ORIGINAL ARTICLE
Reliability of Radiologic Measures of Hip Displacement in a Cohort of Preschool-aged Children With Cerebral Palsy Alex Craven, MBBS (Hons), BSc (Medical Radiations),*w Aaron Pym, MBBS (Hons) BEcon,*w and Roslyn N. Boyd, PhD, MSc (Physiotherapy)*w
Background: Radiologic hip surveillance is recommended for children with cerebral palsy (CP) at risk of hip displacement. Young children with abnormal proximal femoral geometry (Hilgenreiner epiphyseal angle, HEA) may be more likely to develop hip displacement, less likely to respond to nonsurgical intervention, and may benefit from earlier surgical referral. The reliability of radiographic measures of migration percentage (MP) in the immature pelvis of young children has been reported in smaller retrospective studies; HEA has not been examined in this population. This prospective study describes the reliability of MP and HEA in very young children with CP. Methods: Participants were entered from tertiary referral center CP clinics into a prospectively recruited population-based cohort for hip surveillance with pelvic radiography using standardized patient position, at 18, 24, 30, 36, and 48 months. All Gross Motor Function Classification System (GMFCS) levels were included. Two independent raters assessed radiographs for HEA and MP. The intraclass correlation coefficient (ICC) was computed as a measure of interrater and intrarater reliability. The correlation coefficient between HEA and femoral position was computed. Results: Ninety-eight children less than 25 months (spasticity = 83, 85%; GMFCS IV-V = 38, 39%), and 114 children 25 to 48 months (spasticity = 96, 85%; GMFCS IV-V = 37, 32%) were included from 133 unique participants (spasticity = 111, 84%; GMFCS IV-V = 42, 32%). Of these 79 children were studied in both age groups. Overall interrater and intrarater reliability of MP was high [ICC = 0.93; 95% confidence interval (CI), 0.91-0.95]; SEM was 3.9% (single) and 5.5% (sequential). Perfect concordance for classification of marked hip displacement (MP > 30%) occurred in 217 cases (95.2%); nonweighted k = 0.80; 95% CI, 0.68-0.91. For HEA, overall reliability was high (ICC = 0.89; 95% CI, 0.85-0.93); SEM = 4.8% (single) and 6.7% (sequential). Correlation between changes in HEA and femoral abduction was poor (coefficient = 0.27, P = 0.244). From the *Queensland Cerebral Palsy and Rehabilitation Research Center, Royal Brisbane & Women’s Hospital; and wSchool of Medicine, The University of Queensland, Brisbane, Qld, Australia. This study was conducted within the Australian CP Child study, which is funded by a Grant from the Australian National Health and Medical Research Council (NHMRC) (465128). The authors declare no conflicts of interest. Reprints: Roslyn N. Boyd, PhD, MSc (Physiotherapy), Queensland Cerebral Palsy and Rehabilitation Research Centre, Royal Brisbane & Women’s Hospital, The University of Queensland, Block 7, Herston Road, Herston, Brisbane, Qld 4006, Australia. E-mail: [email protected]. Copyright r 2014 by Lippincott Williams & Wilkins
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Conclusions: MP and HEA can be reliably applied to very young children with CP, with high reliability for both measures. Measured HEA values appear to be independent of patient position, and may reflect genuine changes in proximal femoral geometry. A longitudinal study should be performed to determine the relationship between HEA and later hip outcomes. Level of Evidence: Level I/II—testing and development of diagnostic tests. Key Words: hip displacement, pediatrics, cerebral palsy (J Pediatr Orthop 2014;34:597–602)
H
ip displacement is the second most common musculoskeletal complication of CP, with an incidence of 15% to 35%.1,2 Mild hip displacement can progress to dislocation.3,4 Greater displacement has been linked to declining function and complete dislocation resulting in pain, contractures, arthritis, and walking difficulties.5,6 The exact pathogenesis remains unknown, but is probably a combination of abnormal tone in the musculature around the hip, bony abnormalities (persisting increased femoral anteversion from birth and later progressive dysplasia of the acetabulum), and lack of normal weight-bearing.7–11 Hip surveillance, including anterior-posterior (AP) pelvis x-ray, is recommended for children with CP to facilitate early detection and treatment of severe or progressive hip displacement.12,13 The migration percentage (MP) is widely accepted as the gold-standard measure in hip surveillance,7,12–15 measuring femoral head subluxation.16 Other measures include the acetabular index (AI), assessing acetabular dysplasia,17 and the femoral neck-shaft angle (NSA).18 As the pelvis and its radiographic appearance changes extensively between birth and skeletal maturity,19,20 early surveillance may be impacted by bony growth and ossification, particularly if measurements are based on landmarks that are difficult to identify or absent in the immature skeleton. The reliability of MP has been investigated in relatively small studies to date,14–16,21 and reliability data in very young children is infrequent.15 Hilgenreiner epiphyseal angle (HEA) is a radiographic measure previously applied to assessment of coxa valga,20,22 but may offer prognostic information for hips at risk in CP. It is the acute angle between a line drawn parallel to and through the proximal femoral epiphysis www.pedorthopaedics.com |
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and Hilgenreiner line (HL) (Fig. 1). In a retrospective study of typically developing children, HEA increased from 11 to 15 degrees at the age of 12 months and to 21 to 25 degrees at 10 years.20 In children with CP at risk of hip subluxation, a flatter (ie, lower) angle may suggest abnormal proximal femoral morphology; with growth from a more horizontal epiphysis, that femur may be more likely to develop atypical morphology (ie, greater MP and NSA). If true, low-HEA hips may be less likely to respond to nonoperative relief of deforming forces, and may be more likely to require orthopaedic surgical intervention. Measuring HEA may assist clinicians identify which children may benefit from earlier referral for orthopaedic assessment. The reliability of HEA has not been explored in young children with CP at risk of hip displacement, and the reliability of MP only reported in relatively small studies of this population. These measures require reference points that cross a joint, and may be vulnerable to patient position; hip adduction contracture and internal rotation could theoretically alter the relationships as observed in 2-dimensional AP radiographs. Reimers’ demonstrated that the effect of internal rotation on MP is probably negligible,16,21 but the effect of patient position on HEA has not been reported. It is hypothesized that if HEA is susceptible to variation due to patient position,
A
HL HEA
FE
B
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changes in HEA would correlate closely with changes in femoral position. If correlation is poor, then measured HEA may be insensitive to position and may be an accurate measure. Evaluations of interrater reliability (concordance) and intrarater reliability (test-retest) would demonstrate whether radiographic measurements of MP and HEA could be performed consistently in this group, and an exploration of the relationship between femoral position and HEA would determine whether it is impacted by patient position. The primary study aims were to evaluate the reliability and validity of HEA and MP measurements in young children with cerebral palsy (CP). Secondary objectives were to identify whether HEA varies with functional impairment or MP, and whether independent raters can consistently classify a hip as markedly displaced (MP > 30%) in this group.
