Sexual Dimorphism in the Growth of the Cranium

B. BAUGHAN AND A. DEMIRJIAN

Human Growth Research Centre, Uniuersity of Montreal, Montreal, Quebec,
Canada H3T l J 6

KEY WORDS Cranium Pubertal growth . Sexual dimorphism

Cephalization index

ABSTRACT The major sexual dimorphisms in body size appear a t puberty

but, by then, 95%of the growth of the cranium is completed. As sexual dimor-
phism in the cranium is as great as for other parts of the body, this suggests
that it must appear at an earlier age, and that craniumhody size ratios for the
two sexes will vary during growth. Results from a longitudinal study of Mon-
treal children are used t o investigate this phenomenon. The effect is expressed
quantitatively by proportional growth and growth velocity curves, based on the
final size of boys, which show that the dimorphism indeed makes an early ap-
pearance. The data are also analyzed on an age scale relative to the ages of
peak growth velocity in stature, derived from the individual growth curves.
This shows that although there is a minor pubertal spurt in growth for the ex-
ternal cranial dimensions of boys, it contributes relatively little t o the final di-
morphism in cranial size. To summarize this aspect of growth, an index of ceph-
alization is calculated: head length X head widthhtature. Cross-sectional stan-
dards for the change of the mean index with age show a linear decline for boys
and girls until puberty, with a constant difference between them. After puber-
ty, the index becomes equal in the two sexes. Individual development curves for
the index are however not linear.

