on the cranial surface of the skull, but before ossification it has been taken as a point in the ... The maximum breadth of the foramen magnum in ..... the cranial nerves which develop in relation to it, expands laterally at the same rate as the skull.
[ 63 ] THE GROWTH OF THE FOETAL SKULL BY E. H. R. FORD Department of Anatomy, St Thomas's Hospital Medical School INTRODUCTION
Quantitative work on the growth of the foetal skull has hitherto been confined to studies of the undissected foetal head. The dried foetal skull is of limited value owing to the shrinkage and distortion produced by drying. The most important work on the growth of the foetal head is that of Scammon & Calkins (1929), who summarize the previous work on the subject. Their findings are that most dimensions of the foetal head can be related to crown-heel length of the foetus by the formula HD = aL + b, where HD is any given diameter of the head, L is crown-heel length, and a and b constants differing for each diameter. The only exceptions are the bimalar and orbito-auricular diameters. The cranium becomes longer and broader in relation to its height; the face grows relatively more in height and breadth than the cranium, and thus becomes in comparison broader. The various cranial dimensions increase five- to sevenfold from 3 months to birth. Since all their measurements are external, Scammon & Calkins are unable to analyse differential growth rates within the skull. In the present study, by analysing the growth of different parts of the foetal skull, an attempt is made to explain the changes in form which result from differential growth rates within it. MATERIAL AND METHODS
Measurements have been made on seventy-six foetuses of menstrual ages between 10 and 40 weeks, the majority of which have been preserved in formalin, the remainder (seven) being fresh. Exact histories not being usually available, ages have been assigned as follows: crown-rump length, foot length, and weight have been recorded where possible, and then the age has been assigned by means of Streeter's (1920) tables. Where there is a discrepancy between the three measurements, crown-rump length has been taken as the most reliable, and the history (when available) has also been taken into consideration. For ages between 10 and 22 weeks the foetuses have then been arranged in weekly groups (the 10-week group containing all foetuses of estimated age 10 weeks or over but less than 11 weeks) and for ages between 22 and 40 weeks in two-weekly groups (the 22-week group containing all foetuses of estimated age 22 weeks or over but less than 24 weeks). The average of all measurements of a dimension within one group has then been given as the mean for that group. All linear measurements have been made with dividers and a millimetre rule, measurements being recorded to the nearest 0 5 of a millimetre. Angular measurements have been made by placing a sheet of glass on the sagittally-sectioned skull and tracing the three points required for each angle on to the glass; the angle is then measured directly on the glass with a protractor. Some of these angles have been
64
E. H. R. Ford
checked from photographs, and the errors of measurement found to be small. Measurements of overall length and breadth and of bizygomatic diameter have been taken on the external surface of the skull after removal of the overlying soft tissues; measurements on the skull-base in the coronal plane have been made on the internal surface of the base after removal of the skull-cap, brain and dura mater; and measurements of diameters and angles in the sagittal plane have been recorded after sagittal section of the cranial base.
Points, dimensions and angles employed Where no definition of a point or dimension used is given, they are defined as in the adult skull, following the definitions given by Wood Jones (1929). Basion and opisthion. These are defined as in the adult skull, but the former is a cartilaginous point in the younger foetuses, while the latter is not always easy to define precisely owing to the completion of the posterior border of the foramen magnum by fibrous tissue. Prosphenion. This is the most anterior point of the presphenoid in the midline on the cranial surface of the skull, but before ossification it has been taken as a point in the midline between the most anterior points on the curved anterior margins of the lesser wings of the sphenoid. Pituitary point (referred to as pituitary). This is a point in the centre of the floor of the pituitary fossa. The sagittal section of the outline of the fossa is an arc, and the pituitary point is the central point on the arc. Septal point. This is the most anterior point on the straight lower border of the nasal septum, where it meets the anterior border. Septum length. The maximum length of the nasal septum. Septum height. The maximum height of the nasal septum from its lower border to the cribriform plate, perpendicular to the former. Cribriform plate length and breadth. The maximum length and breadth of the cribriform plate on its cranial surface. Foramen magnum length. The distance from basion to opisthion. Foramen magnum breadth. The maximum breadth of the foramen magnum in the coronal plane.
