J. Anat. (1984), 139, 4, pp. 639-651 639With 7 figuresPrinted in Great Britain

Shape changes during human fetal craniofacial growth

M. J. TRENOUTH

University Dental Hospital of Manchester, Higher Cambridge Street,Manchester Ml 5 6FH, England

(Accepted 19 April 1984)

INTRODUCTION

The importance of craniofacial growth before birth and its relevance postnatallyhas been discussed previously (Tienouth & Rabey, 1979; Trenouth & Johnson, 1980;Trenouth, 1981) together with the clinical implications in orthodontics.

It is well established that there is a large increase in size during the fetal period,but the quantitative measurement of shape has proved more difficult because thechanges involved are smaller and more gradual. Attempts to assess changes in shapehave involved the use of angles between lines joining defined anatomical points.Previous workers have found few or no changes in angular measurements (Ford,1956; Mestre, 1959; Inoue, 1961; Johnson, 1962; Burdi, 1965, 1969; Levihn, 1967).Where significant changes have been demonstrated the correlation coefficientsbetween cephalometric angles and age are of a much lower order than those betweensize and age.The apparent stability of cephalometric lines and angles has led to the hypothesis

that the geometrical shape of the face is stable (Inoue, 1961; Johnston, 1962; Burdi,1965, 1969; Levihn, 1967; Houpt, 1970). The finding of a constant facial shape inthe fetus is consistent with similar findings in postnatal cephalometric studies(Rosenberger, 1934; Broadbent, 1937; Brodie, 1941; Ortiz & Brodie, 1949; Koski,1961). There is, however, a contradiction between the cephalometric findings and thequite definite changes in craniofacial shape described by Ford (1955).

Small changes in single planes or angles which may not easily be detected in them-selves may summate to produce a significant change in shape. In an attempt to detectoverall changes in shape produced by the interaction ofmany single factors, Lavelle(1974) has used multivariate statistical techniques, which have demonstrated only a

small but systematic change in shape. However, these multivariate techniques aire notable to locate the site, magnitude and direction of changes in size or shape. Thisproblem has been overcome in the present study by using the analytical method ofmorphanalysis, which enables changes in size and shape ofimage outlines to be plottedin relation to a coordinate reference grid (Rabey, 1968, 1971, 1979). Thus, image out-lines of the fetus can be related to each other via the morphanalysis coordinatereference grid so that the exact places where changes occur can be detected.The present investigation was undertaken in an attempt to resolve the conflicting

evidence between the changes in shape clearly seen by simple observation and thestability of cephalometric measurements of shape. No previous workers have mappedthe exact changes in shape taking place during the fetal period or isolated the exactsites where growth changes occur. The accurate measurement of shape is critical inunderstanding the mechanisms involved in normal and abnormal craniofacialgrowth.

M. J. TRENOUTH

Table 1. Fetal age groups

Group Decimal age Numbernumber in years in group

1 0-15-02 102 0-2-025 143 025-03 104 03-0-35 105 035-04 106 04-0-45 6

MATERIAL AND METHOD

The material consisted of 60 fetuses derived from both spontaneous and thera-peutic abortions and preserved in formalin. They were all Caucasian in origin andwere graded 1 and 2 according to Streeter (1920). The crown-rump extended lengthwas measured in mm from the lateral radiograph and the age in years calculated usingthe equation derived by Bagnall (1976). The fetuses were divided into six age groupsaccording to the age in decimal years (Table 1).Aborted fetuses were considered to be representative of normal growth because

growth curves obtained from ultrasonic measurements in utero correlate highly withthose of fetuses ex utero (Robinson, 1973). Distortion due to formalin fixation hasbeen investigated by Birkbeck, Billewicz & Thomson (1975). They calculated theregression line for crown-rump length and biparietal diameter against crown-heellength for fresh fetuses from social abortions. This was only slightly above that pro-duced by Scammon & Calkins (1929) for formalin-fixed fetuses that aborted spon-taneously. The small differences were attributed to the formalin fixation, but as thetwo regression lines were parallel all age groups would be subject to small but equaldistortion.Records were produced using the standard analytical morphograph (Rabey, 1968,