A study of the literature on human growth
reveals an unresolved problem. It becomes ap-
parent when three pieces of disparate infor-
mation are juxtaposed: first, the famous dia-
gram of Scammon ('30) shown in figure l.
The separate data from which Scammon
('30) assembled this picture related mainly to
the weight of various organs. They suggest
that the brain has attained 90% of its adult
weight by six years of age, and 95%by ten,
while the body as a whole has barely attained
40%of the adult value at six years of age, and
50% a t ten.
Second is the development of sexual dimor-
phism in general body dimensions. We illus-
trate this by the curves for weight recon-
structed from Tanner et al., ('661, shown in
figure 2.
It is seen that dimorphism remains minor
until after puberty when, due t o differences in
timing and intensity of the pubertal growth
spurt, girls have acquired a t 18 years a mean
weight of 10.2%smaller than that of the boys.
Our third and final fact concerns adult sex-
AM. J. PHYS. ANTHROP. (1978)49: 383-390.
ual dimorphism in brain weight. Firmly based
data here are rare: Pakkenberg and Voigt
('64?,for a carefully selected series of Danish
cadavers, give a mean brain weight for 325
women of 1,282 gm, which is 11%smaller than
the 1,440g m mean weight for 765 men.
In summary, therefore, we have an adult
sexual dimorphism in brain size at least as
large as that for total body size. Yet, that body
dimorphism appears at a time when the brain
has apparently completed over 95% of its
growth. Thereby, when does sexual dimorph-
ism in brain size appear; how does the dif-
ferential timing of the two dimorphisms affect
brainhody ratios in childhood; and, more
problematically, by what control mechanism
is t h e earlier dimorphism mediated and
aligned with the final pubertal one?
The problem has to be slightly recast t o be-
come open to study. Modern morphologists
(Moss and Young, '60) accept that it is the
growth of the brain that determines cranial
shape and expansion, rather than vice-versa.
This suggests that a measure of cranial capac-
383
384
- LVMPHQlO TYPE
180
....
__
N E U R & I TYPE
GLNERAL 1 Y P E
AGE I Y E A H S )
Fig. 1 Idealized growth curves for different parts of
the body: after Scammon ('30).
RELATIVE
WtlGHT
30 1 DATA
Fig. 2 Sexual dimorphism in mean growth curves for
weight: after Tanner e t al. ('66).
ity may replace brain weight in growth stud-
ies. In fact, what we report is a study of
changes in external measures of cranial
length and width, related to changes in
stature. Weight, as our introduction indi-
cated, appears more often than stature in the-
oretical discussions, because of its role in
allometric relationships. However, the vary-
ing obesity in modern population makes its
use in human investigations difficult.
Previous work in this field was addressed to
a slightly more limited question-is there a
B. BAUGHAN AND A. DEMIRJIAN
pubertal spurt a t all in cranial growth? -and,
n by failing to examine the proportion of total
growth involved in the spurt, if present, has
missed the implications that we wish to bring
out. Roche and Lewis ('74) present evidence,
based on X-ray measurements, for a pubertal
spurt in the growth of the cranial base, with
the spurt being more marked for boys. HOW-
ever, Nakamura et al. ('72) presented a simi-
lar study of the sphenoid bone which sug-
gested that such changes differ with the sur-
face of the bone and are largely confined to the
lower, or ventral, surface. Several authors
(Eichorn and Bayley, '62; Miklashevskaya,
'66) have suggested pubertal spurts in exter-
nal length, width or circumference measures.
Roche ('53) though shows that much of the
pubertal change in length is confined to the
nasal sinuses within the frontal bone, this
change being more apparent in boys. This
ABSOLUTE
finding is supported by Baer and Harris' ('69)
WEIGHT
study of a limited number of individual
60
KG growth curves of endo- and ectrocranial
length, and by Sekiguchi et al.'s ('73) study of
55 cranial base and cranial length measures. In a
study of children up to 14 years of age, Singh
LO
et al. ('67) do find a pubertal spurt for inner
45 cranial width, but note also greater changes in
the external soft tissue. Lestrel and Brown
10
('76) have also recently reported a pubertal
I5
augmentation in cranial shape changes. In
summary, the evidence supports a pubertal
30 spurt in the external cranial dimensions of
boys, but its existence for internal dimensions,
25
or for girls, remains problematic.
- 20
The results reported here derive from the
AGE
ongoing work of the Montreal Growth Re-
search Centre. The Centre has followed longi-
tudinally two cohorts of school-age children;
the numbers of annual examinations a t dif-
ferent ages, girls and boys separately, are
given in table 1.
Data collection was carried out between
1967-1976, and has now terminated. Any ex-
amination more than 30 days distant from a
child's birthday was excluded from analysis:
91.5%of the examinations were within plus or
minus 15 days of the birthday.
For the analysis with respect to chronologi-
cal age, the entire sample, as enumerated in
table 1, was available. For the analysis with
respect to age of peak growth velocity in sta-
ture, a subsample was used. Because of pro-
gressive drop-out a t the older ages, if we had
 SEXUAL DIMORPHISM IN THE GROWTH OF THE CRANIUM 385
TABLE 1 ference on this measure. Rather than make an
Sample sizes of first and second longitudinal cohorts arbitrary adjustment to some of our measures,
of the Montreal Growth Centre we have left them as recorded.
First cohort Second cohort
To check for errors in our data, we used a
Exact
double procedure: first, cross-sectional, where
age
Girls Boys Girls Boys the extreme values of the distributions which
6 101 109 differed significantly from normality were
7 96 116 separately verified; and then longitudinal,
8 1181 128' where bivariate scatter diagrams of each mea-
9 122' 130'
10 113 117 113 111
sure against the same measure one year later
11 103 108 95 104 were examined. The latter were particularly
12 93 100 82 94 sensitive to technical errors. The final size dis-
13 90 97 67 78 tributions were normal a t all ages, with the
14 86 90 58 72
15 68 83 46 63
exception of boys' head width, which showed a
16 42 53 consistent hut small positive skew. Our veloc-
17 31 53 i t y distributions, as others have found
18 24 46 (Taranger, '761, tended not to be normal. The
1 Samples augmented by new members deviations, positive skew and kurtosis, were
not marked, except for the head measures a t
older ages, where growth has, in fact, nearly
taken all children for which such an age might ceased.
be estimated, we would have had a sample RESULTS
biased towards early puberty, for a proportion Chronological age
of those with a later puberty would have left Figure 3, which shows mean growth curves
the sample before the age could be deter- of head length and of stature, uses methods of
mined. The necessary restricted sample, with presentation common to most of our figures.
a pre-defined complete sequence of' results, The left-hand scale is a proportional one, with
consisted of 73 girls from the first cohort, ages the boy's size at 18 years of age, for head
6 to 15 years, and 47 boys from the second length or for stature, taken as 100%.All other
cohort, ages 10 to 18 years. values for the relevant measures are ex-
The samples were confined to children pressed as a percentage of this figure. On the
with a t least three out of four grandparents right-hand side are separately the absolute
French-Canadian, originating from, a t the
start of the project, Montreal or its suburbs.
REL&TlVE ABSOLUTE
Parents of children in schools, chosen to repre- SIZE SIZE

