Clinieal Anatomy 5:272-288 (1992)

Segmental Patterns of Rib-Vertebra Angles in Chest Radiographs of Children:

Changes Related to Rib Level , Age , Sex, Side and Significance for Scoliosis

THEODOROS B. GRIVAS, R.G. BURWELL, M. PURDUE, J.K. WEBB, AND A. MOULTON

Scoliosis Clinic (T.B .G.) and Department of Orthopaedic S urgery (J.K. W., A.M.), Har/(fW Wood Orthopaedic Hospital, Mansfield , N ottinghamshire and Departments of Human Morphology and Orthopaedics, Nottingham Health Authority, Queen's Medical Centre, University of N ottingham

(R.G.B .); X-Ray Department, University Hosp ital (M.P.), Nottingham, England

Rib-vertebra angles (RVAs) were measured (T1-12) on the chest radiographs of 412 children aged 0-17 years attending the hospital with minimal disorders or diseases (boys 193, girls 219) . A new method for measuring RVAs is used and the asymmetry of rib-vertebra angles is calculated as rib-vertebra angle differences (RVADs). The data are analysed in three age groups-infancy, childhood, and puberty, after the classification of Karlberg (1989) .

The findings show the following : 1) RVAs decrease from T1-12, especially so between T8 and T12 . 2) Between infancy and childhood, RVAs of the upper ribs increase , more so in boys than girls . 3) Between childhood and adoles­cence there is a further elevation of ribs , involving more ribs in boys than girls (boys T1-10, girls Tl-8) . 4) Between infancy and childhood, the lower ribs droop more in girls than boys (boys T9-10/12, girls T7 /8-12) . There is no change in the RVAs of the lower ribs between childhood and puberty in ei ther boys or girls. 5) The hypothesis is suggested that RVAs are influenced by the central nervous system through its influence on trunk muscle activity. 6) Rib­vertebra angle asymmetries (or differences, RVADs) are related to age and sex; their pattern reflects the common age , sex , and laterality patterns of idiopathic scoliosis. Extremes of such asymmetries may be an etiological factor for both infantile and adolescent idiopathic scoliosis. © 1992 Wiley-Liss, Inc.

Key words: rib eage, rib-vertebra angle differenees, idiopathie seoliosis, etiology

Received for publication February 5, 1991 ; revised and accepted November 24, 1991.

Address reprint requests to R.G. Burwell, Department of Hu man Morphology, Medical School , Queen's Medical Centre , Nottingham, NG7 2UH England.

Theodoros B. Grivas is now at 31 D. Bernardou Street, Brilissia 152 35, Athens, Greece.

© 1992 Wiley-Liss, Ine.

Segmental Rib-Vertebra Angles 273

INTRODUCTION

The thorax, like any other part of the skeleton, displays variations in dimensions and proportions which are partly individual and which are also linked to age, sex, and race (Williams and Warwick, 1980). The bony framework of the adult thorax has the shape of a truncated cone. At birth the chest is nearly circular in cross­section and the plane of the ribs is nearly horizontal. As the child grows, the shape of the chest changes so that the width of the chest cavity exceeds the antero­posterior dimension and the ribs become structurally stronger (Meredith and Knott 1937; see Kendig, 1977; Burwell et al. , 1983; Grivas, 1984).

The appraisal of thoracic functions in health and disorder by structural methods has included measurements of the rib cage on radiographs to estimate lung volume (Hurtado and Fray, 1933; Prime, 1971; Simonet al., 1972). The need to study the normal human rib cage segmentally with respect to rib-vertebra angles (RVAs) and thoracic shape emerged from studies of children with scoliosis. In this connection, apical rib-vertebra angle differences (RVADs) and RVAs were first used prog­nostically in children with infantile idiopathic scoliosis (liS) by Mehta (1972) and Kristmundsdottir et al. (1985), respectively. More recently, segmental RVAs have been used to analyse the effect of different surgical operations on the rib cage deformity in patients with adolescent idiopathic scoliosis (AIS) (Wojcik et al., 1990a,b). Lately, Wythers et al. (1992) measured segmental RVAs corrected for vertebral tilt in pre-operative patients wi th thoracic AIS; the method was then developed by Thirlwall (1991) and applied by Wemyss-Holden et al. (1991b) to pre-operative patients with thoracic AIS and non-scoliotic controls.

Grivas et al. (1991a, 1992), studying children with progressive liS , showed that the rib cage is significantly narrower at T1-4 compared with controls. Moreover, the funnel-shaped upper thoracic cage ofiiS is like that of the normal human fetu s. These findings suggest that there are different patterns of postnatal growth in the upper and lower ribs of the human.

To provide a normal base for our scoliotic RVA data , we report here a segmental analysis of RVAs in chest radiographs. Preliminary reports of the findings have been published (Grivas et al., 1991 b, 1992). The data on thoracic shape using thoracic ratios for the same children are published elsewhere (Grivas et al., 1991c).

MATERIALS AND METHODS Subjects

True posteroanterior (PA) chest radiographs were obtained from 412 children attending the Accident and Emergency Department at the University Hospital , Nottingham during 1989-1990 (Table 1). The children selected had minimal disorders or disease, involving mainly trauma, infections , foreign bodies, heart murmurs, and mild asthma. None of the patients had a scoliosis of 5 degrees or more. The chest radiographs were obtained in the standard way in inspiration.

Age and Sex Groups The age of each subject was calculated as decimal age. The subjects were

arranged into three age groups by sex in accordance with the classification of Karl berg (1989) (infancy = 0-2.999 years , boys = 37, gi rls = 54; childhood =

274 Grivas et al.

'D\BLE l. Number of boys and girls by age (n = 412)

Age (years)

0-0.999 1-1.999 2-2.999 3- 3.999 4- 4.999 5-5.999 6-6.999 7-7 .999 8- 8.999 9-9.999

10- 10.999 11-11.999 12-12.999 13- 13.999 14- 14.999 15-15.999 16- 16.999 17-17.999

Boys (n = 193)

13 13 11 16 11 12 10 12 8

12 15 11 11 10 9 7 3 9

Girls (n = 219)

17 18 19 21 12 13 12 10 12 11 11 13 11 8

12 17 2 0

3-10.999 years, boys = 96, girls = 1 02; and puberty = 11-17.999 years , boys = 60, girls = 63.