METHODS Study Design This cross-sectional study was conducted within the Australian CP child study (Australian National Health and Medical Research Council 465128).23 This prospective, population-based cohort study monitors young children from diagnosis of CP at 18 months (corrected age) with motor outcomes at the age of 5 years. Children are referred by clinicians (pediatricians, family physicians, or allied health professionals) with a confirmed or provisional diagnosis of CP for assessment at specialist clinics within tertiary referral centers. These centers maintain large statewide catchment areas and are expert pediatric centers for the management of children with CP. Participating centers recruited a birth cohort of patients born between January 1, 2004 and December 31, 2005 (in Victoria) and January 1, 2006 and December 31, 2007 (in Queensland), achieving high ascertainment, recruiting up to 73% of the expected population with CP.24 Participants were followed up with regular clinics at defined time points (18, 24, 30, 36, 48, and 60 mo). Assessments included periodic hip surveillance with digital AP pelvic radiographs performed according to a standardized protocol at initial assessment, then at 36 and 48 to 60 months.
Study Participants HL HEA FE
FIGURE 1. Hilgenreiner epiphyseal angle (HEA) demonstrated with normal (A) and abnormal (B) values. FE indicates proximal femoral epiphysis; HL, Hilgenreiner line.
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Participants were included if they had a diagnosis of CP confirmed by a pediatrician, child neurologist, or pediatric child rehabilitation specialist. Participants were eligible for inclusion in this study if they had a diagnosis of CP and were born within the appropriate birth years. All motor types25 and Gross Motor Function Classification System (GMFCS)26 levels were included. Exclusion criteria were a subsequent diagnosis of other than CP, a coincidental diagnosis of congenital hip dysplasia, or refusal to undertake radiographic surveillance.
Data and Measurement Participant’s demographic, clinical, and radiologic characteristics were recorded. Three independent r
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pediatric-trained physiotherapists performed clinical assessments at recruitment and at subsequent surveillance clinics. Children were classified for GMFCS,26 motor type, and topographical distribution.25 Radiographs were assessed by 2 independent raters for MP,16 HEA,22 AI,17 and NSA,18 according to surveillance guidelines.27 Marked hip displacement was defined as MP > 30% in that hip. Radiographs were acquired according to a standardized protocol, with patients positioned supine with legs parallel and knees facing anteriorly, thus placing hips in neutral abduction/adduction and rotation. In case of hip flexion contracture or marked anterior pelvic tilt, the legs were raised to minimize lumbar lordosis and pelvic tilt. Radiographs were assessed for photographic quality, rotation, tilt, and absence of significant abduction or adduction of the hips (>10 degrees), as these elements may affect the accuracy of measurement of MP and other measures across the hip joint.28 The interrater and intrarater reliability was calculated for MP and classification of displacement (MP > 30%).29 The HEA was tested for both interrater and intrarater reliability for validation purposes using a random sample of 40 partcipants. Each radiologic measure was recorded by 2 independent raters using seperate hard copies of x-ray images, with a ruler, 0.5-mm pen and 6-inch individual-degree goniometer. They received the images again in a random order for repeat measurement at least 2 weeks after the initial measurements. Previous measurements and measurements by the other rater were hidden until all measurements were completed. All radiographs were assessed for adequete position, with changes to HEA and femoral position recorded. Femoral position relative to neutral was identified by an angle between a line through and parallel to the long axis of the femoral shaft and HL. An angle perpendicular to HL was recorded as 0 degree, with relative adduction recorded as a negative value, and relative abduction recorded as a positive value. For each hip, the HEA and femoral shaft angle were compared at 2 time points (24 and 48 mo).
Statistical Methods The intrarater and interrater reliability of continuous outcome measures (MP and HEA) were evaluated with the intraclass correlation coefficient (ICC) and
Reliability of Radiologic Measures of Hip Displacement in CP
95% confidence interval (95% CI)30 and the SEM, to estimate the error to be expected in single measurements and if measuring change over 2 time points. The interrater reliability of ordinal outcomes (diagnosis of MP > 30%) was determined with the percentage of concordance between raters, and Cohen unweighted k statistic.29 The relationship between HEA and femoral position was estimated by calculating a correlation coefficient. Analyses performed with SPSS version 17.0.0.
Ethical Approvals Institutional approvals were granted by the Royal Children’s Hospital (EHRC 25010C) and Monash Medical Center (05077C) (Victoria), and by Royal Children’s Hospital (HREC/07/QRCH/107) and Cerebral Palsy League of Queensland (CPLQ 2007/08-10010) (Queensland). Informed consent to participate was obtained by an independent member of the research team, who had no prior therapeutic relationship with patients or their families. Parents or guardians were counseled and offered written information. Radiographic hip surveillance was performed by a pediatric-trained radiographer and limited to a single projection. Lead shielding was applied over gonadal regions for most children.
RESULTS A total of 105 children were recruited before age 25 months. Of these, 5 were rediagnosed as other than CP and excluded, and 2 did not have radiographs of suitable quality for analysis (< 10 degrees abduction of either hip). A total of 118 children were recruited at the age of 25 to 48 months; 2 were excluded because they had already undergone bony surgery, and 2 were excluded due to unsuitable radiographs. The final group for analysis was 98 participants’ r24 months and 114 participants’ 25 to 48 months; 79 children were in both the groups. HEA was investigated with participants from the Queensland cohort only, and included 58 participants’ r24 months and 54 participants’ 25 to 48 months, with 38 children in both the groups. The characteristics of these groups are shown in Table 1. All GMFCS levels were included (I = 57, II = 14, III = 20, IV = 20, V = 22). The primary motor type was spasticity (n = 111, 83%) and primary involvement bilateral (n = 70, 64%). These patterns of
TABLE 1. Demographic and Clinical Characteristics of Participants
Age group r24 mo 25-48 mo All unique participants Queensland cohort only r24 mo 25-48 mo
Na
Males (%)
Age [Median (First-Third Quartile)]
MP [Mean (± SD)]
Spasticity (%)
Bilateral CP (%)
GMFCS (IV-V) (%)
98 114 133
65 (66) 72 (63) 85 (64)
23.5 (21.0-24.0) 35.8 (34.5-36.6) 35.6 (30.5-36.4)
18 (± 17) 19 (± 15) 19 (± 16)
83 (85) 96 (85) 111 (84)
54 (55) 62 (54) 70 (53)
38 (39) 37 (32) 42 (32)
58 54
34 (59) 30 (56)
21.9 (18.8-24.0) 35.3 (30.8-36.3)
17 (± 21) 22 (± 18)
50 (86) 45 (83)
32 (55) 30 (56)
22 (38) 19 (35)
a includes 74 participants assessed at both ages. CP indicates cerebral palsy; GMFCS, Gross Motor Function Classification System; MP, migration percentage.
