nishihara S, Sugano N, Nishii T, Ohzono K, Yoshikawa H. Measurements of pelvic flexion angle using three-dimensional computed tomography. Clin Orthop Relat Res 2003;411:140–151. 33. Catterall A, Pringle J, Byers PD, et al. A review of the morphology of Perthes' disease. J Bone Joint Surg [Br] 1982;64-B:269–275.
Three-dimensional morphology and bony range of movement in hip joints in patients with hip dysplasia I. Nakahara, M. Takao, T. Sakai, H. Miki, T. Nishii, N. Sugano From Department of Orthopaedic Medical Engineering, Osaka University Graduate School of Medicine, 2-2, Yamadaoka, Suita, 565-0871, Japan
To confirm whether developmental dysplasia of the hip has a risk of hip impingement, we analysed maximum ranges of movement to the point of bony impingement, and impingement location using three-dimensional (3D) surface models of the pelvis and femur in combination with 3D morphology of the hip joint using computer-assisted methods. Results of computed tomography were examined for 52 hip joints with DDH and 73 normal healthy hip joints. DDH shows larger maximum extension (p = 0.001) and internal rotation at 90° flexion (p < 0.001). Similar maximum flexion (p = 0.835) and external rotation (p = 0.713) were observed between groups, while high rates of extra-articular impingement were noticed in these directions in DDH (p < 0.001). Smaller cranial acetabular anteversion (p = 0.048), centre-edge angles (p < 0.001), a circumferentially shallower acetabulum, larger femoral neck anteversion (p < 0.001), and larger alpha angle were identified in DDH. Risk of anterior impingement in retroverted DDH hips is similar to that in retroverted normal hips in excessive adduction but minimal in less adduction. These findings might be borne in mind when considering the possibility of extra-articular posterior impingement in DDH being a source of pain, particularly for patients with a highly anteverted femoral neck. Cite this article: Bone Joint J 2014;96-B:580–9.
I. Nakahara, MD, PhD, Orthopaedic Surgeon H. Miki, MD, PhD, Orthopaedic Surgeon Osaka National Hospital, Department of Orthopaedic Surgery, 2-1-14 Hoenzaka Chuoku, Osaka, 540-0006, Japan. M. Takao, MD, PhD, Orthopaedic Surgeon, Assistant Professor T. Sakai, MD, PhD, Orthopaedic Surgeon, Lecturer Osaka University Graduate School of Medicine, Department of Orthopaedic Surgery, 2-2, Yamadaoka, Suita, 565-0871, Japan. T. Nishii, MD, PhD, Orthopaedic Surgeon, Assistant Professor Osaka University Graduate School of Medicine, Department of Orthopaedic Medical Engineering, 2-2, Yamadaoka, Suita, 565-0871, Japan. N. Sugano, MD, PhD, Orthopaedic Surgeon, Professor Osaka University Graduate School of Medicine, Department of Orthopaedic Medical Engineering, 2-2, Yamadaoka, Suita, 565-0871, Japan. Correspondence should be sent to Dr N. Sugano; e-mail: [email protected] ©2014 The British Editorial Society of Bone & Joint Surgery doi:10.1302/0301-620X.96B5. 32503 $2.00 Bone Joint J 2014;96-B:580–9. Received 27 May 2013; Accepted after revision 31 January 2014
580
Developmental dysplasia of the hip (DDH) is a major cause of secondary osteoarthritis (OA).1,2 DDH shows characteristic anatomical abnormalities, including a shallow acetabulum, acetabular mal-orientation, and a highly anteverted femoral neck.3-5 These abnormalities cause hip instability and increased joint contact pressure,6 leading to cartilage damage and subsequent OA.7 In the contemporary literature, hip pain induced by femoro-acetabular impingement (FAI)8,9 and ischiofemoral impingement10,11 has been attracting attention. Symptomatic hips with FAI display characteristic morphological features such as over-coverage of the anterior acetabulum, a deep acetabular socket, a non-spherical femoral head, or reduced head–neck offset.8,12-15 Among patients with DDH, the cross-over sign on plain radiographs is considered suggestive of anterior impingement and is reportedly present in 18% of cases.16 Patients with DDH show the morphological features of a highly anteverted femoral neck, which has been reported as a risk factor for posterior impingement.11,17 These findings have led us to question whether some patients with DDH have symptoms due to anterior or posterior impingement.