sent different socio-economic areas of Mon-

treal, were approached. Only those willing to
volunteer for such a project could be recruited.
However, our sample did contain the correct
proportion of children with fathers in manual
occupations, thus avoiding the substantial
middle-classbias which has affected a number 85 -
of longitudinal studies.
Stature was measured with a Harpenden 80-

stadiometre; head length and width, which

were maximum measurable values, with a 15 .
Gneupel sliding caliper. Three anthropome-
trists have worked a t the Centre: using the 70 -

different cohorts, we have been able to com-

pare their mean measures for children of the 65'

same age, and also to examine the correlation

between adjacent ages for the same cohort. L, 1
6
' '
8
' '
10
' '
12
' '
14
' '
16
' '
18
I
Stature and head length showed no disquiet- - BOYS
AGE

ing features; head width was marginal, with ..... GIHLS

one pair of anthropometrists but not the other, Fig. 3 Mean growth curves for head length and
showing a significant, although small, dif- stature of Montreal boys and girls.
386 B. BAUGHAN AND A. DEMIRJIAN

scales, in centimetres, for the two measures. RELATIVE

SIZE
ABSOLUTE
SIZE
The figure shows that the sexual dimorphism
in stature is about 1%until puberty, when,
after a short period during which the girls HEAD LENGTH
X HEAD WIDTH
level with the boys, but do not, in our sample,
overtake them, it quickly widens again to a
final value a t 18 years of age of nearly 8%. -250
Head length, where the curves have a marked-
ly different form, already shows a dimorphism -260

of between 2.5%and 3%,prior t o puberty. That 140-

HEAD
LENGlH
the difference narrows to 2%during the puber- HEAD
X

tal period, widening again to about 4% at 18, WIDTH

gives a preliminary indication of pubertal 130 -

fluctuations in growth rate for this measure,
though of a minor nature. The data for head 120-

width produced almost identical results to STATURE

those of figure 3 and they are not shown sepa-

rately.
6o
L : ' ; ' ; o * ; 2 c ; 4 ' ; 8 ' : 8
I
The literature (Mackinnon e t al., '56; De- - BOYS AGE