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Right hips Left hips r24 mo 25-48 mo All cases
114 114 84 106 228
ICC (95% CI)
SD
SEM (Single)a
SEM (Change)b
0.92 0.94 0.94 0.90 0.93
13.9 15.4 19.8 11.0 14.6
3.9 3.8 4.9 3.5 3.9
5.6 5.3 6.9 4.9 5.5
(0.89–0.94) (0.91–958) (0.91–0.96) (0.86–0.93) (0.91–0.95)
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measure and 6.7 degrees for measuring change between 2 assessments. The correlation between HEA and femoral position was weak (correlation coefficient 0.27, NS), suggesting that changes to HEA are not simply due to changes in femoral position, as in hip adduction contracture. In both age groups, the values for HEA were lower in displaced hips (mean 9.0 degrees) than nondisplaced hips (mean 15.0 degrees) (Table 4). In each age group HEA was compared with MP and correlation between the 2 measures was tested. There was no significant difference in mean values for MP or the new measure between age groups. There was moderate negative correlation between MP and the new measure in the hips of participants aged 24 months and younger c.a. (r = 0.57) and those aged 25 to 48 months (r = 0.47).
TABLE 2. Interrater Reliability of Reimers’ Migration Percentage N
SEM for: single measurement (a) and change between 2 measures (b) (= O2 SEM). CI indicates confidence interval; ICC, intraclass correlation coefficient.
functional severity and motor type and distribution were consistent between age groups, and were consistent with the characteristics of the population from which they were recruited,24 and are representative of a populationbased sample. The reliability of MP was tested against 114 radiographs (228 hips) from 61 children (Table 2). Interrater reliability was high (ICC = 0.93) with a SEM of 3.9% for single measurements and 5.5% for measuring change between 2 assessments. There was no significant difference in interrater reliability according to side of hip or between age bands. The classification of hips as displaced (MP > 30%) was assessed against 2 raters using 228 radiographs. Interrater reliability was high with concordance in 217 cases (95.2%) with substantial agreement (nonweighted k = 0.80).29 There was no significant difference in the reliability according to side of hip or between age bands. The reliability of HEA was calculated from measurements performed on 40 children (80 hips) by 2 independent raters. Intrarater reliability was high for both raters, and interrater reliability was strong in both sessions (Table 3). There was negligible difference due to the side of hip or the age group of the participant. The combined intrarater and interrater reliability was high (ICC = 0.89), with a small SEM of 4.8 degrees for a single
DISCUSSION The major finding was that HEA is a valid and reliable measure in children with CP undergoing hip surveillance. Reimers’ MP also demonstrated excellent reliability in this young cohort, across age groups and gross motor functional levels. This is the largest investigation into the reliability of MP in a cohort of very young children with CP. Interrater and intrarater reliability for HEA was excellent. Unlike other common measures on AP pelvis x-ray (MP and AI),15 interrater reliability was not significantly lower than intrarater reliability; the use of multiple raters in future applications of this measure would be appropriate. Experienced raters found this as an easy measurement to make, except in rare instances when knees were raised significantly to counteract anterior pelvic tilt in children with fixed flexion deformity of the hips. The majority of participants could be adequately positioned. Across the cohort, changes in epiphyseal angles correlate poorly, if at all, with changes in femoral position, suggesting that measured epiphyseal angles reflect genuine changes in proximal femoral geometry and are not positional. The mean HEA was significantly lower in displaced hips than nondisplaced hips (Table 4).
TABLE 3. Reliability of Hilgenreiner Epiphyseal Angle N
SD
Intrarater reliability Rater 1 80 14.6 Rater 2 80 14.6 Interrater reliability Session 1 80 14.6 Session 2 80 14.6 Combined intrarater and interrater reliability Right hips 40 14.8 Left hips 40 14.4 r24 mo 40 14.8 25-48 mo 40 14.4 All cases 80 14.6
ICC (95% CI)
SEM (Single)a
SEM (Change)b
0.93 (0.89–0.95) 0.85 (0.78–0.90)
3.9 5.6
5.6 7.9
0.94 (0.91–0.96) 0.87 (0.81–0.92)
3.5 5.3
4.9 7.4
0.87 0.91 0.90 0.91 0.89
5.3 4.3 4.7 4.4 4.8
7.5 6.1 6.7 6.2 6.7
(0.80–0.92) (0.86–0.95) (0.84–0.94) (0.86–0.95) (0.85–0.93)
SEM for: a single measure (a) and change over 2 assessments (b) (= O2 SEM). CI indicates confidence interval; ICC, intraclass correlation coefficient..
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TABLE 4. Relationship Between Hilgenreiner Epiphyseal Angle, Migration Percentage (MP), and Marked Hip Displacement (MP > 30%) Age Group All participants r24 mo 25-48 mo Total (all participants) Displaced hips (MP > 30%) r24 mo 25-48 mo Total (displaced hips) Nondisplaced hips r24 mo 25-48 mo Total (nondisplaced hips)
Hips
MP [Mean (SD)]
HEA [Mean (SD)] (deg.)
Pearson Correlation
116 108 224
17.2 (19.5) 21.7 (18.1) 20.0 (18.7)
14.0 (6.5) 13.9 (7.1) 13.9 (6.8)
25 23 48
— — —
8.5 (5.3) 9.6 (6.7) 9.0 (6.0)
— — —
91 85 176
— — —
15.5 (6.0) 15.1 (6.7) 15.3 (6.4)
— — —
0.57 0.47 0.52
HEA indicates Hilgenreiner epiphyseal angle; MP, migration percentage.
There was moderate correlation with MP, which supported a relationship between the angle of the femoral epiphysis to the pelvis and the radiologic severity of hip displacement. The cohort characteristics (distribution of sex-bias, functional severity, and motor types) were consistent with other population cohorts of young children with CP31 and with surveillance register populations in Tasmania (Australia),28 Victoria (Australia),2 Sweden,32 Canada,33 and the United Kingdom.4 Clinically, these findings support radiologic surveillance with MP and HEA in very young children with CP. Independent raters can make consistent evaluations, and these children can be appropriately positioned for consistent radiography. As HEA appears to be a reliable measure of proximal femoral geometry and may be related to early hip status, a longitudinal investigation is required to evaluate the long-term outcomes of children with CP with abnormal epiphyseal angles. If this measure can discriminate between young patients most at risk of further hip displacement and/or requiring orthopaedic surgery, it may assist clinicians to decide which children would most be most likely to benefit from earlier intervention and referral for orthopaedic opinion.
