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Late-Onset Idiopathic Scoliosis in Children Six to Fourteen Years Old. A Cross-Sectional Prevalence Study*

ALASTAIR J. STIRLING, F.R.C.S., DENISE HOWEL, M.SC., PETER A. MILLNER, F.R.C.S.(ORTH), SAFA'A SADIQ, M.PHIL., DAVID SHARPLES, B.SC. and ROBERT A. DICKSON, D.SC., LEEDS, ENGLAND

Investigation performed at St. James's University Hospital, Leeds

	Abstract

Top Abstract Introduction Materials and Methods Results Discussion References

 
We performed a point-prevalence survey of 15,799 children, six to fourteen years old, who formed part of a prospective longitudinal study. Our purpose was to detect the prevalence of scoliosis and to investigate associated factors. On the basis of the initial screening, 934 children (5.9 per cent) were referred for additional clinical and radiographic examinations; 896 children returned for this second evaluation. A lateral spinal curve with a Cobb angle of more than 5 degrees was seen in 431 children (2.7 per cent of the 15,799 children). Only seventy-six children (0.5 per cent) had a curve that met our definition of idiopathic scoliosis (a curve of more than 10 degrees with concordant apical rotation). The point-prevalence rate was higher in girls, and it increased with age. The rate was 0.1 per cent (four of 5246) in the age-group of six to eight years, 0.3 per cent (sixteen of 5831) in the age-group of nine to eleven years, and 1.2 per cent (fifty-six of 4722) in the age-group of twelve to fourteen years old. With allowance for the fact that different definitions of idiopathic scoliosis have been used in earlier studies, our results suggest that the natural history of idiopathic scoliosis may be becoming more benign spontaneously.

	Introduction

Top Abstract Introduction Materials and Methods Results Discussion References

 
In many countries, children who are ten to fourteen years old are screened for scoliosis, but this has not yet been recommended in the United Kingdom^4,9,18,27. Screening of this age-group has been advocated on the supposition that a high prevalence of scoliosis is associated with the adolescent growth spurt^23,29. Many of the requirements for screening, according to the World Health Organization recommendations³⁷, remain unfulfilled for idiopathic scoliosis; in particular, knowledge of the natural history of the condition, including development from latent to declared disease, is still unclear. The interpretation of available screening data has been difficult, in part because the intervals of curve magnitude have differed in various surveys. The intervals in our report conform to the conventions of the Scoliosis Research Society, which defines structural scoliosis as a curve of at least 11 degrees³³.

We evaluated a cross section of children, six to fourteen years old, at a single point in time to determine age-specific point-prevalence rates. Our purpose was to record the development of scoliosis from a latent to a declared form, from the early juvenile period to adolescence.

	Materials and Methods

Top Abstract Introduction Materials and Methods Results Discussion References

 
A total of 15,799 children, six to fourteen years old, from sixty-two schools in the Leeds region were screened for spinal deformity. Our purpose was to identify a cohort to be used in a subsequent longitudinal five-year study of the natural history of adolescent idiopathic scoliosis. This age-range was selected to distinguish the cohort from patients who had infantile idiopathic scoliosis. The minimum age of six years was chosen because over the subsequent five years children of this age would be expected to reach the peripubertal stage when changes in spinal configuration, growth velocity, and the prevalence of scoliosis are maximum. In this study, the point-prevalence rates were derived only from measurements made at the initial visit; any changes noted at the subsequent visits are the subject of another investigation.

Rotational, sagittal-plane, and frontal-plane assessments were made by two research nurses who had been recruited from the Leeds Scoliosis Clinic and had been fully trained by the senior one of us (R. A. D.) in the examination for and the detection of spinal deformity. The children were instructed to bend forward, without clasping the hands together, and were examined from behind; this maneuver tends to amplify asymmetry of the trunk and has low specificity but high sensitivity for the detection of spinal deformity³⁰. Readings with a scoliometer were also obtained⁵. The child was referred to the Scoliosis Clinic for a second clinical and radiographic examination if there were physical signs of scoliosis (a rib or loin hump, asymmetrical waist triangles, a visible curve, elevation of the shoulder, or a prominent hip) or if the measurement obtained with the scoliometer was more than 4 degrees. Standardized posteroanterior and lateral radiographs of the spine were made with a technique that minimizes the dose of radiation to the developing thyroid and breast to less than 2 per cent of that associated with conventional radiography¹.