Although proper diagnosis and early intervention may relieve hip pain and possibly prevent development of hip OA in impingement-related disorders,18 the range of movement (ROM) to the point of bony impingement could be better understood in order to clarify the rationale of such interventions. Computer-assisted measurement of the ROM using three-dimensional (3D) models of the pelvis and femur provides an assessment of relative movement between the pelvis and femur to the point of impingement, and allows identification of the site of impingement. Applying this methodology, the maximum range of hip movement in symptomatic hip joints due to FAI,19,20 with Legg–Calvé–Perthes disease,21 coxa valga and highly anteverted femoral necks,20 and normal healthy hip joints,22 have been reported; however, the maximum ROM in DDH patients has not. The primary purpose of this study was to investigate the ROM to the point of bony impingement and its location in DDH. The secondary purpose was to measure the 3D morphology of the acetabulum and proximal femur in order to clarify which morphological parameters influence the ROM. Finally the effects of acetabular retroversion and a highly anteverted femoral neck on anterior and posterior impingement, respectively, were studied. THE BONE & JOINT JOURNAL
THREE-DIMENSIONAL MORPHOLOGY AND BONY RANGE OF MOVEMENT IN HIP JOINTS IN PATIENTS WITH HIP DYSPLASIA
581
Table I. Demographic data of subjects. Data are shown as mean (range) (DDH, developmental dysplasia of the hip) Subjects
DDH n = 29 (52 joints)
Normal n = 49 (73 joints)
p-value*
Age (years) (range) Height (cm) (range) Weight (kg) (range) BMI (kg/m2) (range)
33.0 (16 to 48) 158.1 (147 to 171) 54.0 (46 to 77) 21.6 (18.6 to 31.6)
71.7 (63 to 80) 151.7 (140 to 165) 49.9 (35 to 69) 21.7 (13.7 to 28.4)
< 0.001 < 0.001 0.019 0.930
* Mixed-model ANOVA
Materials and Methods The present investigation used a database of CT images which had been obtained for pre-operative surgical planning for pelvic osteotomies due to DDH from 2006 to 2012. Inclusion criteria were Crowe Group-I DDH23 with a centre-edge (CE) angle ≤ 20°2 on plain anteroposterior (AP) radiography, that had neither signs of advanced or terminal OA (Tönnis classification ≥ grade 2)24 nor Perthes-like femoral head deformity. The DDH group comprised 52 hip joints in 29 women with a mean age of 33.0 years (16 to 48). As controls, CT images of 73 normal hip joints from 49 healthy female volunteers with a mean age of 71.7 years (63 to 80) were obtained from the normal CT image database which was developed for research according to the following criteria: no hip symptoms, no signs of OA (Tönnis classification ≥ grade 1) nor acetabular dysplasia (CE angle ≤ 20°) and no previous hip surgery (Table I). The entire pelvis and bilateral femora were scanned using a helical CT scanner (HiSpeed Advantage, GE Medical Systems, Milwaukee, Wisconsin) with a slice pitch of 1 mm and 1.25 mm thickness. All study protocols were approved by the institutional review board. Both ROM and morphological measurements were performed on standard pelvic and femoral co-ordinate systems. The pelvic reference co-ordinates were defined by sagittal pelvic tilt in the supine position and bilateral anterior superior iliac spines. The femoral reference co-ordinates were defined by the posterior femoral plane, including the most posterior point of the greater trochanter and the posterior femoral condyles, the centre of the femoral head, and the knee centre.22 3D surface models of the pelvis and femur were reconstructed from CT data using an algorithm of marching cubes25 published in the Visualization Toolkit.26 The centre of the femoral head as determined by a best-fit sphere technique was set to be the centre of rotation of the femur, and neutral position of the hip joint was determined when both pelvic and femoral co-ordinates were parallel. Collision of the pelvic and femoral models was automatically checked by rotating the femoral models 0.5° at a time until overlapping of the polygons occurred. The V-Collide library developed at the University of North Carolina, Chapel Hill was used for collision detection.27 Maximum flexion, extension, external rotation, and internal rotation at VOL. 96-B, No. 5, MAY 2014
90° flexion were calculated in each patient model. Additionally, two movement patterns corresponding to the anterior and posterior impingement test9,10 were evaluated. For the anterior impingement test, maximum internal rotation was measured in 10° increments between 80° and 110° of flexion and 0° and 20° of adduction. For the posterior impingement test, maximum external rotation was measured in 10° increments between 0° and 30° of extension and 0° and 20° of adduction. The locations of impingement on both the pelvic and femoral sides were determined for every movement in each patient model. Possible pelvic impingement areas were defined as the acetabular rim, ischium, posterior acetabular wall surface, around the anterior inferior iliac spine, and around the anterior superior iliac spine. The areas of possible femoral impingement were divided into the femoral neck, greater and lesser trochanters, intertrochanteric crest, distal side of the femoral neck, and the femoral shaft. Locations of the rim were further divided in a clock system by defining the locations of the anterior rim, deepest acetabular notch, and posterior rim as three, six, and nine o’clock, respectively. Locations of the femoral neck were also further divided in a clock system by defining the anterior location, the most prominent point of Adam’s arch,28 which shows the thickened medial cortex at the femoral neck, and the posterior location as three, six, and nine o’clock, respectively. Impingement type was specified as intra- or extraarticular impingement according to the location of the impingement zone. Impingement between the rim and neck was defined as intra-articular impingement, and that between all other anatomical areas was defined as extraarticular impingement. Using 3D-viewer software (3D Template; Japan Medical Materials, Osaka, Japan), three orthogonal planes (coronal, sagittal, and axial) were reconstructed. On the axial views, at the femoral head centre level (level 0), and onethird (level 1) and two-thirds (level 2) of femoral head radius from the femoral head centre, the acetabular anteversion was measured. When the anteversion angle was negative at any level, the acetabulum was defined as retroverted. Lateral and anterior CE angles were measured on coronal and sagittal views through the femoral head centre, respectively. When the lateral CE angle was less than 0°, the
582
I. NAKAHARA, M. TAKAO, T. SAKAI, H. MIKI, T. NISHII, N. SUGANO
Fig. 1 3D image showing multiple radial planes through the acetabular axis reconstructed at increments of 15° from the deepest part of the acetabular notch. Acetabular edge angle was defined as the angle between the acetabular axis and a line between the centre of the femoral head and the acetabular edge point in each radial plane.