Strengths and Limitations Study strengths include a representative populationbased cohort of children with CP, with large numbers of hips available for prospective assessment, and strong findings of reliability of the primary measures. The cohort achieved a good ascertainment rate and appears to be representative of such a population, closely matching characteristics reported in large population-based studies with regard to severity, motor type, and distribution of CP.4,28,32,33 As HEA is measured across the joint, relative to a baseline through the pelvis, measurements may be vulnerable to poor patient position. In the case of hip flexion contracture, flexion will cause the femur to not be parallel to the plane of the x-ray, and may cause the epiphysis to appear ellipsoid rather than as a clear line. In these cases, accurate marking of the plane of the proximal femoral r
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epiphysis may be less certain. In addition, the epiphyseal line is related to the position of the femur, and hip abduction or adduction would impact measured values. Across the cohort, the relationship between femoral position and HEA was poor, suggesting that the majority of children can either be brought to neutral for the purposes of their radiographs, or that the effect of adduction is negligible. Some children, however, may be unable to attain a standardized posture for accurate radiographic analysis. REFERENCES 1. Hagglund G, Andersson S, Duppe H, et al. Prevention of dislocation of the hip in children with cerebral palsy. The first ten years of a population-based prevention programme. J Bone Joint Surg Am. 2005;87:95–101. 2. Soo B, Howard J, Boyd R, et al. Hip displacement in cerebral palsy. J Bone Joint Surg Am. 2006;88:121–129. 3. Miller F, Bagg M. Age and migration percentage as risk factors for progression in spastic hip disease. Dev Med Child Neurol. 1995;37:449–455. 4. Scrutton D, Baird G, Smeeton N. Hip dysplasia in bilateral cerebral palsy: Incidence and natural history in children aged 18 months to 5 years. Dev Med Child Neurol. 2001;43:586–600. 5. Bagg M, Farber J, Miller F. Long-term follow-up of hip subluxation in cerebral palsy patients. J Pediatr Orthop. 1993;13:32–36. 6. Hoffer M, Stein G, Koffman M, et al. Femoral varus-derotation osteotomy in spastic cerebral palsy. J Bone Joint Surg Am. 1985;67:1229–1235. 7. Cornell M. The hip in cerebral palsy. Dev Med Child Neurol. 1995;37:3–18. 8. Morrell D, Pearson J, Sauser D. Progressive bone and joint abnormalities of the spine and lower extremities in cerebral palsy. Radiographics. 2002;22:257–268. 9. Bobroff E, Chambers H, Sartoris D, et al. Femoral anteversion and neck-shaft angle in children with cerebral palsy. Clin Orthop Relat Res. 1999;194–204. 10. Laplaza FJ, Root L, Tassanawipas A, et al. Femoral torsion and neck-shaft angles in cerebral palsy. J Pediatr Orthop. 1993;13: 192–199. 11. Samilson R, Rsou P, Aamoth G, et al. Dislocation and subluxation of the hip in cerebral palsy. Pathogenesis, natural history and management. J Bone Joint Surg Am. 1972;54:863–873. 12. Gordon G, Simkiss D. A systematic review of the evidence for hip surveillance in children with cerebral palsy. J Bone Joint Surg Br. 2006;88B:1492–1496.
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13. Wynter M, Gibson N, Kentish M, et al. The Consensus Statement on Hip Surveillance for Children with Cerebral Palsy: Australian Standards of Care. J Pediatr Rehabil Med. 2011;4:183–204. 14. Faraj S, Atherton W, Stott N. Inter- and intra-measurer error in the measurement of Reimer’s hip migration percentage. J Bone Joint Surg Br. 2004;86:434–437. 15. Cobeljic G, Bajin Z, Lesic A, et al. A radiographic and clinical comparison of two soft-tissue procedures for paralytic subluxation of the hip in cerebral palsy. Int Orthop. 2009;33:503–508. 16. Reimers J. The stability of the hip in children. A radiological study of the results of muscle surgery in cerebral palsy. Acta Orthop Scand Suppl. 1980;184:1–100. 17. Hilgenreiner H. Early diagnosis and early treatment of congenital dislocation of the hip. Med Klin. 1925;21:1385–1425. 18. Foroohar A, McCarthy J, Yucha D, et al. Head-shaft angle measurement in children with cerebral palsy. J Pediatr Orthop. 2009;29:248–250. 19. Tonnis D. Congenital Dysplasia and Dislocation of the Hip in Children and Adults. London: Springer-Verlag; 1987. 20. Birkenmaier C, Jorysz G, Volkmar J, et al. Normal development of the hip: a geometric analysis based on planimetric radiography. J Pediatr Orthop B. 2010;19:1–8. 21. Reimers J, Bialik V. Influence of femoral rotation on the radiological coverage of the femoral head in children. Pediatr Radiol. 1981;10:215–218. 22. Haike H, Breuckmann G, Schulze H. [Surgical treatment of so-called congenital hip dislocation]. Arch Orthop Unfallchir. 1969;66:277–285. 23. Boyd RN, Jordan R, Pareezer L, et al. Australian Cerebral Palsy Child Study: protocol of a prospective population based study of
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24. 25. 26. 27. 28. 29. 30. 31. 32. 33.
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motor and brain development of preschool aged children with cerebral palsy. BMC Neurology. 2013;13. Kentish M, Wynter M, Snape N, et al. Five-year outcome of statewide hip surveillance of children and adolescents with cerebral palsy. J Pediatr Rehabil Med. 2011;4:205–217. Sanger T, Delgado M, Gaebler-Spira D, et al. Classification and definition of disorders causing hypertonia in childhood. Pediatrics. 2003;111:389–397. Palisano R, Rosenbaum R, Walter S, et al. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol. 1996;39:214–223. Scrutton D, Baird G. Surveillance measures of the hips of children with bilateral cerebral palsy. Arch Dis Child. 1997;76:381–384. Connelly A, Flett P, Graham H, et al. Hip surveillance Tasmanian children with cerebral palsy. J Paediatr Child Health. 2009;45: 437–443. Viera A, Garrett J. Understanding interobserver agreement: the kappa statistic. Fam Med. 2005;37:360–363. Shoukri M. Measures of Interobserver Agreement. Boca Raton, FL: Chapman & Hall/CRC; 2004. Gorter J, Ketelaar M, Rosenbaum P, et al. Use of the GMFCS in infants with CP: the need for reclassification at age 2 years or older. Dev Med Child Neurol. 2009;51:46–52. Hagglund G, Lauge-Pedersen H, Wagner P. Characteristics of children with hip displacement in cerebral palsy. BMC Musculoskelet Disord. 2007;8:101–107. Gorter JW, Rosenbaum PL, Hanna SE, et al. Limb distribution, motor impairment and functional classification of cerebral palsy. Dev Med Child Neurol. 2004;46:461–467.