The deformity in the coronal plane was measured in 1-degree increments according to an adaptation³⁸ of the Cobb method⁷. With this modified method, a protractor with a free-hanging needle is used to indicate angular changes. The number of curves, the cephalad and caudad end vertebrae, and the apex of each curve were noted. The Perdriolle torsiometer²⁵ was used to measure axial spinal rotation, which was recorded in 5-degree increments. Rotation was concordant when the spinous processes pointed to the concavity of the curve and discordant when the spinous processes pointed to the convexity of the curve. Pelvic tilt was the angle between the cephalad border of the sacrum and a radiopaque plumb line drawn on a true posteroanterior radiograph in which the spinous processes were equidistant from the medial ends of each clavicle. All measurements were made by two of us (A. J. S. and R. A. D.), who came to a consensus. Intraobserver and interobserver variability in measurements of the Cobb angle have been reported to be as much as 4.9 and 7.2 degrees, respectively⁶; however, these variabilities cannot be extrapolated to our methodology, as our technique of measurement was different.

On the basis of the radiographic findings, the children were classified into one of five groups: straight spine—no visible deformity in the coronal or transverse plane and a curve of 5 degrees or less; questionable idiopathic scoliosis—a curve of 6 to 10 degrees with concordant rotation; idiopathic scoliosis—a curve of more than 10 degrees with concordant apical rotation; pelvic tilt—with the curve no more than twice the angle of pelvic tilt, the direction of which was toward the lower side of the pelvis²⁴; and non-classifiable curves—rotational artefacts, congenital curves, and curves that could not be classified into any of the other categories.

Statistical Methods
Prevalence rates and ratios as well as appropriate confidence levels were calculated for subgroups created according to age, the classification of the curve, and the size of the curve. Initially, a logistic regression model was used, with age as a continuous variable¹⁶; however, there were too few patients of each age, so the patients were grouped according to age in three-year increments. Although logistic regression naturally leads to estimates of odds ratios rather than to prevalence ratios, the values of the latter ratios are identical in a condition of such low prevalence. The ratio of the prevalence rate in girls to that in boys was calculated for each type of curve, and logistic regression was used to investigate whether this varied among the age-groups. The chi-square test was used to evaluate the association among the various factors, and confidence intervals were calculated for some of the differences between proportions.

	Results

Top Abstract Introduction Materials and Methods Results Discussion References

 
Of the 15,799 children, 934 (5.9 per cent) were referred to the Scoliosis Clinic for additional clinical and radiographic evaluation. The percentage of children who were referred increased with age for both boys and girls, and girls were more likely than boys to be referred. The rate of referral in the age-group of six to eight years was 3.9 per cent for girls and 2.6 per cent for boys; the corresponding rates were 5.7 and 4.7 per cent in the age-group of nine to eleven years and 12.5 and 7.4 per cent in the age-group of twelve to fourteen years. These rates are based on the numbers of boys and girls in the total population. Of the 7613 girls, 2517 were six to eight years old, 2856 were nine to eleven years old, and 2240 were twelve to fourteen years old. Of the 8186 boys, 2729 were six to eight years old, 2975 were nine to eleven years old, and 2482 were twelve to fourteen years old.

Thirty-eight (4 per cent) of the 934 children did not attend the Scoliosis Clinic. The over-all rate of attendance for all patients was 96 per cent (range, 93 per cent [girls between six and eight years old] to 99 per cent [girls between nine and eleven years old]). Grouping of the children according to age in three-year increments led to a very slight underestimation of the true prevalence in the screened population; however, we did not find it necessary to calculate adjusted rates as has been done in studies in which the non-attendance rate was much higher²⁸.