Measurements in relation to the otic capsule Otic capsule length. The maximum length of the otic capsule along its long axis (which is at about 45° to the sagittal plane). Interauditory diameter. The minimum distance between the medial margins of the internal auditory meatuses at their openings on the surface of the otic capsule. Minimum distance between the inner poles of the two otic capsules. Maximum distance between the outer borders of the two otic capsules on the cranial surface of the skull. Minimum distance between the posterior margins of the superior semicircular canals. Maximum distance between the anterior margins of the superior semicircular canals.
The growth of the foetal 8kull
65
Interoptic diameter. The minimum distance between the medial margins of the optic foramina at their internal openings. Interovale diameter. The minimum distance between the medial margins of the foramina ovalia. Spheno-ethmoidal angle. The angle basion-prosphenion-nasion. Foramino-basal angle. The angle prosphenion-basion-opisthion. Basioccipito-septal angle. The angle basion-pituitary-septal point. Basioccipito-foraminal angle. The angle pituitary-basion-opisthion. Note. The latter two angles have been preferred to the spheno-ethmoidal and foramino-basal angles for two reasons: (1) The prosphenion is difficult to define in the younger foetuses. (2) The point of angulation between the chordal and prechordal parts of the cranial base appear to be in the pituitary region, so that measurement of this angulation at the pituitary point gives a more direct result than at the prosphenion. FINDINGS
Between 10 and 40 weeks the overall dimensions of the skull (length, breadth, and auricular height) increase between six- and sevenfold, and there is a change in the form of the head. At 10 weeks the forehead is prominent, while the occipital region is underdeveloped and there is no clear demarcation from the neck. During growth the frontal region becomes less prominent and the occipital region develops, becoming protruberant. The external auditory meatus is thus relatively and absolutely closer to the back of the skull in the younger foetus. The skull is also higher in relation to length and breadth in the young foetus, and becomes squarer with age, due to the development of the frontal and parietal bosses. The lower jaw is more receded in relation to the upper between 12 and 20 weeks than at either the beginning or the end of the foetal period. Other facial changes will be described later.
A. Growth rates within the skull The dominant structure in the growth of the anterior cranial base is the nasal septum. This doubles its length at 10 weeks by 14 weeks, trebles it by 17 weeks; quadruples it by 22 weeks; it increases fivefold by about 28 weeks, sixfold by 36 weeks, and by birth is between six and seven times its length at 10 weeks. Nasal septum length has been found by the method of least squares to be related to crownrump length by the allometric formula, septum length=0-23 x crown-rump length0 86. Most dimensions of the prechordal part of the cranial base have the same growth rate as the nasal septum; they increase six- to sevenfold between 10 and 40 weeks, at the same rate as the septum. This applies to the following dimensions; septum height, length and breadth of cribriform plate, pituitary-prosthion, nasion-prosthion, and otic capsule length. It also applies to the overall length and breadth of the skull and to the cube root of brain weight. On the other hand, dimensions of the parachordal part of the cranial base have a lower growth rate at all periods; the value at 10 weeks is doubled by 15 weeks, trebled at 22 weeks, quadrupled at 32 weeks, and at birth is only between four and 5
Anat. 90
E. H. R. Ford
66
five times its size at 10 weeks. This applies to pituitary-basion length and to the length and breadth of the foramen magnum. The actual values for the abovementioned dimensions between 10 and 40 weeks are given in Table 4. In order to compare graphically the growth rates of the anterior and posterior parts of the cranial base, values for pituitary-nasion have been plotted against those for pituitary-basion for ages between 10 and 40 weeks (Fig. 1). A linear relationship exists between the two dimensions which can be expressed by the formula pituitary-basion = 0*48 x pituitary-nasion + 2-5 (where the values are expressed in millimetres). 25 _
20
,,
-
20
15
CL' 0
0
5
10
15
20
25
30
35
40
Pituitary-naslon (mm.) Fig. 1. Mean pituitary-nasion lengths for each group of skulls plotted against mean pituitary-basion lengths for the corresponding groups.
