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Developmental changes in the facial soft tissues.

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AMERICAN JOURNAL OF PHYSICAI, ANTHROPOLOGY 79281-288 (1989)
Developmental Changes in the Facial Soft Tissues
P.H. BURKE AND C.A. HUGHES-LAWSON
Department o f Child Dental Health, University of Sheffield, School of
Clinical Dentistry, Sheffield. S10 2SZ. England
KEY WORDS
Craniofacial growth, Cephalometry, Somatic growth
patterns, Neural patterns
ABSTRACT
Short-base stereophotogrammetry was used to study differential growth and development of the soft tissues of the face. Thirteen facial
parameters were measured a t ages 9, 11, 13, 15, and 16 years on 170 facial
contour maps selected from a mixed longitudinal study of 26 boys and 26 girls.
Each parameter was measured three-dimensionally, and its developmental
progress a t the earlier stages was expressed as a percentage of its value at 16
years of age. Standing height development was assessed in the same way.
Three parameters that measured soft tissues surrounding the eyes grew little
but were very advanced in their development, following a “neural” pattern. The
remaining facial parameters grew more but were less advanced, and standing
height was least advanced. There appeared to be three separate patterns of
development, “neural,” “facial,” and “skeletal.” Girls were, in general, smaller
than boys, but their development was more advanced when measured as a
percentage of size at 16 years compared with boys.
Craniofacial growth and development presents complex patterns that have been studied in the main by cephalometry, a method
introduced by Broadbent in 1931 and followed up with a serial report in 1937. At
about the same time, Zeller (1939)published a
contour map of a face a s a n example of shortbase stereophotogrammetry. The accurate
photography needed in cartography, which
uses overlapping aerial photographs to produce three-dimensional contour maps of terrain, could be applied to the face and was
used by Thalmaan-Degen (1944), Bjorn et al.
(1954), Haga et al. (1964), and Berkowitz and
Cuzzi (1977) to measure facial change in
three dimensions. The complexity and expense of the plotting machinery discouraged
its wider use. However, a simpler system was
evolved (Beard and Burke, 1967), and its
accuracy was investigated (Burke and Beard,
1967; Burke, 1971). This system was used to
study facial growth. Serial study suggested
the presence of a n adolescent growth spurt in
the soft tissues of the face (Burke and Beard,
1979). Some of the records from this study
were used for the present investigation.
Previous knowledge about development of
facial soft tissues has either been obtained by
direct measurement, e.g., Davenport (1939),
6 1989 ALAN R. LISS, INC
Meredith and Higley (1951),Meredith (1960),
and many others, or was derived from the
soft tissue midline profiles on serial cephalometric radiographs, e.g., Subtelny (1959),
Posen (1967), Roos (1974), and Bishara et al.
(1985). These studies revealed late facial
development in the increasing convexity of
the midline soft tissue profile when the nose
tip was included in its measurement. Subtelny (1959)correlated the soft tissue changes
with the underlying skeleton and showed
that changes in the soft tissues do not reflect
directly the skeletal changes. None of these
studies included parameters of facial width.
The aim of the original study was to investigate any relationship between growth of the
soft tissues of the face and adolescent somatic
growth as measured by standing height.
Facial maps (Fig. 1)were plotted to allow retrospective study of any aspect of facial soft
tissue growth found to be of interest at a later
date. The cost of the maps became prohibitive, and the present system measures “x,y,z”
coordinates of the landmarks (Burke, 1984).
To the initial group of 13 nonoverlapping
parameters were added eight further paramReceived June 2. 1987; revision accepted September 30, 1988.
282
P.H. BURKE AND C.A. HUGHES-LAWSON
Fig. 1. Contour map of the face with a contourinterval
of 2 mm posed with the Frankfort plane coincidental with
the plane joining the central rays of the stereometric
camera.
4
eters, to extend the range of measurement.
From this group of 21 parameters all oblique
parameters were excluded, leaving 13parameters, all vertical (or near vertical) or horizontal (Fig. 2), to simplify analysis of the
findings for the changes of facial growth and
development.
MATERIALS AND METHODS
The data for this study were derived from a
selection of 170 facial maps selected from a
mixed longitudinal study of 26 boys and 26
girls between the ages of 9 and 16 years
(Burke and Beard, 1979).