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Reliability of Radiologic Measures of Hip Displacement in a Cohort of Preschool-aged Children With Cerebral Palsy Alex Craven, MBBS (Hons), BSc (Medical Radiations),*w Aaron Pym, MBBS (Hons) BEcon,*w and Roslyn N. Boyd, PhD, MSc (Physiotherapy)*w
Background: Radiologic hip surveillance is recommended for children with cerebral palsy (CP) at risk of hip displacement. Young children with abnormal proximal femoral geometry (Hilgenreiner epiphyseal angle, HEA) may be more likely to develop hip displacement, less likely to respond to nonsurgical intervention, and may benefit from earlier surgical referral. The reliability of radiographic measures of migration percentage (MP) in the immature pelvis of young children has been reported in smaller retrospective studies; HEA has not been examined in this population. This prospective study describes the reliability of MP and HEA in very young children with CP. Methods: Participants were entered from tertiary referral center CP clinics into a prospectively recruited population-based cohort for hip surveillance with pelvic radiography using standardized patient position, at 18, 24, 30, 36, and 48 months. All Gross Motor Function Classification System (GMFCS) levels were included. Two independent raters assessed radiographs for HEA and MP. The intraclass correlation coefficient (ICC) was computed as a measure of interrater and intrarater reliability. The correlation coefficient between HEA and femoral position was computed. Results: Ninety-eight children less than 25 months (spasticity = 83, 85%; GMFCS IV-V = 38, 39%), and 114 children 25 to 48 months (spasticity = 96, 85%; GMFCS IV-V = 37, 32%) were included from 133 unique participants (spasticity = 111, 84%; GMFCS IV-V = 42, 32%). Of these 79 children were studied in both age groups. Overall interrater and intrarater reliability of MP was high [ICC = 0.93; 95% confidence interval (CI), 0.91-0.95]; SEM was 3.9% (single) and 5.5% (sequential). Perfect concordance for classification of marked hip displacement (MP > 30%) occurred in 217 cases (95.2%); nonweighted k = 0.80; 95% CI, 0.68-0.91. For HEA, overall reliability was high (ICC = 0.89; 95% CI, 0.85-0.93); SEM = 4.8% (single) and 6.7% (sequential). Correlation between changes in HEA and femoral abduction was poor (coefficient = 0.27, P = 0.244). From the *Queensland Cerebral Palsy and Rehabilitation Research Center, Royal Brisbane & Women’s Hospital; and wSchool of Medicine, The University of Queensland, Brisbane, Qld, Australia. This study was conducted within the Australian CP Child study, which is funded by a Grant from the Australian National Health and Medical Research Council (NHMRC) (465128). The authors declare no conflicts of interest. Reprints: Roslyn N. Boyd, PhD, MSc (Physiotherapy), Queensland Cerebral Palsy and Rehabilitation Research Centre, Royal Brisbane & Women’s Hospital, The University of Queensland, Block 7, Herston Road, Herston, Brisbane, Qld 4006, Australia. E-mail: [email protected]. Copyright r 2014 by Lippincott Williams & Wilkins
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Conclusions: MP and HEA can be reliably applied to very young children with CP, with high reliability for both measures. Measured HEA values appear to be independent of patient position, and may reflect genuine changes in proximal femoral geometry. A longitudinal study should be performed to determine the relationship between HEA and later hip outcomes. Level of Evidence: Level I/II—testing and development of diagnostic tests. Key Words: hip displacement, pediatrics, cerebral palsy (J Pediatr Orthop 2014;34:597–602)
H
ip displacement is the second most common musculoskeletal complication of CP, with an incidence of 15% to 35%.1,2 Mild hip displacement can progress to dislocation.3,4 Greater displacement has been linked to declining function and complete dislocation resulting in pain, contractures, arthritis, and walking difficulties.5,6 The exact pathogenesis remains unknown, but is probably a combination of abnormal tone in the musculature around the hip, bony abnormalities (persisting increased femoral anteversion from birth and later progressive dysplasia of the acetabulum), and lack of normal weight-bearing.7–11 Hip surveillance, including anterior-posterior (AP) pelvis x-ray, is recommended for children with CP to facilitate early detection and treatment of severe or progressive hip displacement.12,13 The migration percentage (MP) is widely accepted as the gold-standard measure in hip surveillance,7,12–15 measuring femoral head subluxation.16 Other measures include the acetabular index (AI), assessing acetabular dysplasia,17 and the femoral neck-shaft angle (NSA).18 As the pelvis and its radiographic appearance changes extensively between birth and skeletal maturity,19,20 early surveillance may be impacted by bony growth and ossification, particularly if measurements are based on landmarks that are difficult to identify or absent in the immature skeleton. The reliability of MP has been investigated in relatively small studies to date,14–16,21 and reliability data in very young children is infrequent.15 Hilgenreiner epiphyseal angle (HEA) is a radiographic measure previously applied to assessment of coxa valga,20,22 but may offer prognostic information for hips at risk in CP. It is the acute angle between a line drawn parallel to and through the proximal femoral epiphysis www.pedorthopaedics.com |
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and Hilgenreiner line (HL) (Fig. 1). In a retrospective study of typically developing children, HEA increased from 11 to 15 degrees at the age of 12 months and to 21 to 25 degrees at 10 years.20 In children with CP at risk of hip subluxation, a flatter (ie, lower) angle may suggest abnormal proximal femoral morphology; with growth from a more horizontal epiphysis, that femur may be more likely to develop atypical morphology (ie, greater MP and NSA). If true, low-HEA hips may be less likely to respond to nonoperative relief of deforming forces, and may be more likely to require orthopaedic surgical intervention. Measuring HEA may assist clinicians identify which children may benefit from earlier referral for orthopaedic assessment. The reliability of HEA has not been explored in young children with CP at risk of hip displacement, and the reliability of MP only reported in relatively small studies of this population. These measures require reference points that cross a joint, and may be vulnerable to patient position; hip adduction contracture and internal rotation could theoretically alter the relationships as observed in 2-dimensional AP radiographs. Reimers’ demonstrated that the effect of internal rotation on MP is probably negligible,16,21 but the effect of patient position on HEA has not been reported. It is hypothesized that if HEA is susceptible to variation due to patient position,
A
HL HEA
FE
B
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changes in HEA would correlate closely with changes in femoral position. If correlation is poor, then measured HEA may be insensitive to position and may be an accurate measure. Evaluations of interrater reliability (concordance) and intrarater reliability (test-retest) would demonstrate whether radiographic measurements of MP and HEA could be performed consistently in this group, and an exploration of the relationship between femoral position and HEA would determine whether it is impacted by patient position. The primary study aims were to evaluate the reliability and validity of HEA and MP measurements in young children with cerebral palsy (CP). Secondary objectives were to identify whether HEA varies with functional impairment or MP, and whether independent raters can consistently classify a hip as markedly displaced (MP > 30%) in this group.
