Psychometric evaluation of spinal assessment methods to screen for scoliosis in children and adolescents with cerebral palsy

Children and adolescents with cerebral palsy (CP) have an increased risk of scoliosis [1]. The reported prevalence varies between 15–64 % based on age, severity of CP, and different definitions of scoliosis [1–3]. This stands in contrast to idiopathic scoliosis in adolescents where the prevalence has been reported at 2–4 % [4]. In children with CP the risk of developing scoliosis is related to the child’s gross motor function and age [1, 5]. Severe scoliosis is associated with pain, sitting problems, hip dislocation, and windswept deformity [1, 6], all of which may impair physical function and quality of life.

It is important to identify a progressive scoliosis early-on as the result of spinal surgery is related to the curve magnitude [7]. It is desirable to have a screening tool with high sensitivity but it is also important to have high specificity to avoid unnecessary radiographic examinations.

In 1994, a follow-up program and registry for children and adolescents with CP (CPUP) was initiated in the south of Sweden, an area of approximately 1.3 million inhabitants. CPUP has been classified as a Swedish National Health Care Quality Registry since 2005 and the program is also used in Norway, Denmark, Iceland, Scotland and New South Wales, Australia. Currently >95 % of all children with CP in Sweden participate in CPUP [8] and it is expanding to include also adults with CP.

The main purpose of CPUP is to prevent hip dislocation, contractures, scoliosis and windswept deformities in individuals with CP [8–11]. The program includes spinal examinations where the children undergo a standardized examination by their local physiotherapist twice a year until six years of age and then once a year. The spine is examined in forward bending and upright position with the child sitting on a plinth. In the event of scoliosis, it is graded as “mild”, “moderate” or “severe”. A child with a moderate or severe scoliosis is referred to radiographic examination. If the Cobb angle exceeds 40° operative treatment is considered.

A commonly used screening-tool for adolescent idiopathic scoliosis is the forward bending test that measures asymmetrical rib prominence [12, 13]. It has been argued that this test does not have a quantitative documentation and the efficacy of the test to screen for scoliosis is still discussed [12, 13].

The scoliometer [14] reliably measures the angle of trunk rotation and it is a commonly used tool to screen for adolescent idiopathic scoliosis [13, 15]. The recommended cut-off value to warrant a radiographic referral in adolescent idiopathic scoliosis varies but ≥7° has been suggested [15]. To our knowledge the scoliometer has not been used in screening for neuromuscular scoliosis.

The Cobb angle has been the gold standard to quantify scoliosis on radiographic examination since 1948 [16]. However, the Cobb angle is a two-dimensional analysis of a lateral deviation of the spine while the forward bending test and the scoliometer reflect a lateral deviation and rotation of a three dimensional deformity. Coehlo et al. found a correlation that was considered good (r > 0.7, p < 0.05) between scoliometer measurement and the Cobb angle in screening for adolescent idiopathic scoliosis [17].

For a screening tool to be useful in clinical practice a high sensitivity and a high specificity is important. When screening for scoliosis in CPUP the purpose is to identify all individuals requiring further radiographic examination and rule out those who do not in order to minimize the dose of radiation exposure.

The purposes of this study were to evaluate the interrater reliability of clinical examination and scoliometer measurement, and to evaluate their sensitivity, specificity and concurrent validity as screening tools by using radiographic examination with the Cobb angle as gold standard.

In CPUP, all participating children have their CP diagnosis verified by a neuropaediatrician at four years of age. CP is defined as a non-progressive brain injury which has developed before the age of two years. Motor impairment and specific neurological signs are defined and classified according to the inclusion criteria of the Surveillance of Cerebral palsy in Europe (SCPE) network [18, 19]. Gross motor function is determined by the child’s physiotherapist according to the expanded and revised version of the Gross Motor Function Classification System (GMFCS) [20, 21]. This is a 5-level system for children and adolescents with CP based on their self-initiated movement where level I delineates the highest level of function and level V the lowest.

Children and adolescents aged 6–16 years at GMFCS levels II-V and enrolled in CPUP were recruited from five child rehabilitation units in southern Sweden. The participants and their families were informed about the study by their local physiotherapists and provided with invitation letters with information about the study. Written consent was obtained from the parents/guardians of all participants. Children were recruited consecutively until at least six children at each relevant GMFCS level had accepted. The decision to include six persons in each GMFCS level (except level I) was based on an earlier study evaluating the Posture and Postural Ability Scale in adults with CP [22, 23]. In addition, a reliability study of the scoliometer by Bonagamba and colleagues included 24 participants and that study had enough power to satisfactorily evaluate reliability [24]. Children at GMFCS level I, which constitutes about 40 % of all children with CP, do not have a higher risk of scoliosis compared to the risk of developing idiopathic scoliosis in adolescents [1] and were therefore not included in this study.