The technique for recording the stereo pair
of facial photographs has been reported
(Burke and Beard, 1967). The subject was
supine, and the face was posed by means of
-2-
6
/
T P-TI
l3
12
1
\&/
5--
7
4
X
Fig. 2. A selection of three-dimensional linear facial
parameters based on soft tissue anatomical and olottinaiandmarks.
283
FACIAL SOFT TISSUE CHANGES
TABLE 1. Means and standard deviations of 13 facial parameters in mm and standing height in cm for boys at 9,
1 1 , 13, 15, and 16 years of age
Parameter
1
2
3
4
5
6
7
8
9
10
11
12
13
Standing
height
9 (n = 8)
30.3 f 2.4
27.6 f 1.7
27.1 f 1.7
33.1 f 1.3
45.8 f 3.1
30.4 f 1.6
28.8 f 3.2
16.1 f 3.8
16.9 f 3.4
62.2 f 4.8
62.8 i 4.7
85.4 f 8.6
82.2 f 4.0
134.6 f 6.4
11 (n = 14)
Ape
- in vears
"
13 (n = 21)
15 (n = 17)
16 (n = 16)
30.5 k 2.3
28.4 k 2.7
28.8 f 4.1
34.4 f 2.4
47.2 f 2.3
31.9 2.3
29.9 i 3.5
15.6 f 3.0
18.4 f 3.8
63.7 f 5.0
63.7 f 4.4
85.8 f 6.2
84.0 f 5.9
140.2 i 6.6
30.8 f 2.2
29.5 f 3.5
28.4 f 2.6
38.4 f 2.4
48.1 f 1.2
33.4 3.3
32.3 f 4.4
16.4 f 3.9
19.7 f 3.8
66.9 f 5.5
66.4 f 5.6
92.0 i 9.2
86.6 f 5.8
155.6 f 8.7
31.8 f 2.1
29.5 k 2.0
29.2 f 1.9
39.5 f 2.7
51.0 f 4.8
37.1 f 3.0
33.0 f 3.0
17.9 f 4.8
21.8 f 4.2
70.9 f 4.0
70.6 f 3.8
98.0 k 7.8
88.4 i 5.4
169.2 f 6.7
31.6 i 2.8
29.6 i 2.4
29.2 1.9
39.6 f 2.9
51.1 i 3.5
37.2 i 2.3
33.6 f 3.4
15.7 2.8
21.8 f 2.9
71.2 i 2.8
71.0 i 3.3
97.8 f 4.4
88.0 f 4.2
172.4 f 5.4
+
ear rods and a n optical pointer, locked at the
same level as the ear rods, to focus on to left
orbitale, which is marked on the face. In this
way, the Frankfort plane was aligned with
the plane joining the axes of the two optical
systems in the camera.
The maps were measured a t ages 9,11,13,
15, and 16 years, and the numbers of children
in the different age groups are given in
Tables 1 and 2. The numbers of maps measured for boys and girls were 76 and 94,
respectively. The maps were life size with a
contour interval of 2 mm (Fig. 1)and included
the eyes, nares, and mouth, extending in
depth 50 mm from the tip of nose, which was
given zero value. All children were healthy
like-sexed twins of European descent. The
value for 16 years for each parameter was
*
*
*
given 100%status, and the percentage value
for the various parameters at the other ages
measured their relative growth and development.