METHODS Study Design This cross-sectional study was conducted within the Australian CP child study (Australian National Health and Medical Research Council 465128).23 This prospective, population-based cohort study monitors young children from diagnosis of CP at 18 months (corrected age) with motor outcomes at the age of 5 years. Children are referred by clinicians (pediatricians, family physicians, or allied health professionals) with a confirmed or provisional diagnosis of CP for assessment at specialist clinics within tertiary referral centers. These centers maintain large statewide catchment areas and are expert pediatric centers for the management of children with CP. Participating centers recruited a birth cohort of patients born between January 1, 2004 and December 31, 2005 (in Victoria) and January 1, 2006 and December 31, 2007 (in Queensland), achieving high ascertainment, recruiting up to 73% of the expected population with CP.24 Participants were followed up with regular clinics at defined time points (18, 24, 30, 36, 48, and 60 mo). Assessments included periodic hip surveillance with digital AP pelvic radiographs performed according to a standardized protocol at initial assessment, then at 36 and 48 to 60 months.
Study Participants HL HEA FE
FIGURE 1. Hilgenreiner epiphyseal angle (HEA) demonstrated with normal (A) and abnormal (B) values. FE indicates proximal femoral epiphysis; HL, Hilgenreiner line.
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Participants were included if they had a diagnosis of CP confirmed by a pediatrician, child neurologist, or pediatric child rehabilitation specialist. Participants were eligible for inclusion in this study if they had a diagnosis of CP and were born within the appropriate birth years. All motor types25 and Gross Motor Function Classification System (GMFCS)26 levels were included. Exclusion criteria were a subsequent diagnosis of other than CP, a coincidental diagnosis of congenital hip dysplasia, or refusal to undertake radiographic surveillance.
Data and Measurement Participant’s demographic, clinical, and radiologic characteristics were recorded. Three independent r
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pediatric-trained physiotherapists performed clinical assessments at recruitment and at subsequent surveillance clinics. Children were classified for GMFCS,26 motor type, and topographical distribution.25 Radiographs were assessed by 2 independent raters for MP,16 HEA,22 AI,17 and NSA,18 according to surveillance guidelines.27 Marked hip displacement was defined as MP > 30% in that hip. Radiographs were acquired according to a standardized protocol, with patients positioned supine with legs parallel and knees facing anteriorly, thus placing hips in neutral abduction/adduction and rotation. In case of hip flexion contracture or marked anterior pelvic tilt, the legs were raised to minimize lumbar lordosis and pelvic tilt. Radiographs were assessed for photographic quality, rotation, tilt, and absence of significant abduction or adduction of the hips (>10 degrees), as these elements may affect the accuracy of measurement of MP and other measures across the hip joint.28 The interrater and intrarater reliability was calculated for MP and classification of displacement (MP > 30%).29 The HEA was tested for both interrater and intrarater reliability for validation purposes using a random sample of 40 partcipants. Each radiologic measure was recorded by 2 independent raters using seperate hard copies of x-ray images, with a ruler, 0.5-mm pen and 6-inch individual-degree goniometer. They received the images again in a random order for repeat measurement at least 2 weeks after the initial measurements. Previous measurements and measurements by the other rater were hidden until all measurements were completed. All radiographs were assessed for adequete position, with changes to HEA and femoral position recorded. Femoral position relative to neutral was identified by an angle between a line through and parallel to the long axis of the femoral shaft and HL. An angle perpendicular to HL was recorded as 0 degree, with relative adduction recorded as a negative value, and relative abduction recorded as a positive value. For each hip, the HEA and femoral shaft angle were compared at 2 time points (24 and 48 mo).
Statistical Methods The intrarater and interrater reliability of continuous outcome measures (MP and HEA) were evaluated with the intraclass correlation coefficient (ICC) and
Reliability of Radiologic Measures of Hip Displacement in CP
95% confidence interval (95% CI)30 and the SEM, to estimate the error to be expected in single measurements and if measuring change over 2 time points. The interrater reliability of ordinal outcomes (diagnosis of MP > 30%) was determined with the percentage of concordance between raters, and Cohen unweighted k statistic.29 The relationship between HEA and femoral position was estimated by calculating a correlation coefficient. Analyses performed with SPSS version 17.0.0.
Ethical Approvals Institutional approvals were granted by the Royal Children’s Hospital (EHRC 25010C) and Monash Medical Center (05077C) (Victoria), and by Royal Children’s Hospital (HREC/07/QRCH/107) and Cerebral Palsy League of Queensland (CPLQ 2007/08-10010) (Queensland). Informed consent to participate was obtained by an independent member of the research team, who had no prior therapeutic relationship with patients or their families. Parents or guardians were counseled and offered written information. Radiographic hip surveillance was performed by a pediatric-trained radiographer and limited to a single projection. Lead shielding was applied over gonadal regions for most children.
RESULTS A total of 105 children were recruited before age 25 months. Of these, 5 were rediagnosed as other than CP and excluded, and 2 did not have radiographs of suitable quality for analysis (< 10 degrees abduction of either hip). A total of 118 children were recruited at the age of 25 to 48 months; 2 were excluded because they had already undergone bony surgery, and 2 were excluded due to unsuitable radiographs. The final group for analysis was 98 participants’ r24 months and 114 participants’ 25 to 48 months; 79 children were in both the groups. HEA was investigated with participants from the Queensland cohort only, and included 58 participants’ r24 months and 54 participants’ 25 to 48 months, with 38 children in both the groups. The characteristics of these groups are shown in Table 1. All GMFCS levels were included (I = 57, II = 14, III = 20, IV = 20, V = 22). The primary motor type was spasticity (n = 111, 83%) and primary involvement bilateral (n = 70, 64%). These patterns of
TABLE 1. Demographic and Clinical Characteristics of Participants
Age group r24 mo 25-48 mo All unique participants Queensland cohort only r24 mo 25-48 mo
Na
Males (%)
Age [Median (First-Third Quartile)]
MP [Mean (± SD)]
Spasticity (%)
Bilateral CP (%)
GMFCS (IV-V) (%)
98 114 133
65 (66) 72 (63) 85 (64)
23.5 (21.0-24.0) 35.8 (34.5-36.6) 35.6 (30.5-36.4)
18 (± 17) 19 (± 15) 19 (± 16)
83 (85) 96 (85) 111 (84)
54 (55) 62 (54) 70 (53)
38 (39) 37 (32) 42 (32)
58 54
34 (59) 30 (56)
21.9 (18.8-24.0) 35.3 (30.8-36.3)
17 (± 21) 22 (± 18)
50 (86) 45 (83)
32 (55) 30 (56)
22 (38) 19 (35)
a includes 74 participants assessed at both ages. CP indicates cerebral palsy; GMFCS, Gross Motor Function Classification System; MP, migration percentage.