1971, 1977 a), which was modified to take fetal material by the use of smaller earpieces and an auxiliary cephalostat for the lateral view (Trenouth & Rabey, 1979).The coordinate reference system was built into the photographic and radiographic

recording system so that only the fetus needed to be adjusted before directly com-parable records could be produced. The same ear-ear-left orbitale convention wasused as for the postnatal method (Rabey, 1968, 1971, 1979). In this convention themidpoint between the tips of the two ear pieces within the external acoustic meatiwas placed at the origin of the rectangular coordinate reference grid to produce twoelement symmetry. A third element was defined by marking the left orbitale. Thiswas constrained to lie on a reference plane fixed within the recording apparatus soas to produce three element planar freedom.

Records were produced in the form of photographs and radiographs taken of thefrontal, lateral and basal aspects. The records were traced with pen and ink oncellulose acetate sheets. The tracings were processed in the University of ManchesterComputer Graphics Unit. The image outlines were digitised in segments so that byadding them in various combinations different components of the image could beanalysed.Computer programs were used to produce the mean outlines for each age group.

This was performed both before and after size-normalisation to an equal area of30000 sq mm for the total skull outline. The location of a series of outlines on the

640

Shape changes during fetal growth

+

-x

-X

-Z

Radiograms

I PhotogramsFig. 1. Mean non-normalised outlines: lateral view (age groups 1 to 6).

coordinate reference grid enabled measurement of the variation within each agegroup in the form of histomorphograms (Rabey, 1977b). For clarity standard devia-tion lines were placed at intervals on the mean outlines so that the significance ofareas where changes occurred could easily be assessed. The mean outlines for thedifferent age groups superimposed on the analytical reference grid were plotted out.

RESULTSNon-normalised outlinesFor each of the six age groups, the mean non-normalised outlines were related to

the analytical reference frame by the standard conventions: Figure 1, lateral view;Figure 2, frontal view; Figure 3, basal view. These showed a marked increase in sizebetween the different age groups together with changes in shape, position and orienta-tion. These latter changes tended to be obscured by the large increase in size, but thetrue situation occurring with growth was represented. For clarity the standard devia-tion lines were omitted because the size changes were so large in relation to thevariation within age groups.

641

642 M. J. TRENOUTH

+Z

+Y/~

-Y

Radiograms+Z

-Z PhotogramsFig. 2. Mean non-normalised outlines: frontal view (age groups 1 to 6).

Lateral view (Fig. 1)The cranium showed a marked expansion, the occipital bone moved backwards

and rotated from near vertical towards the horizontal plane and the frontal regiondemonstrated a similar expansion and rotation. The orbit enlarged and moved for-wards above and along the X axis, whilst the nasomaxillary segment enlarged andmoved forwards beneath and along the X axis. The mandible enlarged and movedforwards and downwards and appeared to rotate first towards the vertical and thenback towards the horizontal. The soft tissue outline reflected the expansion of theunderlying hard tissues.

Frontal view (Fig. 2)The cranium again showed a marked expansion but more so in an upward direc-

tion along the Z axis than laterally. The orbits enlarged and moved laterally andupwards whilst the nasomaxillary segment enlarged and moved downwards. Theright and left halves of the mandible enlarged and moved outwards and downwardsat approximately 45° to the Y and Z axes. The hard tissue changes were again re-flected by the soft tissues.

Shape changes during fetal growth

-Y

Radiograms

-Y

PhotogramsFig. 3. Mean non-normalised outlines: basal view (age groups 1 to 6).

Basal view (Fig. 3)The cranium expanded considerably but to a greater extent along the X axis than

the Yaxis. The orbits enlarged and moved outwards and forwards, whilst the maxillaenlarged and moved forwards. The right and left halves of the mandible enlargedand moved outwards and forwards at 45° to the X and Y axes. The differential ex-

pansion of the skull was reflected by the soft tissues.