Of the 896 children who had an additional evaluation, 465 were found to have a straight spine. This was 2.9 per cent of the total number of children who were screened and represents the prevalence rate of asymmetry of the trunk. The over-all prevalence of curves of more than 5 degrees was 2.7 per cent (431 children). One hundred and sixty-nine children had idiopathic or questionable idiopathic scoliosis, and 262 had a pelvic tilt or a non-classifiable curve; six children who had a non-classifiable curve had congenital scoliosis. If only the children who had a measurable or questionable curve are included, the over-all prevalence of scoliosis was 1.1 per cent (169 of the 15,799 children). If only the idiopathic curves are considered, the over-all prevalence was 0.5 per cent (seventy-six of the 15,799) (Table I).

The proportion of left and right curves in the group of children who had idiopathic scoliosis was the same as that in the group who had questionable idiopathic scoliosis, with a tendency for thoracic and thoracolumbar curves to be right-sided and for lumbar curves to be left-sided (p = 0.02). This association was not as strong (p = 0.24) when only the idiopathic curves were considered. In the combined group of idiopathic and questionable idiopathic scoliosis, the 95 per cent confidence interval for the proportion of right-sided thoracic curves was 48 to 70 per cent; in the idiopathic scoliosis group, it was 50 to 80 per cent.

The distribution of the six possible curve patterns in the group of children who had idiopathic scoliosis differed from that in the group who had questionable idiopathic scoliosis (p = 0.009); the idiopathic curves more frequently had a right thoracic pattern, and the questionable idiopathic curves more often had a left lumbar pattern. Twenty-nine children who had idiopathic scoliosis had a right thoracic curve, compared with nineteen who had questionable idiopathic scoliosis (difference, 18 per cent; 95 per cent confidence interval for difference, 4 to 31 per cent). A left lumbar curve was seen in twenty children who had questionable idiopathic scoliosis and in only four who had idiopathic scoliosis (difference, 16 per cent; 95 per cent confidence interval for difference, 6 to 26 per cent).

The association between the site and the size of the curve was significant (p = 0.007) (Table IV). There was a tendency for large curves to be in the thoracic region, with a more equitable distribution of small curves in the three regions of the spine. Thus, 40 per cent of the smallest curves were in the thoracic region, compared with 69 per cent of the largest curves (difference, 29 per cent; 95 per cent confidence interval, 10 to 49 per cent).

	Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
The natural history of adolescent idiopathic scoliosis remains obscure and the role of screening, contentious. Moreover, inconsistencies in terminology and in the grouping of children according to age have made it difficult to find studies with comparable populations. The reported prevalence of scoliosis is highly dependent on the definition of scoliosis and the distribution of age and gender in the screened population. We analyzed a large population of six to fourteen-year-old children and have provided over-all prevalence rates for all curves with a Cobb angle of more than 5 degrees (all four groups), for curves of more than 5 degrees with concordant rotation (idiopathic scoliosis and questionable idiopathic scoliosis), and for curves of more than 10 degrees with concordant rotation (idiopathic scoliosis). Unfortunately, not all previous studies have used these definitions, and often different thresholds for the magnitude of the curve have been utilized.

Although curves associated with a pelvic tilt or a limb-length discrepancy often are not considered to be structural curves, the types of curves that were in our non-classifiable category may or may not have been included in previous investigations. In the current study, when congenital scoliotic curves were excluded, the remaining non-classifiable curves showed discordant rotation (the spinous processes were rotated into the convexity of the curve) or no rotation. These curves were postural and non-structural with no associated pelvic tilt and represented imperfect positioning for the radiograph, with the curve being nothing more than an oblique view of the normal thoracic kyphosis.