Fig. 2 3D image showing multiple planes including the femoral neck axis reconstructed at increments of 15° from the most prominent part of Adam’s arch. On each plane, the alpha angle was measured.
anterior CE angle was considered to be 0°. To examine acetabular rim coverage three-dimensionally, a plane including the anterior and posterior acetabular edges on the axial plane and the superior acetabular edge on the coronal plane was defined as the acetabular opening plane, while the line perpendicular to this plane and passing through the centre of the femoral head was defined as the acetabular axis. Multiple radial planes through the acetabular axis were reconstructed by rotating planes around the axis in 15° increments from the deepest acetabular notch. On each plane, the angle between the acetabular axis and a line connecting the femoral head centre and acetabular edge was measured (Fig. 1). Locations of the rim were given using the same clock system used for impingement location. On the femoral side, femoral neck anteversion and neck shaft angle were measured according to the previously reported method.29 To investigate the alpha angle15 of the
femoral neck three-dimensionally, multiple radial planes through the femoral neck axis were reconstructed at 15° increments from the most prominent part of Adam’s arch. In each plane, the alpha angle was measured (Fig. 2).15 Locations were again given using the same clock system used for the location of impingement. Statistical analysis. Statistical comparisons of demographic data, ROM, and morphological parameters between the DDH and normal groups were made using a mixed-model analysis of variance (ANOVA) regarding each subject as a random effect and each group as a fixed effect. When each group was further divided into subgroups based on impingement location (extra- or intra-articular impingement), acetabular anteversion (with or without retroversion), and femoral neck anteversion (regularly or highly anteverted), we used a Kruskal–Wallis test to compare subgroups; if significant, we used the Mann–Whitney U test to THE BONE & JOINT JOURNAL
THREE-DIMENSIONAL MORPHOLOGY AND BONY RANGE OF MOVEMENT IN HIP JOINTS IN PATIENTS WITH HIP DYSPLASIA
583
Table II. Range of movement (ROM) and impingement locations in both groups
Mean flexion (°) (range) No. of intra-articular impingements (n, %) No. of extra-articular impingements (n, %) Mean extension in degrees (range) No. of intra-articular impingements (n, %) No. of extra-articular impingements (n, %) Mean external rotation in degrees (range) No. of intra-articular impingements (n, %) No. of extra-articular impingements (n, %) Mean internal rotation at 90° flexion (°) (range) No. of intra-articular impingements (n, %) No. of extra-articular impingements (n, %)
DDH
Normal
p-value
130.3 (105.5 to 153.0) 18 (34.6) 34 (65.4) 66.3 (17.5 to 146.0) 52 (100) 0 (0) 34.5 (7.5 to 68.0) 0 (0) 52 (100) 70.8 (34.5 to 107.5) 49 (94.2) 3 (5.8)
129.2 (113.5 to 146.5) 58 (79.5) 15 (20.5) 50.6 (0.5 to 95.0) 73 (100) 0 (0) 35.3 (0.5 to 67.5) 44 (60.3) 29 (39.7) 49.6 (27.5 to 80.5) 71 (97.3) 2 (2.7)
0.835* < 0.001† 0.001* 0.713* < 0.001‡ < 0.001* 0.648‡
* Mixed-model ANOVA † Chi-squared test ‡ Fisher’s exact test
P < 0.001 0.005
0.032
< 0.001
100
50
< 0.001 0.004
100
60 Degrees
40
50
20
ar ul
ul
ic
ic
rt tr Ex
In
tr
aa
aa
rt
aa
aa tr Ex
tr In
rt
ic
ic
ul
ul
ar
ar External rotation
rt
ul ic rt aa
Ex
In
tr
tr
tr
aa
aa
rt
rt
ic
ic
ul
ar
ar
ar ul
ul ic rt
aa tr
aa tr In Flexion
Ex
aa
rt
rt
ic
ic
ul
ar
ar
ar ul
ar ul ic tr
aa
rt
Ex
tr In
0
ar
0
0
Ex
Degrees
150
P < 0.001
P = 0.026
0.246 < 0.001 0.001 0.182
Degrees
DDH Normal
Internal rotation
Fig. 3 Detailed range of movement (ROM) analysis (mean with range) in directions of flexion, external rotation, and internal rotation at 90° flexion according to impingement locations (Overall p-values (top) measured using the Kruskal–Wallis test; all other p-values used the Mann–Whitney U test).
compare each group. Mann–Whitney U tests were conducted to detect differences in location of impingement zones on the acetabular rim and femoral neck. The chisquared test or Fisher’s exact test were applied to detect differences in the prevalence of intra- and extra-articular impingement. A correlation analysis was performed to examine the relationship between morphological parameters and ROM for both the DDH and normal groups using the Pearson linear correlation coefficient (r). Differences were defined as statistically significant for probability values less than 5%.