kaban and Lieberman, '64;Haack and Mei- ...... GIRLS

hoff, '71; Olivier and Tissier, '75) gives many Fig. 4 Mean growth curves for the product head
formulae for the estimation of cranial capaci- length X width, and for stature, of Montreal boys and
girls.
ty, from dry skull or X-ray measures. They are
all of the form:
Volume = K X (length X width X height) + C
stant to produce true volume figures is of little
where the specific measures of cranial length, import in a comparative study.
width and height vary considerably, and with Figure 4 shows that this product exhibits a
them the values of the constants K and C . sexual dimorphism of 5% prior to puberty, nar-
Unfortunately, none of the combinations of rowing to 4% during the pubertal period, and
measures in the literature coincides exactly finally widening to just over 8%at age 18. If
with those available to us, nor were the equa- one was expecting a close proportionality be-
tions standardized on children. However, cra- tween an indicator of cranial volume and
nial height varies little after 6 years of age stature, then it is clear that this is what is
and shows only a small sexual dimorphism. found for these two dimorphisms at age 18.
Table 2 gives our results for the height of the Just as it is clear that the cranial differences
vertex above the sellanasion plane, measured are present from an early age, while those for
from lateral head X-rays, for some age groups height are not.
of the Montreal sample used in the anthropo- Figure 5 shows the mean growth velocity
metric study. This suggested that the simple curves for head length, head width and for
product, head length x width, important in head length X width, compared to those for
its own right, might also be regarded as an stature, displayed in the same proportional
adequate, though not perfect indicator of cra- fashion as the growth curves of figures 3 and
nial volume. That we lack the conversion con- 4. These show that the growth velocities in
head length and head width are of the order of
TABLE 2
l%, or less, of the 18-year-oldsize per year, and
that for head length X width only occasional-
Distance. in cm, of the vertex above the sella-nasion plane ly rises to 1.5% per year. For stature prior to
for boys and girls between 6and 18 puberty, the growth velocity is 3%of the 18-
Girls Boys year-old size per year, while during the puber-
Exact
age N Mean S.D. N Mean S.D.
tal period it rises to about 4%. The existence of
the pubertal spurt in stature is evident, even
6 45 10.31 0.37 47 10.37 0.41 from those mean curves. For the cranium, the
10 48 10.39 0.37 48 10.60 0.46 curves again indicate the possibility of a
14 48 10.52 0.46 49 10.62 0.51
18 22 10.60 0.53 42 10.79 0.57
pubertal spurt, but of a minor nature.
Table 3 quotes selected standard deviations
 SEXUAL DIMORPHISM IN THE GROWTH OF THE CRANIUM 387
TABLE 3

Standard deviations at selected ages of measures presented in figures

Head
Stature Head length Head width length x nidth
Exact (cm) (cm) (cm) icm)
age
Girls Boys Girls BOYS Girl8 Boys Girls Boys

6 4.83 4.62 0.67 0.70 0.42 0.55 10.49 13.59

10 6.25 5.86 0.61 0.71 0.46 0.49 11.80 13.16
12 6.52 7.00 0.61 0.71 0.50 0.48 12.56 14.13
14 5.47 8.79 0.61 0.76 0.48 0.50 12.82 15.59
18 6.18 5.99 0.65 0.75 0.36 0.60 9.74 17.50

RELATIVE P.ESOLUTE
VELOCITY RELATIVE ABSOLUTE
VELOCITY YELOCITY VELOCITY
' ' ' ' ' ' ' ' ' ' ' '/O/YR,
' I " " " " ' "

:j
STATURE
,PA/,, STATURE
CM/YR

5 -
STATURE
;.\
STATURE
I - .+.. 7- 4-

b-
......... 5-
3 . ..............
6-

HEAD 5-
LENGTH

2- '-44 C M P
3-
HEAD LEffiTH -0.3

2-42

...............
............ 1-41

0 - 1 ' 8 3 ' 8 " ' 8 '..*."I 0-0

HEAD WIDTH

..................................

HEAD LENGTH X HEAD WIDTH

......................................
..........

- BOYS AGE
AGE RELATIVE TO
AGE OF " P H Y '
...... GinLs

Fig. 5 Mean growth velocity curve8 for head length, Fig. 6 Mean growth velocity curve8 for head length,
head width, and their product, compared to those for head width, and their product, compared to those for
stature, according to chonological age, for Montreal boys stature, according to an age scale based on the age of peak
and girls. growth velocity in stature, for Montreal boys and girls.

for our measures (full tabulations for the data already defined, individual growth velocity
from which our diagrams were produced are curves for stature were drawn. From them,
available, upon request, from the authors). the age of peak growth velocity was estimated
Notables are the expected increase in vari- to the nearest three months. A new age scale
ability of stature during the pubertal period, was then constructed for each child, relative
not observed for the cranial measures, and the to this marker age. Figure 6 represents growth
anomalous increase in the variability of head velocities on this new scale. As ages on the
length x width for boys with age, which is new scale were no longer an integer number of
also shown, to a lesser degree, by the two mea- years, the data had to be grouped for plotting:
sures separately. for example, annual velocities for the years
with mid-points 0.75, 1.00, 1.25, and 1.50 were
Peak growth velocity in stature grouped and plotted a t 1.125 on the age scale.
For all members of the special sample, The mean age of peak growth velocity in sta-
388 B. BAUGHAN AND A. DEMIRJIAN