Measurements on Chest Radiographs

Rib-vertebra angles (Fig. 1). The rib-vertebra angles (RVAs) from T1 through T12 were measured in each of the right and left hemithoraces (Mehta, 1972; Kristmundsdottir eta!. , 1985; Wojcik eta!., 1990a, b; Wythers e ta!. , 1992). The techniques used previously were modified because of two factors: 1) the head of the rib is not as clearly evident in older children as it is in infants; and 2) the upper ribs curve upwards and laterally from the spine. The modifications involve the following methods being used to measure RVAs (Fig. 1 ): a) a line is drawn along the distal end-plate of each vertebra; b) at the middle of each end-plate a vertical line is drawn; and c) two points are defined on the rib , one where the rib meets the vertebra, and the second at a point midway between the edge of the vertebra and the outer margin of the thoracic cage. These two points are joined and extrapolated to meet the vertical line (b). The angle formed between the rib line and the vertical vertebral line is measured as the RVA for each segment from T1 to T12, for both left and right hemithoraces.

Rib-vertebra angle asymmetry (RVAD). A derivative for asymmetry, usually referred to as the rib-vertebra angle difference (RVAD) is calculated for each segment as left RVA minus right RVA.

Reliability study for rib-vertebra angles. The chest radiographs of 10 chil­dren, 5 boys and 5 girls, aged within the age range of the study population, were obtained from the "Agia Sofia" Paediatric Hospital, Athens. Rib-vertebra angles (RVAs) from T1-12 ribs were calculated twice (TBG) for the right and left hemi­thoraces on each radiograph . Then the difference for each pair (right and left) of RVAs was calculated. Finally, the intra-observer error was calculated as 95% confidence limits using the formula :

Segmental Rib-Vertebra Angles 2 7 5

Fig. 1. Chest radiograph to show method of measurement of rib-vertebra angles (see text).

Intra-observer error so X2 ff

The inter-observer error was calculated using the first set of TBG readings and those of an Orthopaedic Registrar, using the same formula. The intra- and inter­observer error findings for RVAs for each of the left and right ribs (T1-12) are shown in Table 2.

Statistical Analysis

Statistical techniques included Wilcoxon, Mann-Whitney, Kruskal-Wallis, Pear­son, and Spearmann correlation coefficients, ANOVA, cross-tabulations, t-test for asymmetry, and tests for skewness and kurtosis including the one-sample Kol­mogorov-Smirnov test (Snedecor and Cochran, 1980).

276 Grivas et al.

TABLE 2. Reliability study for rib-vertebra angle measurements: intra- and inter­observer error study (95% confidence limits in degrees)

Rib level

1 2 3 4 5 6 7 8 9

10 11 12

•95% confidence limits .

RESULTS RVAs

Intra-

2.04 2.72 1.90 1.84 1.77 1.30 1.67 1.81 2.10 2.53 2.83 2. 91

Right

Hemithorax/observer error ( ± )•

Left

Inter- Intra-

2.62 2.69 3.07 2.55 2. 18 2.36 2.22 2.70 2.31 1. 70 1.66 1. 79 2.03 1. 70 2.21 2.23 2. 78 2.12 2.89 2. 70 3. 12 2.02 3.21 1.52

Inter-

2.99 2.88 3.02 3.02 2.23 2.28 2.06 2. 73 2.80 3.08 2.23 1.84

Figure 2 shows RVAs by rib level for the left and right hemithorax and for each of boys and girls at the three age groups (infancy, childhood, and puberty, Tables 3A, 3B).

Sliewness and Kurtosis

There is little or no evidence of skewness or kurtosis for RVAs at any spinal level , for left or right hemithorax evaluated separately for each of the boys and girls in the different age groups. The RVADs show skewness at all levels (mostly P < .001) in infant gi rls, but not in infant boys, in childhood in both boys and girls, and during puberty in both boys and girls.

RVA Changes With Rib-Level

Figure 2 shows that for each age group in both boys and girls, the ribs droop increasingly from T 1 to T12 and especially at TS-12 (Tables 3A, 3B).

RVA Changes With Age

Between infancy and childhood , the RVAs of the upper ribs increase with age (Fig. 2, boys' average increase of6.4% at T1-4/5, girls' average increase of2 . 9% at T1-2/3, see Tables 3A, 3B). In the lower ribs, the RVAs decrease with age (boys Tll-12, gi rls T9-12) (Tables 4A, 4B).

Between childhood and puberty, the RVAs also increase with age (Fig. 2, boys T1-10, girls T1-8). At one level the RVAs decrease between childhood and puberty (girls, T12, right). Some ribs arejunctional, in that they droop between infancy and childhood and elevate between childhood and puberty (junctional ribs in boys, right T9-10, left T10; and in girls, right T7-8, left T8).

Segmental Rib-Vertebra Angles 277

Segmental rib-vertebra angles (RVAs) in controls (mean ± 1 SE)

Right RVAs

C/P ***"

**~' **~\ *** •

.------. ***\. ** I Rib elevation I ***\

_.. *::~ I Rib elevation I

Right RVAs

C/P

Boys

(degree s) Left RVAs

~ ~ 0 0 0 0 0 0 0

Girls

(degrees) Left RVAs

12 ***

• Infancy

• Childhood

0 Puberty

C/P

* .. 0.01 < p < 0.05, ** '"'0.001 < p < 0.01 . ** * :: p < 0.001

Fig. 2. Segmental rib-vertebra angles (RVA's in degrees) in boys and girls for each of the infancy (I) , childhood (C), and puberty (P) groups by rib level. Note that 1) in infancy at rib 6, RVAs are about 90 degrees ; 2) between infancy and childhood (IIC) the RVAs increase above rib 6 and decrease below rib 6; 3) between childhood and puberty (C/P) , RVAs increase from ribs 1 to 10 in boys and from 1 to 8 in girls; and 4) the junctional ribs (square brackets & stars) droop from infancy to childhood and elevate from childhood to puberty on the right at two levels (boys ribs 9-10, girls ribs 7-8) and on the left at one level (boys rib 10, girls rib 8) (see text).