Results Maximum extension and internal rotation at 90° flexion was significantly larger in the DDH group than in the normal group. No significant differences were seen in maximum flexion and external rotation. The rate of extraarticular impingement was significantly higher in these directions in the DDH group (Table II). The maximum flexVOL. 96-B, No. 5, MAY 2014
ion until extra-articular impingement was significantly larger than that until intra-articular impingement in both the DDH and normal groups. However, ROM, until either intra- or extra-articular impingement, did not differ significantly between DDH and normal groups. The range of internal rotation at 90° flexion until intra-articular impingement in the normal group was significantly smaller than that in the DDH group, regardless of impingement location. There was no difference in maximum external rotation among the subgroups based on impingement location (Fig. 3). For the anterior impingement simulation, significantly larger maximum internal rotation angles were observed in the DDH group, except for 100° and 110° of flexion with 20° of adduction (Fig. 4). For the posterior impingement simulation, maximum external rotation decreased in the DDH group for the composite movement in 30° of extension with 10° of adduction (Fig. 5). From the analysis of impingement locations, the anterior impingement zones on
I. NAKAHARA, M. TAKAO, T. SAKAI, H. MIKI, T. NISHII, N. SUGANO
40 20 0
80
90
100
20° adduction
10° adduction 80
< 0.001
0.002
60
0.012
40 20 0
110
< 0.001
80
90
Flexion
100
Internal rotation
DDH 0° adduction Normal < 0.001 80 < 0.001 < 0.001 < 0.001 60
Internal rotation
Internal rotation
584
80 0.001 0.008
60
0.053 40 0.124 20 0
110
80
Flexion
90
100
110
Flexion
Fig. 4 Graph showing the results of anterior impingement tests for the developmental dysplasia of the hip (DDH) and normal groups in 0°, 10°, and 20° adduction. The solid line indicates the mean for dysplasia; the dotted line indicates the normal mean with error bars showing the 95% confidence interval (p-values shown above each result used the mixed-model ANOVA).
0.833 0.252
10 0 10
20
Extension
30
30
0.948 0.842
20
0.507 10 0
0.012
External rotation
30
0
40
40
0.870
20
20° adduction
10° adduction
External rotation
External rotation
DDH 0° adduction Normal 0.877 40
30 20
0.720 0.283
10
0.985 0.062 0
0
10
20
Extension
30
0
10
20
30
Extension
Fig. 5 Graph showing results of posterior impingement tests for the developmental dysplasia of the hip (DDH) and normal groups in 0°, 10°, and 20° adduction. The solid line indicates the mean for dysplasia, the dotted line indicates the normal mean with error bars showing the 95% confidence interval (p-values shown above each result use the mixed-model ANOVA).
the femoral neck and posterior impingement zones on the acetabular rim were located more inferiorly in the DDHgroup. A higher prevalence of extra-articular impingement was observed for both anterior and posterior impingement tests in the DDH group (Fig. 6). The DDH group showed significantly smaller cranial acetabular anteversion and CE angles and larger femoral neck anteversion compared with the normal group (Table III). In 3D analysis of acetabular rim coverage, the DDH group also showed lower coverage at all locations compared with the normal group. In both groups, three prominences and three depressions were identified at consistent locations; these prominences were seen generally at clock positions between 1 o’clock and 2 o’clock, between 4 o’clock and 5 o’clock, and between 7 o’clock and 8 o’clock, and the depressions were seen commonly at 11 o’clock, 3 o’clock, and 6 o’clock (Fig. 7). Analysis of the alpha angle, also revealed a significantly larger alpha angle at clock positions from 2 o’clock to 3 o’clock and from 6 to 9 o’clock in the DDH group (Fig. 8).