Size-normalised outlinesThe effect of size was eliminated by normalising the skull outlines to an equal area.

This left only changes in shape, position and orientation. By superimposing the meansize-normalised outlines of different age groups on the coordinate reference grid bystandard analytical methods, the changes in shape taking place during the fetalperiod were analysed: Figures 4-5, lateral view; Figure 6, frontal view; Figure 7,basal view.The differences in the mean outlines at the major sites ofchange were two standard

deviations or more. They were therefore significant on a statistical basis and repre-sented real growth changes and not merely random variation. However, because

643

+,

M. J. TRENOUTH

-Z Photograms

Fig. 4. Mean size-normalised outlines: lateral view (age groups 1 and 6).

growth is a continuous process, the range of variation was bound to overlap con-siderably, especially when the outlines were size-normalised. Also a definite and pro-gressive trend in the changes of the mean outlines was observed throughout thegrowth period measured, which was not random in nature.

Lateral view (Fig. 4)The overall shape of the skull changed from square to ovoid. This was primarily

due to a relative expansion of the cranium in the frontal and occipital regions witha marked rotation of the squamous occipital bone towards the horizontal plane.As these changes occurred in the cranium, the face rotated beneath it with a generaldownward displacement.The orbit and the nasomaxillary segment moved downwards and forwards relative

to the analytical reference frame together with the anterior cranial base, whilst theposterior cranial base moved relatively upwards so that the cranial base as a wholeflattened out.The mandible increased in relative size by upward and somewhat backward ex-

tension in the region of the ramus and condyle. As the nasomaxillary segment shifted

644

Shape changes during fetal growth

-x +x

-ZRadiograms

+zi

-ZRadiogramsRadiograms

Fig. 5. Mean size-normalised outlines: lateral view (age groups I and 2, upper Figure;4 and 6, lower Figure).

downwards and forwards relative to the reference grid, the mandible rotated towardsthe vertical axis, increasing the lower facial height in relative terms.From Figure 5, it was seen that the above changes occurred differentially. The

flattening of the cranial base occurred mainly between age groups 1 and 2, whereasexpansion in the occipital region occurred between age groups 4 and 6. The expansionin the frontal region was most marked between age groups 1 and 2 but continuedbetween age groups 4 and 6.

Frontal view (Fig. 6)The overall shape of the skull became less rounded and more ovoid due to a

relative elongation of the cranium along the Z axis and a relative flattening in theY dimension.The total height of the face increased in relative terms and the cranium became

more overlapped by the face. The orbits moved medially and upwards relative to thereference grid and appeared relatively larger while the nasal apertures increased inrelative width.The right and left halves of the mandible underwent a relative enlargement in the

645

M. J. TRENOUTH

-.

-Z

-Y

Radiograms

-Y

Photograms

Fig. 6. Mean size-normalised outlines: frontal view (age groups 1 and 6).

region of the condyle and ramus, and both moved laterally relative to the referencegrid, altering the lower part of the face from a V to a U shape.

Basal view (Fig. 7)The overall contour of the skull became less egg-shaped and more ovoid, by

relative elongation in an anteroposterior direction. The foramen magnum migratedin a posterior direction, relative to the reference grid, as the occipital region expandedin relative terms.The orbits moved anteriorly and medially, relative to the reference grid, as the

upper face migrated forwards and increased in relative size. The maxilla and man-

dible moved relatively backwards, reflecting the rotation of the face downward andbackward relative to the grid as the cranium expanded in relative terms. Again theright and left halves of the mandible showed a relative backward extension in theregion of the ramus and condyle, as well as backward rotation.

646

+y ~ ~ +

6.

Shape changes during fetal growth

Radiograms

+Yr.'+

Photograms

Fig. 7. Mean size-normalised outlines: basal view (age groups 1 and 6).