RVAs and Sex Differences

In infancy, the upper left ribs (T l-5) in boys droop significantly more than in girls (Table 3A). This sex difference is less evident in right than left RVAs (T2 and 3, Table 3B). In childhood, there are minimal sex differences for RVAs ; and they are weakly significant at only two levels (rightT7-8, Table 3B). In puberty, the lower left ribs (T7 -1 0) in girls droop significantly more than in boys (Table 3A). The lower right ribs (T6-10) also droop significantly more in girls than boys (Table 3B ).

278 Grivas et al.

TABLE 3A. Rib-vertebra angles (left) in de~rees accordin~ to rib level, ~e ~roup, and sex

Boys Girls

Rib P, p P, p

level Age 1/C fo r 1/C for P, (left) group' Mean C/P ±1 SD ageb Mean P/C ±1 SD ageb boys/gi rl s'

I 108.2 ••• 7. 7 111.5 ••• 6.4 • c 115.8 6.6 ••• 115.5 6.2 ••• NS p 121.6 ••• 6.0 122.4 ••• 5.2 NS

2 I 102.6 ••• 7.9 106.7 • •• 7.1 •• c 110.4 8.0 ••• 110.5 6.4 ••• NS p 117.9 ••• 6.5 118.8 ••• 5.7 NS

3 I 97.4 ••• 9.1 102.7 NS 7.3 •• c 104. 1 9.4 ••• 104.6 7.9 ••• NS p 113.4 ••• 7.5 114.6 ••• 6.4 NS

4 I 94.6 •• 8.5 98.4 NS 7.7 • c 99.6 9. 1 ••• 100.1 8.1 ••• NS p 109.0 ••• 7.6 109.9 ••• 6.7 NS

5 I 92.5 • 8.0 95 .3 NS 7.2 • c 96.2 9.0 ••• 95.7 8.4 ••• NS p 105.3 ••• 7.9 105. 1 ••• 7.3 NS

6 I 90.1 NS 7.4 92.2 NS 6.8 NS c 92.8 8.7 ••• 91.6 7.4 ••• NS p 100.8 ••• 8.5 98.9 ••• 7.9 NS

7 I 87.2 NS 6.9 89. 1 NS 6.8 NS c 88.8 7.9 ••• 87. 1 7.2 •• NS p 95.6 ••• 8.5 91.9 ••• 8.3 •

8 I 84.0 NS 6.5 87.0 ••• 6.9 • c 83.5 7.5 ••• 82.3 6.7 ••• NS p 90.2 ••• 8.0 85.6 •• 7.9 ••

9 I 79.5 NS 6.8 83.0 ••• 7.4 • c 77.8 7.3 ••• 76.8 7.0 ••• NS p 83.4 ••• 8.2 78.5 NS 8.6 ••

10 I 73.6 • 7.9 75 .3 ••• 8.3 NS c 70.4 6.9 • 70.1 7.0 ••• NS p 74.5 • 8.5 70.2 NS 8.3 •

11 I 66.0 •• 8.9 66.3 •• 8.5 NS c 62.1 6.6 • 62.4 6.9 •• NS p 63.5 NS 7.5 61.6 NS 7.9 NS

12 I 59.9 ••• 7.7 58. 1 ••• 7.6 NS c 54.5 5.2 ••• 53.8 6.3 ••• NS p 53.3 NS 5.5 72 .3 NS 5.8 NS

'I = infancy; C = childhood ; P = puberty; NS not significant. bKruskal-Wall is test. 'Mann-Whitney test. • .01 < P < .OS . •• . 001 < p < .01. ... p < .001.

Segmental Rib-Vertebra Angles 279

TABLE 38. Rib-vertebra angles (rigltt) in degrees according to rib level, age group, and sex

Boys Girls

Rib P, p P, p level Age IIC for IIC for P, (right) group' Mean CIP ±lSD ageb Mean P/C ±I SO ageb boys/gi rl s<

I 108. 7 ••• 8.4 111.2 ••• 6.9 NS c 115.2 6.8 ••• 115.5 6.5 ••• NS p 121.6 ••• 6.2 122 .0 ••• 5.9 NS

2 I 103.1 ••• 8.7 106.5 •• 6.9 • c 109.9 8.0 ••• 110.4 7.4 ••• NS p 118.1 ••• 6.8 118. 1 ••• 6.1 NS

3 I 97.7 ••• 8.9 102.0 • 7.1 •• c 104.2 9.1 ••• 104.6 8.3 ••• NS p 113 .3 ••• 7. 7 113. 1 ••• 6.3 NS

4 I 94.7 •• 8.5 97.5 NS 7.9 NS c 99.5 8.7 ••• 99.7 8.0 ••• NS p 108.8 ••• 7.5 107.3 ••• 6.6 NS

5 I 93 .0 NS 7.7 94. 1 NS 7.6 NS c 95.6 8.3 ••• 94.8 7.8 ••• NS p 104.7 ••• 7.8 102.2 ••• 7.6 NS

6 I 91.1 NS 7.1 91.3 NS 7.3 NS c 92.0 8.0 ••• 90.1 7.6 ••• NS p 100.4 ••• 8.0 95.7 ••• 7.9 ••

7 I 88.5 NS 6.7 88.5 • 6.8 NS c 88. 0 7.4 ••• 85.6 7.2 •• • p 95.3 ••• 7.9 90.1 ••• 7.9 •••

8 I 85.8 NS 6.6 86.7 ••• 6.8 NS c 83.8 6.6 ••• 81.7 6.8 ••• • p 90.0 ••• 7. 1 84.8 • 8.0 •••

9 I 81.2 • 7.1 82 .7 ••• 7.2 NS c 78.0 6.5 ••• 76.5 7.0 ••• NS p 83.4 ••• 7.4 78. 1 NS 8.9 ••

10 I 75 .0 •• 8.4 75 . 1 ••• 8.0 NS c 70.7 6.4 •• 70.4 6.9 •• NS p 74. 7 •• 7.9 70.0 NS 8.7 ••

II I 66.6 •• 9.2 65 .5 NS 8.8 NS c 62.3 6.3 •• 62 .5 7.4 • NS p 62 .7 NS 7.3 61.0 NS 7.8 NS

12 I 59.7 ••• 8.0 57.4 •• 7.9 NS c 54.0 5.0 ••• 53.5 6.3 ••• NS p 52.6 NS 5.6 51.2 • 5.9 NS

' I = infancy; C childhood ; P puberty; NS not significant. bKruskal-Wall is test. <Mann-Whitney test. • .01 < P < .OS . .. . 001 < p < .01. •••P < .OOJ .