Since the vault of the skull and the brain are growing at the same rate as the anterior part of the cranial base, while the posterior part is growing more slowly, there will be a deficiency in the overall length of the base unless some compensatory structural adaptation exists. This adaptation is in fact a flattening of the cranial base which takes place in the following way: (1) The angles included between the septal and basioccipital parts of the cranial base, and between the basiocciput and the foramen magnum become progressively less acute. (2) The occipital squama moves to a more horizontal position relative to the anterior cranial base. These processes produce the increasing occipital fullness previously noted in the foetal period, which is particularly characteristic of man. As a result of it the posterior cranial fossa, which in the early foetus is funnel-shaped, becomes progressively broader and shallower. In order to demonstrate this flattening of the cranial base, measurements of the five angles shown in Table 1 have been made in each skull. Although there is considerable individual variation, an analysis of the variance within and between the various age-groups indicates that there is a highly significant regression with
67
The growth of the foetal skull
age for each angle (P < 0-001). On the assumption that these regressions are linear, the age changes for each angle have been calculated by the method of least squares, and the results are shown in Table 1. Details of the calculations are described elsewhere (Ford, 1955). Table 1. Changes in the angles of the cranial base with age Calculated value Calculated value at 40 weeks at 10 weeks (degrees) (degrees) 150-5 1315 122-4 104-9 149-0 135-4 143-0 120-2 135-0 109-0
Angle Spheno-ethmoidal Basioccipito-septal Basion-pituitary-nasion Foramino-basal Basioccipito-foraminal
Increase between 10 and 40 weeks (degrees) 19.0 17-5 13-6 22-8 26-0
The first three angles are all included between the prechordal and chordal parts of the cranial base, but are measured from different fixed points. The degree of change in the first two is very similar, and the discrepancy of the third is probably due to upward movement of the floor of the pituitary fossa during growth, secondary to thickening of the basisphenoid, which may mask some of the change in this angle. The latter two angles record the angulation of the foramen magnum to the basiocciput, and give comparable values. Thus between 10 and 40 weeks the angle between the prechordal and chordal parts of the cranial base opens out by 17-19°, while that between the basiocciput and the foramen magnum opens out by about 250, so producing a flattening of the whole cranial base. It follows from this that dimensions of the foetal skull such as basion-nasion, basion-prosthion, and basion-menton, which are functions of the growth of both the prechordal and the chordal parts of the cranial base, and of the angulation between them, will have a growth rate intermediate between those of the anterior and posterior parts of the cranial base, as reference to Table 4 will show. B. Lateral growth in the skull base The relative speeds at which the optic and auditory foramina, and the foramina ovalia move laterally, compared with lateral growth of the skull as a whole, is shown in Table 2. Table 2. Relative rapidity of lateral growth Overall width
Interoptic diameter
x2
14
14
x3
17 22 28 36
34
Age (weeks) at which I0iweek size is- x 4 * x5
x6
*
18
40+
Interovale Interauditory diameter diameter 13 15 16 22 32 22 40 30 40
The optic foramina move laterally at the same relative speed as the skull as a whole up to 18 weeks, but thereafter their rate of separation from each other is markedly slowed; this is related to the fusion of the orbito-sphenoids with the presphenoid, after which movement of the foramina can only take place by 5-2
68
E. H. R. Ford
differential absorption and accretion of bone at their margins, so that they move relatively closer to the midline. The foramina ovalia move laterally at the same relative speed as the skull as a whole up to about 20 weeks. Their lateral movement is slower in the succeeding 6 weeks, after which they again move laterally at the same relative speed as the skull as a whole. The auditory foramina also grow laterally at the same speed as the skull as a whole up to 18 weeks when the otic capsules ossify; after this they come to lie progressively closer to the midline, maintaining a constant relationship to the foramen magnum which is expanding more slowly than the skull as a whole, and is therefore becoming smaller in proportion to overall skull size. C. Growth of the otic capsule The measurements previously described between the two otic capsules at various points, and the interauditory diameter, have been halved to give the distance of each of the points concerned from the mid-sagittal plane. Since the angle which the long axes of the two otic capsules make with each other is about 90° throughout the foetal period, the distances at these points from the midline is proportional to their distance from each other along the long axis of the otic capsule. The results obtained are summarized in diagrammatic form in Fig. 2.