ture for girls was 11.95 years, that for boys TABLE 4
was nearly two years later, at 13.65 years. Cross-sectional analysis of variance for the index of
When the curves of figure 6 are compared cephalization by sex and by ages 6-14. Results
with those of figure 5 based upon chronologi- assembled from three separate models
cal data, it is seen that while the vague puber- Factor F DF P
tal peak for cranial growth in boys of the lat-
ter is made more definite, that of girls almost (from complete model)
completely disappears. The difference be- Sex x age interaction 0.98 8:2722 0.45
(from models with main
tween these curves and those for height is re- effects only)
markable in both sets. Sex (given age) 373.07 1:2722 <0.01
Age (given sex) 604.37 8.2722 <0.01
Index of cephalization Polynomials separately
Linear 4,831.71 1.2722 <0.01
To summarize our results, to allow a par- Quadratic 1.41 1:2722 0.24
simonious sequence of significance tests for Cubic 0.13 12722 0.72
our conclusions, and t o open the way t o fur- 4th-8th 0.34 52722 0.89
ther work, we have defined as an index of
cephalization the product of head length X
head width, divided by stature. Such an index shows that the difference between the sexes is
measures the ratio between cranial and gen- significant; that the trend with age may be
eral skeletal size and allows a precise summa- represented without significant omission as
ry of age and sex differences in this relation- linear; and that, with no significant sex-age
ship. Figure 7 shows the changes in its mean interaction, the two trend lines are parallel. A
value with sex and age. The appearance of the separate analysis, not tabulated, for the ages
diagram is striking, with an apparently linear 15 to 18 years, showed that there were no sig-
trend for both sexes between 6 and 14 years of nificant differences on sex, age or their in-
age. To verify this possibility we performed an teraction, for this period; that is, the mean
analysis of variance for the period, using index had become constant and equal for the
orthogonal polynomials t o represent age. As two sexes. Thus, the descriptive differences
the cells of the model did not contain equal that we have discussed in the last two sections
numbers of cases, three separate analyses were far from artifacts of chance.
were necessary to give proper tests for the in- This said, may we also assume that such
teraction and the two main factors. The re- simple results, useful to cross-sectional work
sults are assembled in table 4. with the index, apply t o individual, that is lon-
The analysis was cross-sectional and relates gitudinal, development curves? Unfortunate-
directly t o the data plotted in figure 7. I t ly not, as a second analysis of variance
showed. Here, in table 5, we give the results of
a longitudinal analysis for all cases with a
complete set of measures between 6 and 14
years of age. In technical terms, the same
program MULTIVARIANCE (Finn, '69)was
INDEX OF CEPHALISATION
HEAD LENGTH X HEAD WIDTH
used, but with the model now multivariate,
STATURE making use of the fact that the measures a t
- 200 different ages were repeated measures on the
same subjects.
The significant differences for sex on the
- 190 polynomially transformed variables for age,
excluding the constant term, show here a real
- 180 sex-age interaction: t h e sex differences
change with age. Further strict analysis
would require the two sexes to be separated,
- 170
but the highly significant cubic term in the
table is a strong indication that these dif-
I ,
6
, .
8
* .
10
, ,
12
, ,
14
, *
16
, ,
18
- 1.60 ferences are curvo-linear, rather than linear
- BWS
AGE in nature.
...... GIRLS Figure 8, which gives our percentile stand-
Fig. 7 Mean development curves of the index of cepha- ards for the index for girls, shows, in a simpler
lization, for Montreal boys and girls. way, the conclusions of these significance
 SEXUAL DIMORPHISM IN THE GROWTH OF THE CRANIUM 389
TABLE 5 cross-sectional standards. This difference be-
Longitudinal multivariate analysis of variance for the tween cross-sectional and longitudinal stand-
index of cephalization by sex and ages 6-14.Results ards is known for a single measure, such as