280 Grivas et al.

'L\BLE 4A. Rib-vertebra angles (left) for boys and girls showing relation to age (decimal years) and sex

Linear regression Correlation Rib level equation (y = a+ bx) coefficient (left} Sex a b Sign.r

Boys 108.4 .0.952 0.591 •••• Girls 110.3 0.836 0.568 ••••

2 Boys 102.1 1. 125 0.611 •••• Girls 105. 1 0.924 0.580 ••••

3 Boys 95.9 1. 212 0.576 •••• Girls 100.1 0.943 0.528 ••••

4 Boys 92.5 1. 113 0.555 •••• Girl s 95.8 0.911 0.501 ••••

5 Boys 90.1 1.013 0.519 •••• Girls 92 .3 0.816 0.453 ••••

6 Boys 87.7 0.876 0.468 •••• G irls 89.5 0.591 0.369 ••••

7 Boys 84.8 0. 712 0.415 •••• Girls 86.8 0.293 0. 188 •••

8 Boys 81.0 0.573 0.356 •••• Girls 84.7 - 0.048 - 0.033 NS

9 Boys 76.4 0.426 0.270 •••• Girl s 81. 2 - 0.323 0.200 •••

10 Boys 70.3 0.240 0.153 •• Girls 74.4 - 0.401 - 0.247 ••••

II Boys 63 .9 -0.075 - 0.050 NS Girls 66.0 - 0.390 - 0.246 ••••

12 Boys 58.4 - 0.407 - 0.323 •••• Girls 57.6 - 0.438 - 0.316 ••••

• ANOVA for sex corrected for age, sign .r = probabil ity fo r r. NS = not significant. •• .01 < P < .OS . ... . 001 < p < .01. uup < .001 .

RVADs

p (boys/ girls) •

NS

••

••

••

NS

NS

NS

NS

NS

NS

NS

NS

Figure 3 shows the RVADs plotted against age for each age group (Table 5) . A weak asymmetry is seen in infant boys at T8 , whereas infant girls show asymmetry at two levels (T4- 5). Girls in childhood show significant asymmetry at T6-7 and adolescent girls at T4-7. The childhood and pubertal boys show little or no significant asymmetry.

Comparing infancy with childhood , the boys show a significant lessening of the droop of the left ribs relative to the right at each of 5 levels (T5-9) . The girls show little or no change in RVADs between infancy and childhood . Comparing child­hood with adolescence, the boys show no change in RVADs; but the girls show increasing droop of right ribs relative to left at each of 2 levels (T3-4).

Fourteen subjects have RVADs of 20 degrees or more: infancy one; childhood , boys 4 (three with ribs drooping more on left), girls 3 (two with ribs drooping more on left); and puberty, boys 2 (both with ribs drooping more on right), girls 4 (three with ribs drooping more on right).

Analys is of RVADs against age show a weakly significant positive correlation but

Se~ental Rib-Vertebra Angles 281

ThBLE 48. Rib-vertebra angles (right) for boys and girls showing relation to age (decimal years) and sex

Linear regression Correlation p Rib level equation (y =a+ bx) coefficient (boys/ (right) Sex a b Sign.r girls)•

Boys 108. 1 0.980 0.589 •••• NS Girls 110.3 0.812 0.527 ••••

2 Boys 102.0 1.137 0.602 •••• NS Girls 105.1 0.894 0.534 ••••

3 Boys 96.3 1.180 0.510 •••• NS Girls 100.1 0.858 0.487 ••••

4 Boys 92. 8 1.077 0.459 •••• NS Girls 95.5 0.795 0.458 ••••

5 Boys 90.4 0.935 0.503 •••• NS Girls 91.6 0.702 0.409 ••••

6 Boys 88.1 0.791 0.450 •••• •• Girls 88.9 0.421 0.259 ••••

7 Boys 85.3 0.628 0.387 •••• •••• Girls 86.2 0.202 0.131 ••••

8 Boys 82. 5 0.451 0.308 •••• ••• Girls 84.5 -0.085 - 0.056 NS

9 Boys 77. 9 0.300 0.205 ••• •• Girls 80.8 - 0.302 - 0.185 •••

10 Boys 71.9 1.140 0.075 NS NS Girls 74.4 - 0.400 - 0.246 ••••

11 Boys 65.3 -0.245 - 0. 165 •• NS Girls 65.6 - 0.372 -0.227 ••••

12 Boys 58.3 -0.440 -0.342 •••• s Gi rls 57.3 - 0.463 -0.324 ••••

• ANOVA for sex corrected for age, sign.r = probability for r. NS = not significant. •• .01 < P < .OS . ... . 001 < p < .01. .... P <.OOl.

only for the boys at each ofT9 (r = 0.14, P = .046) and T ll (r = 0.18, P = .014); the girls show no statistically significant relation between RVAOs and age at any level.

DISCUSSION Rib Cage Functions

The outstanding function of the thorax is in respiration . In this connection, Keith (1909) dis tinguished four mechanisms in the enlargement of the thoracic cavity during inspiration:

The thoracic lid (1 st rib and manubrium sterni). The upper costal se ries (2nd-5th ribs inclusive). The lower costal series (6th-10th ribs inclusive). The diaphragm.