DISCUSSION

In the present study, because shape was measured analytically by relating imageoutlines indirectly via the morphanalysis coordinate reference grid, the site, magni-tude and direction of changes could be detected. Previous workers have failed tomeasure shape accurately because they were measuring angular changes betweenlines joining anatomical points defined arbitrarily, leading to the conclusions thatfacial shape is established early in fetal life and that it remains constant. In the currentstudy it is clearly demonstrated that the shape of the skull and soft tissues changesprogressively throughout growth, as do the relationships between the cranium andthe facial components.

Change in shape of the craniumThe changes observed in the shape of the cranium are almost certainly related to

the development of the brain and the neural pattern of growth. The brain stem,cerebellum and forebrain appear to have different growth curves (Jenkins, 1921;Ford, 1955; Dobbing & Sands, 1973; Tanner, 1977). The phylogenetically older

647

brain stem apparently develops more extensively at first and is then overtaken bythe cerebellum and forebrain. The phylogenetically most recent parts of the brainshow the greatest degree of enlargement.

Since different parts of the brain grow at different rates, an overall change in shapeseems inevitable. The force vectors generated by the developing bIain presumablychange in relative magnitude and direction, so altering the equilibrium of the ex-panding forces applied to the cranium, thus accounting for the observed changes inshape.The relative expansion in the frontal and occipital regions observed in the lateral

view is accompanied by the relative elongation and narrowing of the cranium as seenin the other views. This leads to an increase in cephalic index during the fetal periodwhich has been well documented by previous workers (Schultz, 1926; Scammon &Calkins, 1929; Ford, 1955). The factor responsible for the elongation of the craniumis almost certainly the development of the occipital and frontal lobes of the cerebrum.It is unlikely that the action of the temporalis muscles is important as these musclesare only poorly developed at this stage and appear to have no effect on the endo-cranial shape of the skull when removed experimentally in the rat (Washburn, 1947).

It is clearly seen (Fig. 5) that expansion in the frontal region is most marked be-tween age groups 1 and 2, but continues between age groups 4 and 6. On the otherhand, there is no backward expansion of the occipital region between age groups 1and 2 although a later more marked expansion occurs between age groups 4 and 6.This is due almost certainly to the later development of the occipital lobes of thecerebrum (Macalister, 1898) together with growth of the cerebellum, which shows adelay in development relative to the forebrain (Dobbing & Sands, 1973).

Flattening of the cranial baseThe anterior part of the cranial base together with the nasomaxillary segment

moves relatively downwards and forwards whilst the posterior part of the cranialbase moves relatively upwards so that the cranial base as a whole flattens out. Thisoccurs mainly between age groups 1 and 2 (Fig. 5) and it is probable that earlygrowth of the temporal lobes of the cerebrum is responsible for the displacement ofthe anterior cranial base.Most previous workers have found that the cranial base angle (Nasion-Sella-

Basion) opens out during growth (Ford, 1956; Mestre, 1959; Kvinnsland, 1971).Although Burdi (1965) has failed to demonstrate any significant correlation with agefor fetuses in the second trimester, he finds a significant change after subsequentlyadding mateiial from the third trimester (Burdi, 1969). Lavelle (1974), however,notes little general change in the cranial base angle but measures the Nasion-Sella-Bolton point instead of Nasion-Sella-Basion. More recently, Diewert (1983) findsno change in the cranial base angle Nasion-Sella-Basion between 7 and 9 weeks,the angulation being approximately 128°, which is similar to the normal postnatalvalue. The confusion may well have arisen because the sella moves upwards andbackwards during growth as observed in the histological study by Latham (1972) andconfirmed in the present study (Fig. 5), thereby masking the flattening of the cranialbase. Moyers, Bookstein & Guire (1979) consider angular relationships inappropriatefor studying growth because measurements using anatomical landmarks often cutacross areas of growth and remodelling, obscuring rather than revealing changes.