E E
E
0
30-
20
-
13
~~A
10
20 30 40 Weeks Fig. 2. Diagram of the growth of the otic capsule and petrous temporal bone, showing the distances from the midline of the points described in the text at ages between 10 and 40 weeks. The alteration of the mode of growth which takes place at the time of ossification can be seen. 10
Up to about 18 weeks the otic capsule grows interstitially in cartilage at the same rate as the enclosed internal ear. At 18 weeks the latter has attained virtually its adult size (Bast & Anson, 1949), the capsule is rapidly ossified throughout, and interstitial growth ceases. The petrous temporal bone has to increase in size to
69
The growth of the foetal skull
fulfil its secondary function of providing a floor for the skull; this is done by addition of bone at its lateral and medial ends. The bone added laterally, which is much more than that added medially and which amounts at birth to more than half the total length of the bone, is added from growth cartilage which is present at the posterolateral margin of the bone and represents the most lateral part of the otic capsule, which remains unossified, plus that part of the tectum posterius which is attached to the postero-lateral margin of the otic capsule. The bone added medially, however, is laid down from the periosteum, the cartilaginous bridge which originally joined otic capsule and basisphenoid having been by this stage replaced by fibrous tissue. As a consequence of this mode of growth the internal ear comes to lie relatively nearer to the median plane during the last 20 weeks of prenatal life. D. Facial growth Comparison has been made of upper facial height (nasion-prosthion), facial depth (represented by nasal septum length) and facial width (bimalar diameter). Means of all measurements in the groups 10-15, 16-20, 21-30 and 31-40 weeks have been taken, and Table 3 gives the ratios of the dimensions to each other for each group.
Table 3. Changes in facial proportions with age Age group (weeks)
Depth
10-15
Height 1*30
16-20 21-30 31-40
1-32 1.15 1-23
Width Height 1-92 2-26 2-13 2-30
Width Depth 1-58 1-75 1-89 1-93
This indicates that width is increasing in relation to both height and depth, while height is also increasingin relation to depth. The increase in height relative to depth is due to the growth of the alveolus, since facial height is compounded of septum height and alveolar height, and it has been seen that the proportions of the nasal septum are constant during the foetal period. The relative increase is not as marked as might be expected, and this is due to slight movement downward of the nasion relative to the nasal septum. The even greater relative growth in width is related to orbital development. In order to study prognathism the values for the angle pituitary-nasion-prosthion have been analysed, and it has been found that there is no statistically significant change in the angle with age, the mean value being about 78°, although there is a slight tendency for the value to increase in the last 10 weeks, due to alveolar development. This implies that the degree of true (as opposed to alveolar) prognathism of an individual depends on the position of the alveolus in relation to the nasal septum, and that this is fixed by the beginning of the foetal period. The dimensions basion-prosthion and basion-menton have been compared, and it has been found that basion-menton length is relatively less in relation to basionprosthion length between 12 and 20 weeks than before or after this period. This corresponds to the period at which the lower jaw is obviously receded in relation to the upper, and is related to the development of the secondary cartilages of the
mandible.