282 Grivas et al.

Infancy

Segmental rib-vertebra Mgle asynnetry (RVAD) in conbols

!ffl!l.~fn t:l~~ lliBJ{J]I6fJIKM ~/biB t:l~~a /liJKH/6D fJJI6D ~llfNfl:~

Childhood Puberty leh RVA t Right RVA + Leh RVA + Right RVA + Leh RVA t Right RVA +

· 3 · 2 · 1 0 · 2 · 1 0 · 3 · 2 · 1 0 1 2

Plsex P I asymmetry PI sex P I :symmetry Plsex P I asymmetry

4 *

3 * Boys-Boys'·,· ..

4 ** *** ~ s *** s ** *** 0 0 6 *** ** 6 ** *** z

*** * • **

' ** 10 10 10

, *

12 12 12

P . probabili ty, * = 0.01 < p < 0.05, ** = 0.001 < p < 0.01, ** * = p < 0.001, NS = not significant

Fig. 3. Segmental rib-vertebra angle asymmetry (rib-vertebra angle difference , RVAD) in the boys and girls for each of the infancy (I) , childhood (C) , and puberty (P) groups. The statistically significant differences are given by level for each of 1) asymmetry of RVAs (P/asymmetry); and 2) boys and girls compared (P/sex). Note that 1) the boys show asymmetry of RVAs in infancy (smaller on left than on right) , but not in childhood and puberty; and 2) the girls show RVA asymmetry in each of infancy, childhood , and especially in puberty (smaller on the right than on the left).

In addition, the ribs are the principal agents for the support of the thoracic vertebrae by virtue of their rigidity not only as bony braces but also because of their service as instruments through which the forces exerted by the attached muscles and ligaments and the forces of intrathoracic pressures and stresses are transmitted to the vertebrae through their costovertebral articulations (Bisgard , 1934 ). During walking, the trunk must balance on the pelvis which moves along vertical and lateral axes as well as the progressional axis (Waters and Morris, 1972; see Newman, 1968).

In attempting to interpret the changes ofRVAs with respect to rib level, age, sex, and side, it is necessary to bear in mind not only the respiratory function of the rib cage but also its balancing role in the standing and sitting positions in gait and in many movements. Present evidence is consistent with the view that the lower ribs help to control spinal rotation and lateral flexion under the influence of muscles attached to them (see Gregersen and Lucas, 1967; Waters and Morris, 1972; Burwell et al. , 1990, 1992a; Cole et al. , 1990).

ICP Model of Growth

An important feature in our analysis of the thoracic ratios in children from 0 to 17 years (Grivas et al., 1991a, c) is the use of the ICP model of Karl berg (1989) which we also use here in analysing RVAs and RVADs.

This model breaks down growth mathematically into three additive and partly

Segmental Rib-Vertebra Angles 283

TABLE 5. Rib-vertebra angle difference (RVAD, left minus ri~t) in de~ees according to rib level, age ~oup, and sex

Boys Girls

P, p P, p Rib Age 1/C for 1/C for P, level group• Mean C/P ± 1 SD po ageb Mean PIC ±1 SD po ageb boys/girlsc

I -0.486 NS 2. 642 NS 0 .204 NS 2.910 NS NS c 0.573 2. 566 • NS -0.010 2.1 22 NS NS NS p -0.083 NS 0.889 NS 0.429 NS 2.575 NS NS

2 I -0. 568 NS 4.634 NS 0.185 NS 2.934 NS NS c 0.406 2.347 NS NS 0.020 2.952 NS NS NS p -0.283 NS 1. 718 NS 0.651 NS 3.446 NS NS

3 I -0.324 NS 4.583 NS 0.630 NS 2.890 NS NS c -0. 167 2.566 NS NS -0.069 3.387 NS • NS p 0. 117 NS 2.415 NS 1.524 •• 4.610 NS •

4 I -0. 189 NS 3.879 NS 0.926 NS 3.244 • • c 0. 042 3.221 NS NS 0.353 4.155 NS NS NS p 0. 150 NS 2. 635 NS 2.540 • 5.095 ••• ••

5 I -0.595 • 4.304 NS 1.130 NS 3.127 • ••• c 0.542 3.476 NS NS 0.892 5.062 NS NS NS p 0.533 NS 2. 514 NS 2.810 NS 5.515 ••• ••

6 I -1. 081 •• 4.997 NS 0.889 NS 3.306 NS ••• c 0.771 4.401 NS • 1.451 4.462 •• NS NS p 0.433 NS 3.346 NS 3. 111 NS 5.795 ••• ••

7 I -1.351 • 5. 167 NS 0.481 NS 3.185 NS • c 0.740 4.226 NS • 1.431 4.116 ••• NS NS p 0.300 NS 3.509 NS 1.825 NS 5.681 • NS

8 I -1.892 • 5.269 • 0.204 NS 2.743 NS •• c -0.302 5.320 NS • 0.598 3.594 NS NS NS p 0.133 s 3.260 NS 0.778 NS 5.014 NS NS

9 I -1.703 • 5.243 NS 0.204 NS 3.372 NS •• c -0.198 4.681 NS • 0.284 3.547 NS NS NS p 0.000 NS 3. 119 NS 0.365 NS 5.404 NS NS

10 I -1 .405 NS 5. 946 NS 0.111 NS 3.795 NS NS c -0.354 4.343 NS NS - 0.275 4.340 NS NS NS p -0.250 NS 4.963 NS 0.175 NS 4.914 NS NS

11 I -0.676 NS 6. 347 NS 0.722 • 3.098 NS • c -0.271 4.330 NS NS 0.127 4.036 NS NS NS p 0.833 NS 4.450 NS 0.571 NS 4.805 NS NS

12 I -6.784 NS 7. 674 NS 0.667 NS 4.084 NS NS c -7.875 4.983 NS NS 0.245 3.668 NS NS NS p -9.450 NS 6. 547 NS 8.762 NS 5.882 NS NS

•I = infancy; C = childhood; P = puberty; NS = not significant; po = probability for asymmetry. bKruskal-Wallis test. cMann-Whitney test . • . 01 < p < .05 . •• . 001 < p < .01. •••P < .OOl.