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Right hips Left hips r24 mo 25-48 mo All cases
114 114 84 106 228
ICC (95% CI)
SD
SEM (Single)a
SEM (Change)b
0.92 0.94 0.94 0.90 0.93
13.9 15.4 19.8 11.0 14.6
3.9 3.8 4.9 3.5 3.9
5.6 5.3 6.9 4.9 5.5
(0.89–0.94) (0.91–958) (0.91–0.96) (0.86–0.93) (0.91–0.95)
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measure and 6.7 degrees for measuring change between 2 assessments. The correlation between HEA and femoral position was weak (correlation coefficient 0.27, NS), suggesting that changes to HEA are not simply due to changes in femoral position, as in hip adduction contracture. In both age groups, the values for HEA were lower in displaced hips (mean 9.0 degrees) than nondisplaced hips (mean 15.0 degrees) (Table 4). In each age group HEA was compared with MP and correlation between the 2 measures was tested. There was no significant difference in mean values for MP or the new measure between age groups. There was moderate negative correlation between MP and the new measure in the hips of participants aged 24 months and younger c.a. (r = 0.57) and those aged 25 to 48 months (r = 0.47).
TABLE 2. Interrater Reliability of Reimers’ Migration Percentage N
SEM for: single measurement (a) and change between 2 measures (b) (= O2 SEM). CI indicates confidence interval; ICC, intraclass correlation coefficient.
functional severity and motor type and distribution were consistent between age groups, and were consistent with the characteristics of the population from which they were recruited,24 and are representative of a populationbased sample. The reliability of MP was tested against 114 radiographs (228 hips) from 61 children (Table 2). Interrater reliability was high (ICC = 0.93) with a SEM of 3.9% for single measurements and 5.5% for measuring change between 2 assessments. There was no significant difference in interrater reliability according to side of hip or between age bands. The classification of hips as displaced (MP > 30%) was assessed against 2 raters using 228 radiographs. Interrater reliability was high with concordance in 217 cases (95.2%) with substantial agreement (nonweighted k = 0.80).29 There was no significant difference in the reliability according to side of hip or between age bands. The reliability of HEA was calculated from measurements performed on 40 children (80 hips) by 2 independent raters. Intrarater reliability was high for both raters, and interrater reliability was strong in both sessions (Table 3). There was negligible difference due to the side of hip or the age group of the participant. The combined intrarater and interrater reliability was high (ICC = 0.89), with a small SEM of 4.8 degrees for a single
DISCUSSION The major finding was that HEA is a valid and reliable measure in children with CP undergoing hip surveillance. Reimers’ MP also demonstrated excellent reliability in this young cohort, across age groups and gross motor functional levels. This is the largest investigation into the reliability of MP in a cohort of very young children with CP. Interrater and intrarater reliability for HEA was excellent. Unlike other common measures on AP pelvis x-ray (MP and AI),15 interrater reliability was not significantly lower than intrarater reliability; the use of multiple raters in future applications of this measure would be appropriate. Experienced raters found this as an easy measurement to make, except in rare instances when knees were raised significantly to counteract anterior pelvic tilt in children with fixed flexion deformity of the hips. The majority of participants could be adequately positioned. Across the cohort, changes in epiphyseal angles correlate poorly, if at all, with changes in femoral position, suggesting that measured epiphyseal angles reflect genuine changes in proximal femoral geometry and are not positional. The mean HEA was significantly lower in displaced hips than nondisplaced hips (Table 4).
TABLE 3. Reliability of Hilgenreiner Epiphyseal Angle N
SD
Intrarater reliability Rater 1 80 14.6 Rater 2 80 14.6 Interrater reliability Session 1 80 14.6 Session 2 80 14.6 Combined intrarater and interrater reliability Right hips 40 14.8 Left hips 40 14.4 r24 mo 40 14.8 25-48 mo 40 14.4 All cases 80 14.6
ICC (95% CI)
SEM (Single)a
SEM (Change)b
0.93 (0.89–0.95) 0.85 (0.78–0.90)
3.9 5.6
5.6 7.9
0.94 (0.91–0.96) 0.87 (0.81–0.92)
3.5 5.3
4.9 7.4
0.87 0.91 0.90 0.91 0.89
5.3 4.3 4.7 4.4 4.8
7.5 6.1 6.7 6.2 6.7
(0.80–0.92) (0.86–0.95) (0.84–0.94) (0.86–0.95) (0.85–0.93)
SEM for: a single measure (a) and change over 2 assessments (b) (= O2 SEM). CI indicates confidence interval; ICC, intraclass correlation coefficient..
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TABLE 4. Relationship Between Hilgenreiner Epiphyseal Angle, Migration Percentage (MP), and Marked Hip Displacement (MP > 30%) Age Group All participants r24 mo 25-48 mo Total (all participants) Displaced hips (MP > 30%) r24 mo 25-48 mo Total (displaced hips) Nondisplaced hips r24 mo 25-48 mo Total (nondisplaced hips)
Hips
MP [Mean (SD)]
HEA [Mean (SD)] (deg.)
Pearson Correlation
116 108 224
17.2 (19.5) 21.7 (18.1) 20.0 (18.7)
14.0 (6.5) 13.9 (7.1) 13.9 (6.8)
25 23 48
— — —
8.5 (5.3) 9.6 (6.7) 9.0 (6.0)
— — —
91 85 176
— — —
15.5 (6.0) 15.1 (6.7) 15.3 (6.4)
— — —
0.57 0.47 0.52
HEA indicates Hilgenreiner epiphyseal angle; MP, migration percentage.
There was moderate correlation with MP, which supported a relationship between the angle of the femoral epiphysis to the pelvis and the radiologic severity of hip displacement. The cohort characteristics (distribution of sex-bias, functional severity, and motor types) were consistent with other population cohorts of young children with CP31 and with surveillance register populations in Tasmania (Australia),28 Victoria (Australia),2 Sweden,32 Canada,33 and the United Kingdom.4 Clinically, these findings support radiologic surveillance with MP and HEA in very young children with CP. Independent raters can make consistent evaluations, and these children can be appropriately positioned for consistent radiography. As HEA appears to be a reliable measure of proximal femoral geometry and may be related to early hip status, a longitudinal investigation is required to evaluate the long-term outcomes of children with CP with abnormal epiphyseal angles. If this measure can discriminate between young patients most at risk of further hip displacement and/or requiring orthopaedic surgery, it may assist clinicians to decide which children would most be most likely to benefit from earlier intervention and referral for orthopaedic opinion.