648 M. J. TRENOUTH

Shape changes during fetal growth

Relative displacement of the nasomaxillary segmentThe nasomaxillary segment migrates forwards relative to the other craniofacial

components in a progressive manner while maintaining the same grid orientationand decreasing in relative size. The observed nasomaxillary protrusion is consideredto be due to displacement rather than enlargement, as shown by the large anteriormigration in association with a relative decrease in size.Growth of the temporal lobes of the cerebrum with flattening of the cranial base

appears, therefore, to be the prime factor responsible for the displacement. Growthof the orbital contents and the nasal septum is considered to be of lesser importance,owing to the relative decrease in size of the latter two structures. These findings areconsistent with the view that the major sites of bone growth in the fetal maxilla arethe orbital and posterior borders, in response to displacement (Mauser, Enlow,Overman & McCafferty, 1975).Relative position and orientation of the mandibleThe mandible shows a small posterior shift, relative to the coordinate grid, with

a larger rotation towards the vertical axis, increasing the height of the lower part ofthe face. This is an alteration in the mean position and orientation of the mandibleand therefore represents a true growth change. It probably reflects the developmentand maturation of reflex muscular activity and posture which is known to occur atthis time (Humphrey, 1970; Moyers, 1975). The mandible increases in relative sizeandchanges in shape due to development ofthe ramus and condyle, enlargement oftheangle and coronoid process and development of the alveolar process. The greatest in-crease occurs in the region of the ramus and condyle as the mandible grows upwardsand backwards, whilst maintaining approximately the same anterior position. Thislends support to the theory that the condylar cartilage reacts in response to musculardisplacement of the mandible (Petrovic & Strutzman, 1972; McNamara, 1972).ConclusionFrom the present study it appears that, during the fetal period, brain growth pre-

dominates over that of the face and has a marked influence on facial shape, par-ticularly the upper part of the face. The cranial base flattens out as the brain expandsin the frontal and occipital regions, tilting the face relatively downwards and back-wards. The definitive position of the nasomaxillary segment is largely determined byrelative expansion of the temporal lobes of the cerebrum and to a lesser extent bygrowth of the orbits and nasal septum. The musculature of the lower part of the facein turn appears to adjust mandibular growth to adapt to the positioning of the naso-maxillary segment. Thus, during the fetal period, the shapes of the cranium andface change progressively in all three dimensions. The impression given by cephalo-metric studies that facial shape is stable is not supported by the present investigation,which clearly demonstrates a progressive alteration in shape with age. This may wellaccount for the wide variation in facial shape observed postnatally and play an

important role in the aetiology of malocclusion.

SUMMARY

An investigation into craniofacial growth during the fetal period was undertakenin order to measure changes in shape. Previous workers have reported little or nochange in cephalometric angular measurements, leading to the conclusion that facial

649

shape is stable, in contradiction to the changes in shape perceived by simple observa-tion. The major problem has been the development of quantitative methods whichaccurately measure shape. The analytical method ofmorphanalysis was used in orderto overcome the problem. Image outlines of fetuses were related to each other via a

rectangular reference grid. The exact sites where growth changes occurred wereplotted in relation to the coordinate reference grid and therefore could be isolated.The shape of the head was found to change progressively in all three dimensions

during the fetal period. The impression given by cephalometric studies that facialshape is stable was not supported by the present investigation, which clearly demon-strated a progressive alteration in shape with age. It appeared that brain growth pre-dominated over that of the face during the fetal period. This not only produced analteration in the shape of the cranium, causing its elongation, but influenced theposition of the nasomaxillary segment to which the musculature of the lower facein turn adjusted mandibular growth.

I should like to thank Dr J. S. Johnson for his advice and encouragement duringthis study and Dr G. P. Rabey for his constant guidance and for the use of thefacilities at the International Centre for Morphanalysis. I am also indebted toMr Ray Miller-Lawson for technical assistance in recording the morphographs,Dr R. J. Hubbold, Mr A. C. Arnold and Mr W. T. Hewitt for their help in theComputer-Graphics Unit, and Mr W. N. Bennett for writing the programs forcentroid analysis.

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