The selection of facial parameters was controlled by the availability of soft tissue anatomical landmarks, which can be recognised
with reliability when the overlapping facial
stereo pair of photographs are projected to
form a three-dimensional image of the face. It
is important to realise that linear parameters
defined by two landmarks within the plot are
not subject to a posing error. A posing displacement results in the contours being recorded differently, but they compensate
exactly to record the same distance threedimensionally. To reduce location error of tip
of nose this landmark was plotted four times
TABLE 2. Means and standard deviations of 13 facial parameters in mm and standing height in em for girls at 9,
1 1 , 13,15, and 16 years of age
Parameter
9 (n = 6)
11 (n = 20)
Age in years
13 (n = 20)
15 (n = 24)
28.2 f 2.3
25.4 i 3.9
26.8 i 0.5
32.1 f 2.0
43.0 f 3.1
30.7 3.1
27.4 f 2.4
13.7 f 2.5
18.1 f 2.5
62.1 1.3
62.0 f 2.0
16.7 f 2.5
74.8 f 3.2
133.1 f 6.4
29.7 f 2.0
27.3 f 2.1
27.1 f 1.9
33.1 f 2.8
45.5 f 3.3
31.8 f 2.6
29.0 k 2.4
14.0 & 2.2
18.2 2.5
65.1 f 2.7
64.6 3.0
82.1 f 5.5
81.0 f 3.6
143.7 f 5.8
30.2 f 2.7
27.4 f 2.6
27.8 f 3.1
34.7 f 2.6
47.7 f 3.5
34.0 i 2.6
30.1 i 1.7
14.2 f 2.2
18.3 f 2.8
66.0 f 2.3
65.6 f 2.3
84.8 i 5.6
83.0 t 3.8
154.0 f 6.3
31.0 2.8
26.6 f 2.3
27.7 f 2.5
35.7 2.4
47.9 2.4
34.7 i 2.8
31.1 f 2.1
13.9 f 2.1
18.8 f 3.2
66.8 k 2.4
66.5 f 2.4
87.8 k 6.0
83.0 f 4.0
161.0 f 4.4
*
10
11
12
13
Standing
height
*
+
*
+
+
*
16 (n = 24)
30.0 i 2.8
27.5 i 2.1
27.4 f 1.6
35.5 i 2.8
47.7 f 2.6
33.9 f 2.5
30.9 i 2.3
14.4 f 1.6
18.9 i 3.2
67.0 3.5
66.9 f 3.5
88.0 f 4.2
83.8 i 3.2
163.1 i 4.2
*
284
P.H. BURKE AND C.A. HUGHES-LAWSON
and mean values used for coordinates. In
view of the small facial growth velocities, the
absence of posing error was important. The
parameters used in this study are illustrated
in Figure 2 and are defined below:
1. Right internal canthus to left internal
canthus
2. Right internal canthus to right external
canthus
3. Left internal canthus to left external
canthus
4. Right external ala of nose to left external ala of nose
5. Right angle of mouth to left angle of
mouth
6. Skin overlying midpoint of intercanthal
line to tip of nose (vide infra)
7. Tip of nose to midpoint of vermilion
border of upper lip
8. Midpoint of vermilion border of upper
lip to corresponding point on lower lip
9. Midpoint of vermilion border of lower lip
to soft tissue pogonion
10. Right external canthus to right angle
of mouth
11. Left external canthus to left angle of
mouth
12. Skin overlying midpoint of intercanthal line (as in parameter 6) to soft tissue
pogonion
13. Right external canthus to left external
canthus
Soft tissue pogonion was a landmark difficult to locate in subjects with little chin prominence. In such children each individual series of maps was examined to achieve a
consistency of location relative to the pattern
of contour lines. Plotting definitions were
required for three landmarks:
1. Tip of nose: the centre of a circle of
diameter 4 mm that rests on the summit
plateau of nose tip.
2. Ala of nose: the most lateral contour line
defining the ala with a distance of 1 mm or
more on the map to the adjacent lateral contour contained within the cheek.
3. Mid canthal point: this rests on the skin
overlying the midpoint of the intercanthal
line measured on a plane parallel to the
Frankfort plane.
ence for the landmarks to give a threedimensional expression.
The values were age-corrected using the
transformation ratios on growth charts
(Tanner et al., 1966), and means and standard deviations were calculated for each
parameter for boys and girls for the ages 9,
11, 13, 15, and 16 years.
Accuracy of the method
The original analysis of variance (Burke,
1971)was based on the same face being posed
and photographed on three separate occasions, and two plots being constructed from
each facial stereo pair. The standard deviation was 0.69 mm for repeated observations
of 6 sets of 13 linear parameters (not subject
to posing error); 0.65 mm was due to plotting
error. The maps were originally measured
manually with a dial calipgauge. In this
study, the maps were measured on a digitisor
on which 200 repeated observations gave
standard deviations of 0.17 mm in “x” and
0.206 mm in “y.” The “z” coordinate of the
landmark was read from the map and fed
into the computer. If the landmark was not
on or immediately near a contour line, the
value for the “z” coordinate was obtained by
interpolation and, depending upon its distance from the two adjacent contour lines,
was estimated to a n accuracy of 0.5 mm.