Correlation analysis identified that the maximum flexion showed a positive correlation with acetabular anteversion, as well as weak negative correlations with anterior CE angle and neck–shaft angle. Acetabular anteversion, CE angles, and mean acetabular rim coverage all correlated negatively with maximum extension. In external rotation, negative correlations were indicated with both acetabular anteversion and femoral neck anteversion. The maximum internal rotation at 90° flexion correlated negatively with CE angles and mean acetabular rim coverage and positively with femoral neck anteversion and neck–shaft angle. The alpha angle did not show correlations with any direction of the ROM (Table IV). The retroverted acetabulum was observed only at the cranial level in eight hips (15.3%) in the DDH group and in five hips (6.8%) in the normal group. No significant difference in prevalence was seen between groups (p = 0.214, chi-squared test). The retroverted DDH hips showed smaller ranges until anterior impingement than the remaining DDH cases in excessive flexion and adduction. THE BONE & JOINT JOURNAL
THREE-DIMENSIONAL MORPHOLOGY AND BONY RANGE OF MOVEMENT IN HIP JOINTS IN PATIENTS WITH HIP DYSPLASIA
585
Table III. Morphological measurements for both groups
Acetabular anteversion (level 0) Acetabular anteversion (level 1) Acetabular anteversion (level 2) Lateral CE angle Anterior CE angle Femoral anteversion Neck–shaft angle
DDH
Normal
p-value*
22.1 (0.2 to 36.4) 18.9 (-3.2 to 37.4) 12.9 (-9.5 to 34.1) 4.6 (-15.5 to 17.9) 23.1 (0 to 53.8) 38.9 (8.3 to 66.0) 126.9 (119.1 to 140.0)
23.3 (12.8 to 37.4) 22.4 (0.2 to 39.3) 16.8 (-3.4 to 38.0) 35.6 (21.4 to 59.2) 58.6 (34.6 to 73.9) 25.1 (1.0 to 47.5) 125.6 (113.1 to 137)
0.251 0.053 0.048 < 0.001 < 0.001 < 0.001 0.230
* Mixed-model ANOVA test
Anterior impingement pelvic side
Anterior impingement femoral side
100
100
80
DDH Normal
DDH Normal
P = 0.054
60
40
P < 0.001
60
Rate (%)
Rate (%)
80
40
P < 0.001 20
20
0
0
P < 0.001
Intraarticular Posterior impingement pelvic side
P < 0.001
100
DDH Normal
80 P < 0.001
60
Rate (%)
Rate (%)
80
100
40
Posterior impingement femoral side P < 0.001
DDH Normal
P = 0.371
60
40
20
20
0
0
Intraarticular
Intraarticular Fig. 6
Histograms showing the impingement zones for anterior impingement tests and posterior impingement tests in developmental dysplasia of the hip (DDH) and normal hips
Compared with the retroverted normal hips, ranges until anterior impingement were significantly larger in less flexion and adduction and were not restricted in any hip positions. The comparison with the non-retroverted normal hips, revealed ranges until anterior impingement that were also significantly larger in less flexion and adduction but in excessive flexion and adduction, they were restricted (Fig. 9). A highly anteverted femoral neck over 50° was observed in only 13 hips of the DDH group (25%) VOL. 96-B, No. 5, MAY 2014
and the prevalence was significantly different (p < 0.001, Fisher’s exact test). Significantly smaller ranges until posterior impingement were frequently observed compared with DDH and normal hips with regular anteversion (Fig. 10).
Discussion We have demonstrated maximum extension and internal rotation at 90° flexion in DDH which were significantly larger when compared to normal hip joints. In flexion and
586
I. NAKAHARA, M. TAKAO, T. SAKAI, H. MIKI, T. NISHII, N. SUGANO
DDH Normal
Angle (º)
100 90 80 70 60 0:00 1:30 3:00 4:30 6:00 7:30 9:00 10:30 Acetabular location Fig. 7 Graph showing the result of circumferential acetabular edge angle. The solid line indicates the mean for developmentally dysplastic hips (DDH); the dotted line indicates the normal mean with error bars showing the 95% confidence interval. Significant differences in acetabular edge angle existed in all locations (p < 0.001; mixed-model ANOVA).
DDH Normal
Angle (º)
50 45 40 35 30 0:00 1:30 3:00 4:30 6:00 7:30 9:00 10:30 Femoral neck location
Location
p-value
0.00 0.30 1.00 1.30 2.00 2.30 3.00 3.30 4.00 4.30 5.00 5.30 6.00 6.30 7.00 7.30 8.00 8.30 9.00 9.30 10.00 10.30 11.00 11.30
0.885 0.153 0.936 0.054 0.034 0.005 0.003 0.531 0.329 0.054 0.458 0.444 0.026 0.005 < 0.001 0.006 0.010 0.039 0.413 0.942 0.453 0.722 0.392 0.566
Fig. 8 Graph showing the result of circumferential alpha angle. The solid line indicates the mean for the developmentally dysplastic hips (DDH) group; the dotted line indicates the mean for the normal group with error bars showing the 95% confidence interval (p-values were assessed using the mixed-model ANOVA).