E. H. R. Ford
70
Table 4. Mean values of certain dimensions of the foetal skull for age-groups between 10 and 40 weeks (All diameters expressed in millimetres)
E E . |i
-6a~~~~~~~~~~~~
Ce
a~~~~~~~~~~4 a; bL ~
10 1-
~
~
191
~
15
a
~
1--
-
a
a
6-
a
27 2211 28-25 23 34 27-5
-:
2 -6a 8
5¢527
18-5 8-5 16 3-5 18-7 9-25 4-75 5.5 21 11 6 36-5 29.5 22-2 13 35-25 25-3 14-5 6-5 43 6-5 40 34-5 16 50O 8 50 39 5 31-5 18 42 52 34-5 18-5 8 - 20 9-5 54 42 9-5 56 49 38-5 19 925 64 49 42-5 21 75 61 45-5 23-5 10-25 24 12 75-25 25 47 26 12 85-5 67-5 54 58-5 28-5 13 945 73 32 98 74-5 64 30-5 14 16 76 -32 34 101 -341 5 16 36101-5 79-5 16 69-5 34 38 108 80 16 73-5 35 40 110 87 12 13 14 15 16 17 18 19 20 21 22 24 26 28 30
3
a
-6-
-000,
6-7 a
5
4-5 5.5 6 7
7.5 8-75 10-25 10-5 10 11 12 13 14-25 11 13
16 15 15-5 15-5
4-7
0
10-5 10
45 6-5 7 9 10-5 11 13
-
a
6 8-5 8-5 10 12 4 14-5 15-5 13 17-5 4-5 16 16-5 19 21 5 6 19-5 21 13-5 15-5 23 14-75 16 6-5 21 14 15 6 22 23 17 16 6 24 26 16-75 25-25 19 7-5 25 20-25 705 255 285 20 21-5 8-5 28-5 31.5 21 9 24 31 33.5 23 2 8 32-5 385-5 24 27 825 325 36-5 25 30 9 36 38-5 27 26 34 9 537 41 2 275 35 10-5 10-5 40 30 36-5 46 3
3-75 10-75 11 4.5 13 14
0
10-7
g¢
10 13 14-75 17-5 21 22-5 25-5 24-5 33.5 29 34 29
11-5 15 17-75 21 24 25-5 28 29-5
8-55.55
9 11-5 12 14 17 19-5 18 23-75
6 75 8-5
8-5 11-5
-
5-5
4-5
6-5
5-5
8-5
2 2 1 3 3 1 2 2 1 1
6-5 7-5 8-5 9 7*5 8 12 10 11 11 9 24-5 13-75 12-75 9 14 15 10 22 13 27 13-511 35-531 15-5 145 11-5 2 37 32 28 2 12 16-5 15 41 34-5 31 17 17 12-5 3 44175 39 34 18 17-5 13-5 2 45 41 37 3 4 14 19-5 20 215 40 7 20 14 46 42-5 20 50 8 15 20 21 53 47 44 4 20 21 17 54 50 47 13 22 18 55.5 53 495 20 11 24 21 595 57 52-5 22 10-5
DISCUSSION
The observations on the relative growth rates of the prechordal and chordal parts of the cranial base supplement those of Ortiz & Brodie (1949) who found that in the newborn baby growth in the anterior part of the cranial base is more rapid than in the posterior part. The growth rates appear at first to contradict the law of developmental direction which states that, in general, development (including growth and differentiation) in the long axis of the body appears first in the head region and progresses towards the tail. Since the growth rate of any part or organ is highest when development begins, and declines progressively with age, parts more recently developed will be growing relatively more rapidly at any given stage of foetal development than parts developed earlier. The more rapid growth of the prechordal part of the cranial base implies that it develops later than the chordal part. This does not contradict the law if it is assumed that this is reversed for the prechordal part of the skull as Kingsbury (1924) has suggested, on qualitative studies, that it may be; since the anterior end of the notochord marks the primitive rostral extremity of the head, the prechordal part of the cranial base is both phylogenetically and ontogenetically more recent than the chordal part, and this accounts for its more rapid growth at any given stage of development. The law may thus be amended to state that development commences at the anterior end of the notochord, and progresses both rostrally and caudally from that point.