Reproducibility of this value was fairly consistent, but the plotting variance in “z” still
remained, and the “z” coordinate was subject
to posing error.
To investigate the variance in “z” further,
the “z” values for all 11 landmarks were
abstracted from the six maps of the original
analysis of variance. The standard deviation
for the ‘‘z” coordinate for 24 repeated measurements of the eight landmarks from the
three stereo pairs was 0.279 mm; thus, the
variance of the “z” values was slightly larger
than those for the “x” and “y” values. The
only comparable values for three-dimensional
measurements are those of Savara and Singh
(1966),who measured bony growth of the face
three-dimensionally on lateral and posteroanterior cephalometric radiographs. All his
standard deviations of linear parameters
were greater than 1.0 mm.
RESULTS
The values of the parameters were derived
Means and standard deviations of facial
by measuring the distance between the land- parameters in millimetres and standing
marks on the maps using a n x,y,z digitiser height in centimetres are reported for the varand incorporating the contour height differ- ious ages in Tables 1 (boys) and 2 (girls).
FACIAL SOFT TISSUE CHANGES
285
TABLE 3. Relative growth expressed as a percentage of its own size at 16 years of age for the same 13 parameters
at ages 9, 11,13, and 15 years for boys and girls
Age in years
Girls
Boys
Parameter
1
2
3
4
5
6
7
8
9
10
11
12
13
Standing height
9
11
13
15
9
11
13
15
96
93
93
84
90
82
86
100
78
87
88
87
93
78
97
96
97
89
92
86
89
99
84
89
90
88
95
81
98
100
97
97
94
99
96
100
99
94
96
94
98
90
100
100
100
100
100
100
99
100
100
100
99
100
100
98
94
92
98
90
90
91
89
95
96
93
93
a7
89
81
99
99
99
93
95
94
94
97
96
97
97
93
97
88
100
100
100
98
100
100
97
100
96
98
98
96
99
94
100
100
100
100
100
100
100
100
99
100
100
100
99
99
These values are expressed as percentages of
their sizes at 16 years in Table 3 for boys and
girls. In general, girls are seen to be smaller
than boys, but, in terms of proportional size,
are more advanced at comparable ages,
Most facial parameters grow appreciably
between 9 and 16 years. The exceptions are 1,
2, 3, and 13 (eye measurements), 8 (mouth
height), and 9 (chin height) in girls. Parameters 1,2,3, and 13may be considered as “neural” since the eyes are an extension of the
central nervous system and therefore follow
the neural pattern (Scammon, 1930).Parameter 8 measuring mouth height shows little
change in either sex, and this may be related
to the need, early in life, for a sphincter for
suckling and subsequent change of function
to a slit for access for food conveyed by finger
and thumb. The other parameter that grows
little in girls, 9 (chin height), agrees with the
recent findings of Buschang et al. (1986). All
other simple facial parameters in this study
grow well, as is demonstrated by the means
and the proportionate development when
expressed as percentages (Table 3).
The composite parameters 12 (facial height)
and 13 (facial width at eye level or biocular
width) reflect the changes of their individual
components. Facial height shows considerably greater growth changes, whereas facial
width (at eye level) shows less growth (except
for the increment between 9 and 11 years for
girls). These changes reflect the typical
lengthening of the face in the older child.
Mean percentage sizes for the two groups of
nonoverlapping parameters neural (1-3) and
facial (4-7, 9-11-but excluding 8) are reported in Table 4. Interestingly, the corresponding values for standing height are
less advanced a t all levels of development for
both sexes.
The differentiation of neural, facial, and
somatic growth patterns at 9, 11, and 13
years is graphed in Figures 3 and 4 for boys
and girls, respectively.