external rotation, we identified no significant differences in maximum ROM. In the present study, smaller CE angles and a more anteverted femoral neck were confirmed in DDH. These findings mirror previous reports.3-5,30,31 The 3D analysis of the acetabular rim demonstrated that its coverage in DDH was significantly lower in each location but the wave-
shaped pattern of the rim was similar to that of normal hips, although the acetabulum is shallower overall. Circumferential alpha-angle analysis of hips with DDH showed larger alpha angles in the anterosuperior and postero-inferior aspects compared to normal hips. Some of these differences in morphology correlated with the ROM. Maximum extension and internal rotation at THE BONE & JOINT JOURNAL
THREE-DIMENSIONAL MORPHOLOGY AND BONY RANGE OF MOVEMENT IN HIP JOINTS IN PATIENTS WITH HIP DYSPLASIA
587
Table IV. Coefficients of correlation (r) (with p-value) between range of movement (ROM) and morphological parameters
Acetabular anteversion (level 0) Acetabular anteversion (level 1) Acetabular anteversion (level 2) Lateral CE angle Anterior CE angle Mean acetabular rim coverage Femoral neck anteversion Neck–shaft angle Mean alpha angle
Flexion
Extension
External rotation
Internal rotation at 90° flexion
0.491* (< 0.001) 0.461* (< 0.001) 0.507* (< 0.001) -0.171 (0.056) -0.298* (< 0.001) -0.139 (0.121) 0.108 (0.230) -0.241† (0.007) -0.097 (0.280)
-0.516* (< 0.001) -0.504* (< 0.001) -0.464* (< 0.001) -0.457* (< 0.001) -0.384* (< 0.001) -0.459* (< 0.001) -0.145 (0.108) 0.110 (0.221) 0.164 (0.069)
-0.324* (< 0.001) -0.254† (0.004) -0.249† (0.005) -0.012 (0.896) 0.061 (0.498) -0.060 (0.506) -0.619* (< 0.001) 0.037 (0.676) 0.025 (0.781)
0.043 (0.636) -0.096 (0.289) -0.037 (0.679) -0.704* (< 0.001) -0.675* (< 0.001) -0.679* (< 0.001) 0.775* (< 0.001) 0.209‡ (0.019) 0.038 (0.670)
* p < 0.001 † p < 0.01 ‡ p < 0.05
DDH with retroverted DDH with non-retroverted Normal with retroverted Normal with non-retroverted 10º adduction
20º adduction
100
100
80
80
80
60 40 20
Internal rotation
100 Internal rotation
Internal rotation
0º adduction
60 40
0
0 80
90
100
110
40 20
20
0
60
80
90
Flexion
100
80
110
90
100
110
Flexion
Flexion 80° flexion
90° flexion
100° flexion
110° flexion
0° adduction
vs DDH without retroverted vs non-retroverted normal hips vs retroverted normal hips
0.277 0.001 < 0.001
0.423 0.003 < 0.001
0.723 0.087 0.024
0.429 0.462 0.091
10° adduction
vs DDH without retroverted vs non-retroverted normal hips vs retroverted normal hips
0.703 0.007 0.001
0.437 0.173 0.029
0.094 0.824 0.365
0.009 0.244 0.242
20° adduction
vs DDH without retroverted vs non-retroverted normal hips vs retroverted normal hips
0.135 0.779 0.174
0.024 0.329 0.620
< 0.001 0.007 0.724
< 0.001 < 0.001 -
Fig. 9 Graph showing the results of anterior impingement tests for the developmentally dysplastic (DDH) and normal groups with and without acetabular retroversion in 0°, 10°, and 20° adduction (table shows p-values at each result).
90° flexion increased with decreasing acetabular rim coverage. The significantly larger ROM in these directions depend on the shallow acetabulum. Maximum internal rotation at 90° flexion also increased with greater femoral neck anteversion. The larger femoral neck anteversion in DDH contributed to the increased ROM as well. In contrast, increasing femoral anteversion reduced maximum external rotation due to a reduced distance until impingement. Increasing acetabular anteversion increased maximum flexion and reduced maximum extension. Significant VOL. 96-B, No. 5, MAY 2014
differences in cranial anteversion and femoral neck anteversion between groups might make the maximum ROM different but the differences in the location of impingement between groups resulted in no significant differences in maximum flexion and external rotation. Although larger alpha angles were noticed in DDH, the lack of correlation between alpha angle and ROM in any direction suggested that the effect of the difference was negligible. FAI is often caused by impingement between the acetabular rim and femoral neck in a combination of flexion,
588
I. NAKAHARA, M. TAKAO, T. SAKAI, H. MIKI, T. NISHII, N. SUGANO
DDH with high anteversion DDH with regular anteversion Normal with regular anteversion 0º adduction
10º adduction
40
30 20 10
External rotation
40 External rotation
External rotation
40
20º adduction
30 20
0
0 0
10 20 30 Extension
20 10
10
0
30
0
0
10 20 30 Extension
10 20 30 Extension
0° extension
10° extension
20° extension
30° extension
0° adduction
vs DDH with regular anteversion vs normal with regular anteversion
< 0.001 < 0.001
0.005 0.017
0.098 0.090
0.007 0.003
10° adduction
vs DDH with regular anteversion vs normal with regular anteversion
< 0.001 0.002
0.050 0.034
0.134 0.033
0.028 < 0.001
20° adduction
vs DDH with regular anteversion vs normal with regular anteversion
< 0.001 0.002
0.030 0.148
0.040 0.002
0.006
Fig. 10 Graph showing the results of posterior impingement tests for the developmental dysplastic hip group (DDH) with regular and high femoral neck anteversion and normal with regular femoral neck anteversion in 0°, 10°, and 20° adduction (p-values shown in table).