Strengths and Limitations Study strengths include a representative populationbased cohort of children with CP, with large numbers of hips available for prospective assessment, and strong findings of reliability of the primary measures. The cohort achieved a good ascertainment rate and appears to be representative of such a population, closely matching characteristics reported in large population-based studies with regard to severity, motor type, and distribution of CP.4,28,32,33 As HEA is measured across the joint, relative to a baseline through the pelvis, measurements may be vulnerable to poor patient position. In the case of hip flexion contracture, flexion will cause the femur to not be parallel to the plane of the x-ray, and may cause the epiphysis to appear ellipsoid rather than as a clear line. In these cases, accurate marking of the plane of the proximal femoral r
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epiphysis may be less certain. In addition, the epiphyseal line is related to the position of the femur, and hip abduction or adduction would impact measured values. Across the cohort, the relationship between femoral position and HEA was poor, suggesting that the majority of children can either be brought to neutral for the purposes of their radiographs, or that the effect of adduction is negligible. Some children, however, may be unable to attain a standardized posture for accurate radiographic analysis. REFERENCES 1. Hagglund G, Andersson S, Duppe H, et al. Prevention of dislocation of the hip in children with cerebral palsy. The first ten years of a population-based prevention programme. J Bone Joint Surg Am. 2005;87:95–101. 2. Soo B, Howard J, Boyd R, et al. Hip displacement in cerebral palsy. J Bone Joint Surg Am. 2006;88:121–129. 3. Miller F, Bagg M. Age and migration percentage as risk factors for progression in spastic hip disease. Dev Med Child Neurol. 1995;37:449–455. 4. Scrutton D, Baird G, Smeeton N. Hip dysplasia in bilateral cerebral palsy: Incidence and natural history in children aged 18 months to 5 years. Dev Med Child Neurol. 2001;43:586–600. 5. Bagg M, Farber J, Miller F. Long-term follow-up of hip subluxation in cerebral palsy patients. J Pediatr Orthop. 1993;13:32–36. 6. Hoffer M, Stein G, Koffman M, et al. Femoral varus-derotation osteotomy in spastic cerebral palsy. J Bone Joint Surg Am. 1985;67:1229–1235. 7. Cornell M. The hip in cerebral palsy. Dev Med Child Neurol. 1995;37:3–18. 8. Morrell D, Pearson J, Sauser D. Progressive bone and joint abnormalities of the spine and lower extremities in cerebral palsy. Radiographics. 2002;22:257–268. 9. Bobroff E, Chambers H, Sartoris D, et al. Femoral anteversion and neck-shaft angle in children with cerebral palsy. Clin Orthop Relat Res. 1999;194–204. 10. Laplaza FJ, Root L, Tassanawipas A, et al. Femoral torsion and neck-shaft angles in cerebral palsy. J Pediatr Orthop. 1993;13: 192–199. 11. Samilson R, Rsou P, Aamoth G, et al. Dislocation and subluxation of the hip in cerebral palsy. Pathogenesis, natural history and management. J Bone Joint Surg Am. 1972;54:863–873. 12. Gordon G, Simkiss D. A systematic review of the evidence for hip surveillance in children with cerebral palsy. J Bone Joint Surg Br. 2006;88B:1492–1496.
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13. Wynter M, Gibson N, Kentish M, et al. The Consensus Statement on Hip Surveillance for Children with Cerebral Palsy: Australian Standards of Care. J Pediatr Rehabil Med. 2011;4:183–204. 14. Faraj S, Atherton W, Stott N. Inter- and intra-measurer error in the measurement of Reimer’s hip migration percentage. J Bone Joint Surg Br. 2004;86:434–437. 15. Cobeljic G, Bajin Z, Lesic A, et al. A radiographic and clinical comparison of two soft-tissue procedures for paralytic subluxation of the hip in cerebral palsy. Int Orthop. 2009;33:503–508. 16. Reimers J. The stability of the hip in children. A radiological study of the results of muscle surgery in cerebral palsy. Acta Orthop Scand Suppl. 1980;184:1–100. 17. Hilgenreiner H. Early diagnosis and early treatment of congenital dislocation of the hip. Med Klin. 1925;21:1385–1425. 18. Foroohar A, McCarthy J, Yucha D, et al. Head-shaft angle measurement in children with cerebral palsy. J Pediatr Orthop. 2009;29:248–250. 19. Tonnis D. Congenital Dysplasia and Dislocation of the Hip in Children and Adults. London: Springer-Verlag; 1987. 20. Birkenmaier C, Jorysz G, Volkmar J, et al. Normal development of the hip: a geometric analysis based on planimetric radiography. J Pediatr Orthop B. 2010;19:1–8. 21. Reimers J, Bialik V. Influence of femoral rotation on the radiological coverage of the femoral head in children. Pediatr Radiol. 1981;10:215–218. 22. Haike H, Breuckmann G, Schulze H. [Surgical treatment of so-called congenital hip dislocation]. Arch Orthop Unfallchir. 1969;66:277–285. 23. Boyd RN, Jordan R, Pareezer L, et al. Australian Cerebral Palsy Child Study: protocol of a prospective population based study of
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motor and brain development of preschool aged children with cerebral palsy. BMC Neurology. 2013;13. Kentish M, Wynter M, Snape N, et al. Five-year outcome of statewide hip surveillance of children and adolescents with cerebral palsy. J Pediatr Rehabil Med. 2011;4:205–217. Sanger T, Delgado M, Gaebler-Spira D, et al. Classification and definition of disorders causing hypertonia in childhood. Pediatrics. 2003;111:389–397. Palisano R, Rosenbaum R, Walter S, et al. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol. 1996;39:214–223. Scrutton D, Baird G. Surveillance measures of the hips of children with bilateral cerebral palsy. Arch Dis Child. 1997;76:381–384. Connelly A, Flett P, Graham H, et al. Hip surveillance Tasmanian children with cerebral palsy. J Paediatr Child Health. 2009;45: 437–443. Viera A, Garrett J. Understanding interobserver agreement: the kappa statistic. Fam Med. 2005;37:360–363. Shoukri M. Measures of Interobserver Agreement. Boca Raton, FL: Chapman & Hall/CRC; 2004. Gorter J, Ketelaar M, Rosenbaum P, et al. Use of the GMFCS in infants with CP: the need for reclassification at age 2 years or older. Dev Med Child Neurol. 2009;51:46–52. Hagglund G, Lauge-Pedersen H, Wagner P. Characteristics of children with hip displacement in cerebral palsy. BMC Musculoskelet Disord. 2007;8:101–107. Gorter JW, Rosenbaum PL, Hanna SE, et al. Limb distribution, motor impairment and functional classification of cerebral palsy. Dev Med Child Neurol. 2004;46:461–467.
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