for the fsignificantl sex x age interaction only height (Tanner and Whitehouse, '761, and
Factor F DF P clinicians should note its recurrence for this
index of cephalization.
Sex: multivariate analysis
with constant omitted 6.23 8:70 <0.01 CONCLUSIONS
L e . , sex x ageinteraction)
Step-down univariate tests We started this article by suggesting that
on separate polynomials an unsolved problem might exist concerning
Linear 0.04 1:77 0.85 sexual dimorphism in human growth: our re-
Quadratic 2.30 1:77 0.13 sults show that the problem is real. Sexual di-
Cubic 26.49 1:77 < 0.01 morphism in the cranium is present from an
4th 4.34 1:77 0.04
5th 9.92 1:77 < 0.01 early age, as figure 4 clearly shows, while the
6th 0.02 1:77 0.88 major dimorphism in stature appears a t
7th 0.81 1:77 0.37 puberty. Girls, prior to puberty, as our index of
8th 0.62 1:77 0.43
cephalization summarizes, have a smaller cra-
nium, both absolutely and in relation t o
RELRTIVE IIRSOLUTE
stature, than boys of the same age. Further-
INDEX lNDEX
more, although several authors (Eichorn and
Bayley, '62; Roche and Lewis, '74; Lestrel and
135
-220 Brown, '76) have reported a pubertal spurt in
INDEX OF CEPHALISATION
cranial growth, our results (fig. 61, support
M
- 2 10 this only for boys and, more importantly, by
comparing it quantitatively with the growth
125
in stature, show that, although it contributes
- 200 to sexual dimorphism in adult cranial size, i t
120
is not its main cause.
-190
The major theoretical implication of these
115
findings would seem t o be the raising of dif-
ficult questions concerning the control of
110 - 1 80
growth. The simplistic view of the physical
child as a neuter being, who is then given a
105
- 170 hormonal jolt a t puberty, so producing the
major sexual dimorphism of adult men and
1W
women, has never been completely adequate.
- 160
Minor differences in size have been well-
Y
95
known and not inconsiderable differences in
- 160 pre-pubertal bone and tooth development have
90
3\,/: '... been established (Garn et al., '66; Perreault et
6 8 10 12 14 16 18 al., '74). A major sex difference in size prior to
ffiE
puberty, and moreover one which neatly
Fig. 8 Three individual development curves of Mon- aligns itself with differences in height which
treal girls, for the index of cephalization, presented only appear a t puberty, is much more difficult
against the cross-sectional percentile standard5 of the
index. to explain. Mother Nature is no doubt wonder-
ful, and always ends up with just the right
answer, but the problem is how?
tests and, a t the same time, illustrates the Of practical importance, i t seems to us, is
potential clinical use of the index. As the the development of clinical standards for the
index has a normal distribution a t all ages, the index. Head circumference and height have
percentiles were calculated from the standard long been used separately to monitor the de-
deviations. Plotted against this background of velopment of children: The use of a relative
cross-sectional standards are three individual standard for the two measures might well in-
longitudinal curves, all of girls with an early crease the sensitivity of that monitoring. We
puberty, which are seen not to follow the ap- hope to pursue this possibility elsewhere,
parent development canals provided by the though for full practical use it will be neces-
390 B. BAUGHAN AND A. DEMIRJIAN
sary to cover also the age range from birth to
six years, which the data presented here lack.
ACKNOWLEDGMENTS
The authors would like to thank all the per-
sonnel of the Human Growth Research Cen-
tre, who have contributed over 12 years t o the
research reported here. In particular, they
would mention the three anthropometrists
who took all the measures of the children:
Mrs. S. Demirjian, Miss N. Trudel, and Mr. C .
Magnan; Miss M. Boies, who prepared the
figures for this report, and Miss L. Pinson-
neault, who prepared the typescript; and
above all, the many Montreal families without
whose cooperation there would have been no
project at all.
This work was supported by grants from the
Department of National Health and Welfare
Canada.
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