adduction, and internal rotation.8,9 Acetabular retroversion is one of the risk factors of FAI8,12-15 and is sometimes observed even in patients with DDH.16 In our study, larger ranges until anterior impingement were observed and the rate of extra-articular impingement was higher in DDH. Furthermore, maximum internal rotation at 90° flexion in DDH with acetabular retroversion was much larger than that in previous reports on FAI patients, which described mean values of 11°.18,19 Even when the acetabulum was retroverted, ranges were not restricted at all in adduction 0° and 10° in DDH compared to normal hips. However, in 20° abduction the ranges until anterior impingement decreased. Inferior areas of the acetabular rim and femoral neck come into contact with increased adduction, where ranges until impingement tend to be restricted in comparison with less adduction. The anterior impingement which occurs at inferior areas in DDH might have been responsible for the restricted ranges seen in excessive adduction in the retroverted pattern in DDH. Despite the restriction, the ranges were at least of a similar level compared to the retroverted normal hips. These results suggest that anterior intraarticular impingement seldom occurs in DDH during daily activities, even in the presence of a retroverted acetabulum. Ischiofemoral impingement is caused by impingement between the ischium and lesser trochanter in a combination
of extension, adduction, and external rotation.10,11 In the present study, the range until posterior impingement in DDH was limited when the hip was positioned with excessive extension with adduction and the prevalence of extraarticular impingement was much higher. DDH with a highly anteverted femoral neck notably restricted the ROM. These findings indicate that posterior extra-articular impingement will frequently occur in DDH, especially for hips with a highly anteverted femoral neck. As femoral offset in the AP view was reduced when the femoral neck anteversion was higher, the proximity of the ischium to the femur would influence the reduction in the ROM. Some limitations need to be considered in this study. First, control subjects were much older than DDH subjects. In older individuals, the pelvis tends to tilt backward with degenerative changes in the spine,32 which may influence the results of the analysis of the hip ROM. However, no normal subjects showed atypical backward tilt of the pelvis. Furthermore, because control subjects had neither symptoms nor osteoarthritic changes, despite their old age, selection of this elderly population as a control group was of value in representing normal hip joints in the true sense. Second, hips with severe subluxation such as Crowe Groups II, III, and IV23 DDH and hips with Perthes-like deformities were excluded from the present study. Since THE BONE & JOINT JOURNAL
THREE-DIMENSIONAL MORPHOLOGY AND BONY RANGE OF MOVEMENT IN HIP JOINTS IN PATIENTS WITH HIP DYSPLASIA
previous reports have shown that hip morphology differs according to the Crowe classification5,31 and hips with Perthes-like deformities display unique morphological characteristics,33 the ROM until bony impingement would differ in each subgroup due to morphological differences. We therefore focused solely on Crowe Group I DDH without any marked OA present, therefore allowing the present study to analyse range of hip movement and morphology based on the original acetabulum. In conclusion, significant differences in the ROM until bony impingement (including larger maximum extension and internal rotation at 90° flexion) were seen in DDH compared with normal hip joints. Although maximum flexion and external rotation were similar between groups, extra-articular impingement more frequently acted as the endpoint of the ROM in DDH. The shallower acetabulum and larger femoral neck anteversion contributed to the increased maximum ROM in DDH. Prevalence of cranial retroversion in DDH is similar to normal hips and the risk of anterior impingement in retroverted DDH is similar to that in retroverted normal hips in excessive adduction but minimal in less adduction. However, consideration should be given to extra-articular posterior impingement in DDH being one of the sources of hip pain, particularly in the presence of a highly anteverted femoral neck. No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. This article was primary edited by G. Scott and first proof edited by D. Rowley.
References 1. Rosendahl K, Markestad T, Lie RT. Developmental dysplasia of the hip: prevalence based on ultrasound diagnosis. Pediatr Radiol 1996;26:635–639. 2. Wiberg G. Studies on dysplastic acetabula and congenital subluxation of the hip joint, with special reference to the complication of osteo-arthritis. Acta Chir Scand Suppl 1939;83(Suppl 58):29–38. 3. Dandachli W, Kannan V, Richards R, et al. Analysis of cover of the femoral head in normal and dysplastic hips: new CT-based technique. J Bone Joint Surg [Br] 2008;90-B:1428–1434. 4. Murphy SB, Kijewski PK, Millis MB, Harless A. Acetabular dysplasia in the adolescent and young adult. Clin Orthop Relat Res 1990;(261):214–223. 5. Sugano N, Noble PC, Kamaric E, et al. The morphology of the femur in developmental dysplasia of the hip. J Bone Joint Surg [Br] 1998;80-B:711–719. 6. Chegini S, Beck M, Ferguson SJ. The effects of impingement and dysplasia on stress distributions in the hip joint during sitting and walking: a finite element analysis. J Orthop Res 2009;27:195–201. 7. Murphy SB, Ganz R, Müller ME. The prognosis in untreated dysplasia of the hip. A study of radiographic factors that predict the outcome. J Bone Joint Surg [Am] 1995;77-A:985–989. 8. Beck M, Kalhor M, Leunig M, Ganz R. Hip morphology influences the pattern of damage to the acetabular cartilage: femoroacetabular impingement as a cause of early osteoarthritis of the hip. J Bone Joint Surg [Br] 2005;87-B:1012–1018.