In sitting position, a scoliometer was placed in forward bending at the top of the thoracic spine, with the 0 (zero) mark over the spinous process, and slowly moved down the spine noting the highest degree of truncal rotation. The degree of scoliosis was recorded separately and independently by the three examiners. A higher degree of truncal rotation indicates worse inclination. The value used to detect moderate scoliosis that should be referred to radiographic examination was set to ≥7°.

Radiographic examinations were performed in a sitting position, in an anteposterior (AP) projection. The magnitude of the curve was determined based on the Cobb angle [16] and moderate or severe scoliosis was defined as Cobb angle ≥20°. The radiographic examinations were performed at three radiology departments using standardized instructions for patient position and x-ray imaging. The Cobb angles were measured by three different radiologists with a special interest in skeletal radiology. The measurements were reevaluated and confirmed by a fourth independent examiner. None of the radiologists had information about the previous results of the clinical examinations or the scoliometer measurements.

We found both the clinical examination and the scoliometer measurement to have high interrater reliability. However, the clinical examination showed a higher specificity, sensitivity and a larger area under the curve compared to the scoliometer method. For both the clinical examination and the scoliometer, the negative and positive predictive values were the same as for specificity and sensitivity. The reason for this was that the outcome table was symmetrical on the diagonal with the same number of false positives and false negatives (Table 2). The predictive value could otherwise have been negatively influenced by the low prevalence of scoliosis. The informative value and the usefulness of the test were refined for the clinical assessment by analyzing the LR, where the results were in favor for the clinical examination compared to the scoliometer measurement.

A limitation of this study was the small number of children with moderate or severe scoliosis. Based on previous psychometric studies we calculated a sample size of six children at each GMFCS-level. Everyone involved were blinded to the spinal curves of the participants prior to the examinations. A higher prevalence of scoliosis graded as moderate or severe would most likely have resulted in a narrower confidence interval for the outcome measures. This could explain the wide CI for sensitivity for both assessment methods. However, the purpose was to evaluate screening methods used to identify scoliosis in a population of children with CP and to select those in need of further investigation. As such, especially the clinical examination seems useful in a clinical setting. The prevalence of scoliosis in this study is fairly representative for children with CP. The specificity of the clinical examination was high (95.8 %) thereby reducing unnecessary referrals for radiographic examination. The radiographic examinations were performed at three radiology departments and the Cobb angle measurements were done by three radiologists. To reduce measurement error the instructions for patient positioning, x-ray imaging were standardized and all Cobb angle measurements were confirmed through a reassessment by one orthopaedic surgeon.

There was no disagreement among the assessors regarding the rating of moderate or severe scoliosis. The higher kappa values for the clinical examination may partially be explained by the narrow range of the scale (0–3).

The cutoff point for the scoliometer measure was set to 7°. When screening, a balance has to be struck in terms of not referring too many or too few for a radiographic examination and this is related to the sensitivity and the specificity of the test. Bunnell [15] studied the outcome of spinal screening with scoliometer in adolescent idiopathic scoliosis and recommended 7° as an appropriate referral criterion. To use 7° as the referral criterion reduced the prognostic referral rate from 12 % to 3 % compared to if 5° would have been the criterion for referral. When creating guidelines for assessment of adolescent idiopathic scoliosis Coelho [17] et al. concluded that if a cutoff point of 5° for scoliometer measurement was used the sensitivity would be approximately 100 % and the specificity approximately 47 %. However, if 7° was used as the cut-off instead, the sensitivity dropped to 83 % while the specificity rose to 86 %. The results from Coelho and colleagues informed the choice of cut-off point in this study. The purpose of screening for adolescent idiopathic scoliosis is to detect scoliosis in time to start bracing, and thereby reducing the need for surgery. In neuromuscular scoliosis, an additional purpose of screening is to find a progressive scoliosis in time for surgery. It is also important to identify postural asymmetries that induce a worse sitting position with poor head control, uneven weight distribution, and pelvic obliquity which could increase the development of contractures, windswept position, and hip dislocation [22].

The clinical examination and the scoliometer measurement proved somewhat difficult when examining children who had problems bending forward in sitting because of decreased flexibility of spinal muscles, short hamstrings or limited hip flexion. In one person a baclofen pump prevented the child from bending forward properly. For these individuals a moderate or severe scoliosis is often apparent when sitting in an upright position. As a consequence, when the child is unable to bend forward, the examiner is only likely to miss a mild scoliosis.

In summary, this study showed an excellent interrater reliability for both the clinical spinal examination used in CPUP and for the scoliometer measurements. The sensitivity was higher for the clinical assessment compared to the scoliometer measurement, while the specificity was almost the same for both methods. There was a high validity correlated to the Cobb angle measurement. The findings should be interpreted cautiously until further research with a larger sample can verify these results. However, the clinical spinal examination used in CPUP seems to be an appropriate screening method for scoliosis in children with CP.