The Scoliosis Research Society criterion³³ of 11 degrees or more for the classification of a curve as scoliotic is entirely empirical and excludes a large group of otherwise non-classifiable curves that show clear evidence of being structural scoliosis. It is important to include curves that are smaller than this arbitrary minimum magnitude, particularly because most of these curves appear and then subsequently resolve. Our inclusion of the questionable idiopathic curves allowed comparison with the findings in earlier studies in which a smaller minimum magnitude has sometimes been used.

Our definition of idiopathic structural scoliosis includes concordant apical rotation. The vertebral rotation is more responsible for the clinical features of structural scoliosis, such as prominence of the rib or loin^2,26, than is the lateral curve. The sagittal component predisposes to mechanical instability and buckling of the spinal column^11,12. Despite the three-dimensional aspects of scoliosis, this problem of axial rotation has not been given due consideration, even qualitatively, and thus the concept of discordant rotation (postural or non-structural scoliosis) or concordant rotation (true structural scoliosis) has not been considered.

The use of the Cobb angle⁷ in the current definition of a scoliotic curve ensures the continuing arbitrary nature of interpretation, particularly among different observers. We advocate the addition of the criterion of more than 5 degrees of concordant rotation, as measured with the Perdriolle torsiometer²⁵, to the definition of structural scoliosis, in order to exclude minor postural rotations. Drerup^13,14 showed that vertebral rotation can be measured with an accuracy of approximately ±5 degrees with the Perdriolle method; mathematical modifications of the technique may improve the accuracy. Therefore, although an accurate and reproducible quantitative assessment of a small degree of vertebral rotation may be difficult, a limit of at least 5 degrees should allow qualitative discrimination between concordant and discordant rotation. The inclusion of concordant rotation in the definition of structural scoliosis may assist in the exclusion of postural and non-progressive curves and may make it possible to give less consideration to the Cobb angle, with its many recognized deficiencies¹⁰. Nonetheless, the Cobb angle is the popular measure of the size of the curve, despite large intraobserver and interobserver variations. The adaptation by Whittle and Evans³⁸, which we used, reduces the magnitude of error to less than 2 degrees.

A rotational artefact has not been included as a radiographic finding in most series. Avikainen and Vaherto³ studied the radiographs of ninety-nine women and found rotation in 86 per cent, although only 15 per cent had a scoliotic curve of more than 10 degrees and the maximum curve was 25 degrees. The direction of rotation was not documented, but there was evidence of rotation even in spines that had a Cobb angle of less than 3 degrees. Pelvic-tilt scoliosis has long been recognized as an artefact, but it has been defined clearly and the prevalence has been quantified only recently. In a screening study of 5303 children who were ten to fourteen years old, Walker and Dickson³⁶ found that 375 children (7.1 per cent) had a curve of 5 to 9 degrees. Of the 375 children, 138 (37 per cent) had scoliosis related to pelvic tilt, which was due to pelvic asymmetry in nineteen, a limb-length inequality in thirty-two, and both of these causes in eighty-seven.

The prevalence of thoracic curves increased with the size of the curve in both girls and boys. On the basis of our findings, we refute the popular consensus that curves in the thoracic region are nearly always right-sided. The calculated confidence intervals for the proportion of right thoracic curves suggested that this supposed predominance is a weak association, at least for the smaller curves seen in this study. When the non-idiopathic curves were excluded, the proportion of right thoracic curves increased with the magnitude of the curve and was higher in the group of children who had idiopathic scoliosis than in the group who had questionable idiopathic scoliosis. This trend indicates the vulnerability for progression of a scoliotic curve in this region of the spine. Furthermore, the effect of growth velocity^22,31 on progression of the curve was evidenced by the low prevalence rates of idiopathic and questionable idiopathic curves in boys who were less than twelve years old and in girls who were less than nine years old.