284 Grivas et al.

superimposed components-infancy, childhood, and puberty. These components strongly reflect the different hormonal phases of the growth process. As a result, the model provides an improved instrument for detecting and understanding growth failure. It has already been applied to Perthes' disease (Burwell et al., 1986 ), slipped upper femoral epiphysis (Hagglund et aL, 1987), and adolescent idiopathic scoliosis (Hagglund et al., 1992).

Relation of RVAs to Spinal Level and Age

Six features of the RVA results (Fig. 2) are worthy of comment: 1) the gradual decrease in RVAs from T1 to T12 and especially from T8 to T12; 2) between infancy and childhood the upper ribs elevate, like a bucket handle. This is greater in magnitude and occurs at more levels in boys than girls (boys 6.4% at T1-4/5, girls 2. 9% at T1-2/3); 3) between childhood and puberty there is a further elevation of the ribs, again more extensive in boys than girls (boys Tl-10, girls T1 -8); 4) in the lower chest between infancy and childhood the ribs droop, more in girls than boys (boys T9-10/12, girls T7-8/12); 5) between childhood and puberty, the lower RVAs show virtually no change (boys Tll-12, girls T9-12); 6) some ribs, junctional between those that elevate and those that droop , droop early in develop­ment only to elevate later (boys, right T9-10, left T10; girls , right T7-8, left T8, see Figure 2, marked ** and *).

Elsewhere, we show that the funnel-shaped upper chest of the newborn human gradually changes its shape to adopt a barrel-shaped chest (Grivas et al., 1991a, c). The elevation of the upper 6-7 ribs during postnatal development may alter respiratory volume. We suspect that it also provides , first, more stability of the upper thoracic spine, second, more control of the spine in the frontal plane (lateral flexion), and third, more control of spinal counter-rotations in response to the rotations of the thoracolumbar spine and pelvis during gait with a cross-over at T7 (see Gregersen and Lucas, 1967). The drooping of the lower ribs seems to provide a mechanism to narrow the chest and so reduce the rotational inertia transmitted to the thorax from the rotating thoracolumbar spine and pelvis in gait (see Grivas et al. , 1991 b, c).

Possible Factors Causing the Age-Related Changes in RVAs-­Neuromuscular Mechanisms

In growing, healthy subjects , RVAs will be influenced by muscles attached to the ribs. Some back muscles exert their pulls in a superior or an inferior direction (see Carey, 1932). In this connection , Cook et al. (1991) , in a segmental study of iliocostalis, suggests that the flat muscles of the tru nk, including serratus anterior and abdominal muscles, are important in rotatory control of the spine through muscle and upper ribs. Wemyss-Holden et al. (1991a , b) suggest that the muscles causing trunk rotation in gait form a composite spiral. .\1oreover, they suggest that asymmetries of this muscular spiral may play a role in scoliosis etiology; and in particular that the droop of the upper concave ribs may result from greater asym­metrical action of trunk rotator muscles on the concavity than of the convexity of the idiopathic scoliotic curve .

We suggest the hypothesis that the angle which a rib makes with its vertebra is, in part, the result of summated muscular forces acting in opposite directions along the length of the growing trunk, i.e. , RVAs express muscle balance. In this

Segmental Rib-Vertebra Angles 285

muscular hypothesis, the elevation of upper ribs during normal growth would result from relatively more powerful cranially situated muscles attached to ribs. Drooping of lower ribs during normal growth results from relatively more powerful caudally situated muscles. This concept implies that there is a physiological alteration of muscle balance on ribs during growth, due to an inherited programme of develop­mental change in the central nervous system. The more extensive rib elevation in boys is consistent with the greater development of the shoulder girdle in boys. More powerful cranially situated muscles in males would explain why the adult male manubrium is positioned at a higher level than that in females (Williams and Warwick, 1980; see Grivas et al. , 1991c).

Relation of RVAs to Sex The sex differences in RVAs are mostly evident in infancy and puberty, with few

differences in childhood. The changes in puberty reflect the narrowing of the chest as revealed by using thoracic ratios (Grivas et al., 1991c).

We suggest that the greater droop of the upper ribs (T1-5, Tables 3A and B) in infant boys compared with infant girls is accounted for by neuromuscular mecha­nisms associated with the maturational delay of boys.

The greater droop of the lower ribs in girls (T6-10, Tables 3A and B) compared with boys is reflected in the narrower chest of girls revealed by using thoracic ratios (Grivas et al. , 1991c). In this connection, the vertebrae of girls are significantly more slender than are those of boys (Glasbey, 1983; Schultz et al., 1984 ). The drooping of the lower ribs of girls occurs between infancy and childhood, or largely before the girl's pelvis increases in size (Burwell et al., 1983 ); Nicolopoulos et al., 1985). We suggest that the mechanism by which this rib droop occurs is through neuromuscular factors. Between childhood and puberty, the increased rotational inertia generated b the larger pelvis of girls is not associated with further lower rib drooping but, we suggest, with rib growth impairment (relative to spinal growth) in the lower half of the chest (Grivas et al., 1991c; see Cole et al., 1990). During the same developmental period (childhood to puberty), boys show no further relative narrowing of the chest.

Side Differences-Rib-Vertebra Angle Asymmetry Asymmetry of RVAs is generally referred to as the rib-vertebra angle difference

(RVAD, Mehta, 1972). In previous work on RVADs and RVAs attention has been directed almost exclusively to patients with scoliosis, initially at the apex of the scoliosis curve (Mehta, 1972; Kristmundsdottir et al., 1985) and more recently, segmentally (Wojcik et al. , 1990a, b; see Wythers 1992; Thirlwall, 1991; Wemyss­Holden et al., 1991 b).

~ean Differences The pattern of asymmetry ofRVAs in the normal rib cage is shown in Table 5 and

plotted as RVADs for infancy, childhood, and adolescence in Figure 3. The RVAD findings show significantly more drooping left ribs at T8 in infant

boys. In childhood and puberty the boys show little or no RVA asymmetry. In contrast the RVAs in girls are significantly asymmetrical in infancy (T4-5), in childhood (T6-7) and markedly so in puberty (T4-7, Fig. 3). The ribs droop more on the right in the girls in each of these age groups.