VOL. 96-B, No. 5, MAY 2014
589
9. Ganz R, Parvizi J, Beck M, et al. Femoroacetabular impingement: a cause for osteoarthritis of the hip. Clin Orthop Relat Res 2003;417:112–120. 10. Stafford GH, Villar RN. Ischiofemoral impingement. J Bone Joint Surg [Br] 2011;93-B:1300–1302. 11. Sutter R, Pfirrmann CW. Atypical hip impingement. AJR Am J Roentgenol 2013;201:W437–W442. 12. Banerjee P, McLean CR. Femoroacetabular impingement: a review of diagnosis and management. Curr Rev Musculoskelet Med 2011;4:23–32. 13. Tannast M, Siebenrock KA, Anderson SE. Femoroacetabular impingement: radiographic diagnosis--what the radiologist should know. AJR Am J Roentgenol 2007;188:1540–1552. 14. Jamali AA, Mladenov K, Meyer DC, et al. Anteroposterior pelvic radiographs to assess acetabular retroversion: high validity of the "cross-over-sign". J Orthop Res 2007;25:758–765. 15. Nötzli HP, Wyss TF, Stoecklin CH, et al. The contour of the femoral head-neck junction as a predictor for the risk of anterior impingement. J Bone Joint Surg [Br] 2002;84-B:556–560. 16. Fujii M, Nakashima Y, Yamamoto T, et al. Acetabular retroversion in developmental dysplasia of the hip. J Bone Joint Surg [Am] 2010;92-A:895–903. 17. Siebenrock KA, Steppacher SD, Haefeli PC, Schwab JM, Tannast M. Valgus hip with high antetorsion causes pain through posterior extraarticular FAI. Clin Orthop Relat Res 2013;471:3774–3780. 18. Beck M, Leunig M, Parvizi J, et al. Anterior femoroacetabular impingement: part II. Midterm results of surgical treatment. Clin Orthop Relat Res 2004;418:67–73. 19. Kubiak-Langer M, Tannast M, Murphy SB, Siebenrock KA, Langlotz F. Range of motion in anterior femoroacetabular impingement. Clin Orthop Relat Res 2007;458:117–124. 20. Tannast M, Kubiak-Langer M, Langlotz F, et al. Noninvasive three-dimensional assessment of femoroacetabular impingement. J Orthop Res 2007;25:122–131. 21. Tannast M, Hanke M, Ecker TM, et al. LCPD: reduced range of motion resulting from extra- and intraarticular impingement. Clin Orthop Relat Res 2012;470:2431– 2440. 22. Nakahara I, Takao M, Sakai T, et al. Gender differences in 3D morphology and bony impingement of human hips. J Orthop Res 2011;29:333–339. 23. Crowe JF, Mani VJ, Ranawat CS. Total hip replacement in congenital dislocation and dysplasia of the hip. J Bone Joint Surg [Am] 1979;61-A:15–23. 24. Tönnis D. Normal values of the hip joint for the evaluation of X-rays in children and adults. Clin Orthop Relat Res 1976;119:39–47. 25. Lorensen W, Cline H. Marching cubes: a high resolution 3D surface construction algorithm. Computer Graphics 1987;21:163–170. 26. Schroeder W, Martin K, Lorensen W. The Visualization Toolkit: An Object Orient Approach to Computer Graphics. Second ed. New Jersey: Prentice Hall, 1997. 27. Jiménez P, Thomas F, Torras C. 3D collision detection: a survey. Comp Graph 2001;25:269–285. 28. Lohfert H, Schmelzeisen H. Biomechanics of the femoral neck. Calculation of pressure and tension distribution in the human femoral neck, applying principles of the theory of elasticity and strength of materials. Arch Orthop Trauma Surg 1980;96:31– 33. 29. Sugano N, Noble PC, Kamaric E. A comparison of alternative methods of measuring femoral anteversion. J Comput Assist Tomogr 1998;22:610–614. 30. Fujii M, Nakashima Y, Sato T, Akiyama M, Iwamoto Y. Pelvic deformity influences acetabular version and coverage in hip dysplasia. Clin Orthop Relat Res 2011;469:1735–1742. 31. Noble PC, Kamaric E, Sugano N, et al. Three-dimensional shape of the dysplastic femur: implications for THR. Clin Orthop Relat Res 2003;417:27–40. 32. Nishihara S, Sugano N, Nishii T, Ohzono K, Yoshikawa H. Measurements of pelvic flexion angle using three-dimensional computed tomography. Clin Orthop Relat Res 2003;411:140–151. 33. Catterall A, Pringle J, Byers PD, et al. A review of the morphology of Perthes' disease. J Bone Joint Surg [Br] 1982;64-B:269–275.