The growth of the foetal 8kull
71
The changes in the angles of the cranial base in foetal life are brought about mechanically by the expansion of the cranial contents; since the growth of the posterior part of the cranial base is slower than that of the brain, flattening of the cranial base must take place in compensation. If the mechanical force of brain expansion is absent, as in anencephalus, or is reduced, as in microcephalus, the angle between the prechordal and chordal parts of the cranial base often remains a right angle, as in early foetal life (Augier, 1931). In post-natal life the pre-natal change is reversed in man and most primates (Duckworth, 1915), the foramino-basal angle becoming smaller. This again is probably for mechanical reasons, the growth of the cranial base, particularly at the spheno-occipital junction, being more prolonged than that of the brain, and so partially reversing the earlier changes. It has been seen that the chondrocranium, with those foramina for the cranial nerves which develop in relation to it, expands laterally at the same rate as the skull as a whole up to 18 or 20 weeks, but thereafter comes to lie relatively closer to the midline; this reflects the more rapid growth of the cerebral hemispheres at this time compared with the brain-stem, from which most of the nerves are arising. Owing to this rapid cerebral expansion most of the growth in width of the base of the skull after 20 weeks takes place laterally in the membrane bones. The dominant feature of facial growth during foetal life is the cartilaginous nasal capsule. The position of the upper alveolus in relation to the nasal septum is already fixed by early foetal life, so that the degree of true (as opposed to alveolar) prognathism does not alter during foetal life. The position of attachment of the alveolus to the nasal septum is characteristic in man, being relatively less rostral than in other primates; this is due to the small size of the premaxilla, and to its early fusion with the maxilla, and it explains the projecting nose and prominent nasal spine of man. In other primates the premaxillae grow forward beyond the nasal septum, which becomes submerged in the face. The recession of the lower jaw which is conspicuous between 12 and 20 weeks is related to the mode of growth of the mandible. In the early foetal period forward growth of the mandible is due to the growth of Meckel's cartilage; as development proceeds this becomes smaller and less important, and the phylogenetically and ontogenetically more recent temporo-mandibular joint and secondary cartilage of the mandibular condyle are developed, from which most of the future forward growth of the mandible takes place. It is during the period when Meckel's cartilage is becoming relatively small and insignificant, whilst the mandibular condyle has not fully assumed its growth function, that mandibular growth lags behind that of the upper jaw. If there is interference with growth at this stage the temporary inequality in the positions of the two jaws may become fixed. SUMMARY
1. The growth of the foetal skull between 10 and 40 weeks has been studied by measurements on a series of dissected formalin-preserved foetal heads. 2. Overall skull size, brain size and the anterior (prechordal) part of the cranial base increase between six- and sevenfold in linear dimension between 10 and 40 weeks, while dimensions of the posterior (chordal) part of the base only increase
72
E. H. R. Ford
between four- and fivefold. To compensate for this slower growth of the posterior part of the cranial base, the angles between the pre- and para-chordal parts of the base, and between the basiocciput and the foramen magnum, become flattened, resulting in increased prominence of the occiput. 3. The parts of the cranial base derived from the chondrocranium come to lie relatively closer to the midline after 18-20 weeks. Growth of the otic capsule is described; this, after ossification, grows mainly at its postero-lateral end from growth cartilage, but there is some subperiosteal accretion of bone at the anteromedial end. 4. Facial width increases relative to both height and depth, while height also increases relative to depth, but the degree of prognathism remains constant. Growth of the lower jaw lags behind that of the upper between 12 and 20 weeks while the condylar growth centre is not yet fully developed.
This work was made possible by a grant from the St Thomas's Hospital Endowment Fund. I am grateful to Professor D. V. Davies for providing facilities and material for the work, and also to Professors R. E. M. Bowden, J. D. Boyd, R. J. Harrison and R. D. Lockhart for foetal material. In the statistical analyses I was advised by Mr M. J. R. Healey of the Rothamsted Research Station, who also did most of the computations, for which I am very grateful. I also wish to thank Mr G. A. Wooding for carrying out the photographic work. REFERENCES AUGIER, A. (1931). In Poirier & Charpy, Traite d'Anatomie Humaine, 4th ed., Tome 1, Fasc. 1, p. 627. Paris: Masson et Cie. BAST, T. H. & ANSON, B. J. (1949). The Temporal Bone and the Ear, p. 245. Illinois: Charles C. Thomas. DUCKWORTH, W. H. L. (1915). Morphology and Anthropology, 2nd ed. vol. I, p. 232. Cambridge University Press. FORD, E. H. R. (1955). The growth of the foetal skull. M.D. thesis, University of Cambridge. KINGSBURY, B. F. (1924). The significance of the so-called law of cephalocaudal differential growth. Anat. Rec. 27, 305-321. ORTIZ, M. H. & BRODIE, A. G. (1949). On the growth of the human head from birth to the third month of life. Anat. Rec. 103, 311-333. SCAMMON, R. E. & CALKINS, L. A. (1929). The Development and Growth of the External Dimensions of the Human Body in the Fetal Period. Minneapolis, University of Minnesota Press. STREETER, G. L. (1920). Weight, size, and age of human embryos. Contr. Embryol. Carneg. Instn. 11, 143-170. WOOD JONES, F. (1929). Measurements and landmarks in physical anthropology. Bull. Bishop Mus., Honolulu, no. 63. Hawaii.