286 Grivas et al.

Using the neuromuscular hypothesis already mentioned, we suggest that " nor­mal" RVA asymmetry results from an alteration of physiological balance of muscles attached to ribs on each side of the chest. In infantile idiopathic scoliosis, an RVAD of20 degrees or more at the curve apex is used to predict curve progression (Mehta, 1972). In our series, one infant had an RVAD of 20 degrees or more; in childhood and puberty there were 4.0% of subjects in this category (chi ldhood, 4 boys and 3 girls; puberty 2 boys and 4 girls).

Significance of the RVA and RVAD Findings for the Etiology of Idiopathic Scoliosis

The findings we report here for "normal" children reveal RVA asymmetries (RVADs) in infancy, childhood, and puberty (Fig. 3). Overall, the pattern of this " normal" RVA asymmetry reflects the age, sex, and laterality patterns of idiopathic scoliosis. It suggests that extremes of RVADs may be etiological factors for both infantile and adolescent idiopathic scoliosis; this possibility is included in our concept of the pathogenesis of idiopathic scoliosis which now implicates the central nervous system and specifically an asymmetry of central pattern generators in the spinal cord which control human posture and gait (Burwell et al., 1992a, b).

Grivas et al. (1990, 1991a), studying children with progressive infantile id­iopathic scoliosis (liS), showed that the rib cage is significantly narrower at T1-4 compared with controls. Moreover, the funnel -shaped upper thoracic cage of liS is like that of 1) the normal human fetus and 2) the normal rabbit. In this connection, we have suggested the hypothesis that the size (and mass) of the pelvis in relation to

the developmental stage of the rib cage needs to be in biomechanical balance throughout growth so as to prevent the thoracic cage being overloaded during the pelvi-spinal rotations of human bipedal gait (Burwell et al. 1991).

ACKNOWLEDGMENTS

The authors are indebted to Action Research Leading Medical Research for financial support, Dr.] .C. G. Pearson, Senior Lecturer, DepartmentofCommu­nity Medicine and Epidemiology, for statistical advice, Dr. N. Tsoutsaio for contributing to the reliability study and Mrs. A. Bexon for manuscript prepara­tion .

REFERENCES

Bisgard, J. 1934 Thoracogenic scoliosis. Influence of thoracic disease and thoracic operations on the spine. Arch. Surg., 29:417- 445 .

Burwell, R.G., N .J. James, F . Johnson , J.K. Webb, and Y.G. Wilson 1983 Standardised trunk asymmetry scores: a study of back contour in healthy schoolchildren. J. Bone Joint Surg. [Br. ], 65:452-463 .

Burwell , R.G., C.L Vernon , P.H . Dangerfield , D.]. Hall , and F. Kristmundsdottir 1986 Raised somatomedin activity in the serum of you ng boys with Perches' disease, revealed by bioassay. A disease of growth transition? Clin Orthop., 209:129- 138.

Burwell , R.G., S.S. Upadhyay, A.S. Wojcik, N.C.M. Bacon, A. Moulton, and j .K. Webb 1990 Ultrasound in evaluating scoliosis. In Proceedings of the Eighth Phillip Zorah Scoliosis Symposium, 26-28 October 1988, London. D. Siegler, D. Harrison, and M. Edgar (eds.). London: Phillip Zorah Scoliosis Research Fund, pp. 48-67.

Segmental Rib-Vertebra Angles 287

Burwell, R.G., A.A. Cole, T.B. Grivas, A.W. Kiel, A. Moulton, S.S. Upadhyay, j.K. Webb, A.S. Wojcik, and D.j . Wythers 1992a Screening, aetiology and the Nottingham theory for idiopathic scoliosis. In 6th International Symposium on Surface Topography and Spinal Deformity, Hotel Estoril Eden, 19-20 September 1990. A. Alberti , R. Drerup, E. Hierholzer (eds.). Stuttgart: Gustav Fischer Verlag, pp. 136-161.

Burwell , R.G., A.A. Cole, T.A. Cook, T.B. Grivas, A.W. Kiel, A. Moulton, A.S. Thirlwall, S.S. Upadhyay, J.K. Webb, S.A. Wemyss-Holden, D.J. Whitwell, A.S. Wojcik, and D.J Wythers 1992b Pathogenesis of idiopathic scoliosis: The Nottingham concept. Proceedings of the Combined Meeting of the British Scoliosis Society and the Nordic Scoliosis Society, Newcas­tle upon tyne, 5-6 June 1991. J. Bone Joint Surg. [Br.] (in press).

Carey, J. 1932 Scoliosis: etiology, pathogenesis and prevention of experimental rotary lateral curvature of the spine. }.A.M.A. 98:104-110.

Cole, A.A., R. Barson, R.G. Burwell, K.J. Jacobs, A. Moulton, W.A. Wallace, j .K. Webb, and A.S. Wojcik 1990 The use of CODA to measure pelvic movements in normal gait: the concept of coupled pelvi-s pinal rotation. Clin. Anat., 3:65 .

Cook, T.A., R.G. Burwell , S.A. Wemyss-Holden, and j .K. Webb 1991 A segmental study of iliocostalis: functional and clinical implications. Clin . An at., 4:387.

Glasbey, J .A. 1983 A study of vertebral body shape and skeletal shape in healthy and scoliotic children. Thesis: University of Nottingham.

Gregersen, G.G., and D. B. Lucas 1967 An in vivo study of the axial rotation of the human thoracolumbar spine . J . Bone Joint Surg. [Am.], 49:247-262.

Grivas, T .B. 1984 Survey for the lower limbs of early school age children. Thesis: University of Athens (in Greek), p. 93.

Grivas, T.B., R.G. Burwell , M. Purdue, j .K. Webb, and A. Moulton 1992 The rib-cage deformity in infantile idiopathic scoliosis-the funnel-shaped upper chest in relation to specific rotation as a prognostic factor. An evaluation of thoracic shape in progressive scoliosis and control children during growth. In 6th International Symposium on Surface Topography and Spinal Deformity, Hotel Estoril Eden, 19-20 September 1990. A. Alberti, B. Drerup, and E . Hierholzer (eds.). Stuttgart: Gustav Fisher Verlag, pp. 93-109.