Bunnell⁵ evaluated 1065 children and suggested that, if a scoliometric reading of 5 degrees had been considered to be diagnostic for scoliosis, 3.6 per cent of the children would have been referred for further evaluation, 2.1 per cent would have been found to have had a true-positive result for a spinal curve of at least 20 degrees, 0.1 per cent would have been found to have had a false-negative result (a scoliometric reading of less than 5 degrees but a Cobb angle of at least 20 degrees), and 96.4 per cent would have been found to have had a true-negative result. In our study, a scoliometric reading of 4 degrees or more was considered to be positive; this ensures greater sensitivity (a low rate of false-negative findings) and specificity (a low rate of false-positive findings). We did not determine intraobserver or interobserver error because we were only identifying an at-risk cohort for further study.

Rogala et al.²⁹ reported a 4.5 per cent prevalence of idiopathic scoliotic curves of more than 5 degrees in 26,947 children who were twelve to fourteen years old; the prevalence was 3.4 per cent in another group of 3074 younger children (mean age, 11.7 years). This suggests that adolescent idiopathic scoliosis, at least in the latent form, is present in younger children. We compared the prevalence rates in our series with those in three studies^8,21,29 that were comparable with regard to age distribution but in which a less restrictive definition of scoliosis was used (Table V). The lowest and highest rates were found in the two studies from England (the present study and the study of Dickson⁸). Some of the differences can be explained by the slightly different definitions used, some were a result of the inclusion of six to nine-year-old children (an age when the condition is less common) in our study, and some may have been the result of a real decrease in the prevalence of scoliosis. In children who were ten to fourteen years old, the prevalence was 3.9 per cent when 5 degrees was used as the defining point and 0.8 per cent when 10 degrees was used⁸.

In the present study, the prevalence of a curve of greater than 5 degrees in the age-group of twelve to fourteen years was only five times that in the age-group of six to eight years. This finding demonstrates that idiopathic scoliosis is by no means a phenomenon seen exclusively in adolescents. In the 1950's, more than a third of the patients who were referred to a scoliosis clinic had infantile idiopathic scoliosis, and most of the curves were progressive¹⁵. In less than two decades, infantile idiopathic scoliosis had become rare, with more than 90 per cent of the curves resolving spontaneously¹⁹. Lonstein et al.²⁰ noted that, between 1971 and 1979, the mean age at which an operation was performed for scoliosis stayed relatively constant within a range of 13.75 to 14.5 years old; however, the mean size of the curve decreased from 60 to 42 degrees during this period of time. The absolute and relative numbers of children for whom management with a brace was considered necessary also decreased over this period. These changes often have been attributed to effective community-screening programs^20,35. This assumption may be erroneous, as the reduction in the average magnitude of the curve may well have been the result of curves of clinically unimportant sizes that would otherwise have been undetected being found through such screening programs¹⁷. It is clear, however, that if the average age at the time of operative intervention remains the same while the average size of the curve decreases, then the course of the condition must be becoming more benign spontaneously. The reasons for this radical change are open to conjecture. It may be that in some instances, a minor degree of spinal asymmetry, established in infancy, forms the template for the development of adolescent scoliosis with subsequent growth; this would account for the prevalence that is seen in six to eight-year-old children. It is interesting to note that, in infancy, the most progressive curve is one with a right thoracic pattern in a girl³⁴. A comparison of the low prevalence of scoliosis in the present study with that in a similar study from England⁸, reported on in 1983, suggests that adolescent idiopathic scoliosis is similar to infantile idiopathic scoliosis in that its natural history has become more benign. Longitudinal follow-up is continuing for the cohort in the present study. Such an extended analysis should be of great assistance in defining the natural history of the condition as, to our knowledge, no study to date has included a minimum five-year follow-up of patients who have a minor curve.

NOTE: The authors thank Mrs. Doris Followell and Mrs. Carol Garforth for their assistance with school screening and clinical follow-up, Mrs. Shirley Cook for administration of the study, and Paul Nicholson and Jon Duke of the Leeds University Computing Service for their help with data-processing.

	Footnotes

 
*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. Funds were received in total or partial support of the research or clinical study presented in this article. The funding sources were a grant from the Medical Research Council and an Action Research Fellowship grant (P. A. M.).

Level 5, Clinical Sciences Building, St. James's University Hospital, Leeds LS9 7TF, England.

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