Grivas, T. B. , J. K. Webb, and R. G. Bunvell1991a T he funnel-shaped upper chest of progressive infantile idiopathic scolios is (liS): sign ificance for rib growth patterns, rib dysplasia and aetiology of the spinal deformity. Clin . Anat., 4:73 .

Grivas, T.B., R.G. Burwell , M. Purdue, J.K. Webb, and A. Moulton 1991b The segmental patterns of rib-vertebra angles in chest radiographs of children: significance for idiopathic scoliosis. Clin. Anat., 4:387.

Grivas, T .B. , R.G. Burwell , M. Purdue, j.K. Webb, and A. Moulton 1991cAsegmentalanalysis of thoracic shape in chest radiographs of children. Changes related to spinal level , age, sex, side and significance for lung growth and scoliosis.]. Anat. 178:21-38.

Hagglund, G., L.I. Hansson, V. Hansson, and j . Karlberg 1987 Growth of children with physiolysis of the hip . Acta Orthop. Scand., 58:117-120.

Hagglund , G. , ]. Karlberg, and S. Willner 1992 Growth in girls with adolescent idiopathic scoliosis. Spine 17: 108-111.

Hurtado , A., and W. W. Fray 1933 Studies of total pulmonary capacity and its subdivisions. III. Changes with body posture . J. Clin . Invest., 12:825-832.

Karl berg, J. 1989 A biologically-orientated mathematical model (ICP) for human growth. Acta. Paediatr. Scand. [Suppl.], 350:70-94.

Keith, A. 1909 The Mechanism of Respiration in Man. Further Advances in Physiology. London: Arnold .

Kendig, E. L. 1977 Disorders of the Respiratory Tract in Children. History and Physical Exam­ination. Philadelphia: W.B. Saunders Co., p. 88-89.

King, H.A., j .H . Moe, D.S. Bradford, and R.B . Winter 1983 The selection of fusion levels in thoracic idiopathic scoliosis . ]. Bone Joint Surg. [Am. ], 65:1302-1313.

Kristmundsdottir, F . , R.G. Burwell, and J.I .P. James 1985 The rib-vertebra angles on the convexity and concavity of the spinal curve in infantile idiopathic scoliosis. Clin . Orthop., 201:205-209.

288 Grivas et al.

Mehta, M. 1972 The rib-vertebra angle in the early diagnosis between resolving and progressive infantile scoliosis. 1. Bone Joint Surg. [Br. ], 54:230-243.

Meredith , H.V. , and V.B. Knott 1937 Changes in body proportions during infancy and the preschool years: I. The thorax index. Child Dev., 8 :173-190.

Newman, P.H . 1968 The spine , the wood and the trees. Proc. R. Soc. Med . , 61:34-41. N icolopoulos , K.S., R.G. Burwell , and j.K. Webb 1985 Stature and its components in healthy

children: sexual dimorphism and age related changes. j . Anat. , 141 :105-114. Prime, F.j. 1971 Comparisons between rates of growth of lung volume and " radiological chest

volume" in normal and scoliotic children . In Scoliosis and Growth. Proceedings of a Third Symposium. P.A. Zorah (ed.). London: Churchill Livingstone, pp. 124-127.

Schultz, A.B ., S.E. Sorensen, and G.B.] . Anderson 1984 Measurements of spine morphology in children , ages 10-16. Spine, 9:70-73.

Simon, G. , L. Reid , j .M. Tanner, H . Goldstein , and B. Benjamin 1972 Growth of radiologically determined heart diameter, lung width and lung length from·5- 19 years , with standards for clinical use . Arch . Dis . Child ., 47:373-381.

Snedecor, G. W. , and W. G. Cochran 1980 Statistical Methods , 7th ed. Ames, IA: The Iowa State University Press.

Thirlwall, A.S. 1991 T he relation of King curve type to the surface and radiological deformity of preoperative scoliosis. T hesis: Unive rsity of Nottingham.

Waters, R.L., and j .M. Morris 1972 Electrical activity of muscles of the trunk during walking. J . Anat., 111:191-199.

Wemyss-Holden , S.A., R.G. Burwell , T.A. Cook, C. Binch, j .K. Webb, and A. Moulton 1991a A spiral com posite muscle trunk rotator in man? Relevance to gai t, idiopathic and sportsman's scolioses and stroke. Clin . An at., 4:386.

Wemyss-Holden, S.A., K.j. Jacobs, R.G. Burwell , S.A. McNeill , F.j . Polak, j.K . Webb, and A. Moulton 1991 b The rib cage in adolescent idiopathic scoliosi s (AIS): a segmental analys is of rib-vertebra angles (RVAs) revealing crossed RVA asymmetry with ae tiological implications . Proceedings of a Joint Meeting of the British Association of C linical Anatomists and the American Association of Clinical Anatomists, Norwich , 8-1 1 July 1991. Clin . A nat. (in press).

Williams , P. L ., and R. Warwick (eds.) 1980 Gray's Anatomy, 36th edition. New York: Churchill Livingstone, pp . 291 and 1252 .

Wojcik, A.S., J .K. Webb, and R.G . Bu rwell 1990a An analysis of the effect of the Zielke operation on th e rib-cage of S-shaped curves in idiopathic scoliosis. Spine, 15:8 1-86.

Wojcik , A.S., ].K . Webb, and R.G. Burwell 1990b Harrington-Luque and Cotrel-Dubousset instrumentation for idiopathic thoracic scoliosis-a postoperative comparison using segmental radiologic analysis. Spine, 15:424-431.

Wythers, D .j. , R.G. Burwell , J. K. Webb , and A.S. Wojcik 1992 The segmental surface and rib deformity of progressive adolescent idiopathic scoliosis: a preoperative segmental appraisal suggesting aetiological factors in the lumbar spine. In 6th International Symposium on Surface Topography and Spinal Deformity, Hotel Estoril Eden, 19- 20 September 1990. ed. A. Alberti, B. Drerup , and E. Hierholzer (eds. ). Stuttgart: Gustav Fischer Verlag, pp. 119-135.