In boys, the developmental paths of the
facial and neural parameters are completely
separate until age 13 years when they begin
to merge. In girls, this separation is less
clearly defined at 9 years (parameter 2 is
based on a small sample size). Nevertheless,
by 11years it is complete. By 13 years a convergence of all parameters occurs. The percentage values of standing height at 9, 11,
and 13 years in both boys and girls are at
lower levels than the facial values.
TABLE 4. Means of ‘heural,” “facial,” and ‘<skeletal”
parameters at ages 9, 11, 13, and 15 years for boys
and girls
Age
(veard
Boys
9
11
13
15
Girls
9
11
13
15
Mean percentage of size at 16 years
Neural
Facial
Skeletal
94
97
98
100
85
88
96
100
78
81
90
98
95
99
100
100
92
95
98
100
81
88
~~
94
99
286
P.H. BURKE AND C.A. HUGHES-LAWSON
BOYS
GIRLS
IW
95
90
,‘
I
70
a
85
80
I
I
75’
a,’
S H
15
I
I
I
9
in
11
I
12
,
13
1
1
14
15
7
16
J
,
,
,
9
10
11
I
12
13
14
15
16
hie (Years1
A x lyearrl
Fig. 3. Relative growth at various ages expressed as a
percentage of size at 16 years, of neural, facial, and skeIetal parameters for boys.
Fig. 4. Relative growth at various ages expressed as a
percentage of size at 16 years, of neural, faciaI, and skeIetal parameters for girls.
DISCUSSION
Their conclusions were as follows: “A distinct
facial pattern of growth is established. In
terms of the proportion of final size achieved
during childhood, it is below the cranial pattern but above the general skeletal one.”
A similar study based on serial lateral
cephalometric radiographs was carried out
by Buschang et al. (1983) on 26 boys and 26
girls between the ages of 4 and 16 years. This
study revealed similar findings, namely three
separate patterns of growth and development
for neural, facial, and skeletal organs. Further, they proposed a continuous developmental gradient running from the cranium to
the upper and lower face similar to Tanner’s
(1962, 1978) suggestion for the trunk and
limbs.
The findings in this study support the concept of a developmental gradient between
neural and general somatic growth with soft
tissue facial growth following a n intermediate path. Somatic growth is characterised
by its sustained nature in the second decade
and a n adolescent spurt (Tanner, 1962). The
fact that the face appears not to follow this
pattern exactly may explain the difficulties
experienced in demonstrating a facial adolescent growth spurt on serial cephalometric
records (Broadbent et al., 1975).
Scammon (1930) was among the first
workers to draw attention to the developmental differences between the general skeletal
and the neural longitudinal growth curves.
While most of the rapid neural growth takes
place in the 1st decade of life, skeletal growth
follows a sigmoid curve until the pubertal
growth spurt, after which it decelerates and
essentially ceases as the end of the second
decade approaches. Since the face grows well
into the 2nd decade (Broadbent et al., 1975)it
has been presumed that the face follows the
latter pattern of development. Evidence for
an adolescent growth spurt has been presented by Nanda (1955), Bjork (1964), and
Savara and Singh (1966).These studies were
based on lateral and frontal cephalometric
radiographs, and Savara and Singh evaluated three-dimensional parameters.
Baughan et al. (1979) studied serial lateral
cephalometric records for 50 French-Canadian girls between the ages of 6 and 15 years
and arrived at different conclusions. Mean
size changes for cranial and facial parameters were expressed as a proportion of the size
at 15 years to measure development. Standing height was treated in the same way.
FACIAL SOFT TISSUE CHANGES
This study also reveals some coordination
between developmental pattern of parameters concerned with anatomical entities on
the face. For example, parameters 4 and 6,
which measure nasal width and nasal height,
both follow a relatively delayed path of
development compared with many other
facial parameters. In contrast, mouth width
(5) and height (8) are advanced. This is true
in both sexes, but at the age of 9 years cheek
height (10 and 11) is relatively advanced in
girls compared to boys. The growth patterns
of cheek height (10 and 11) are similar to
those of facial height in the midline (12),
while facial width growth slows down. Thus,
the differential velocity of growth of the vertical and horizontal parameters produces a n
overall change in facial shape.
These findings suggest that growth and
development of the soft tissues of the face are
organ orientated, and priority of development varies between different organs and in
time. Particular examples are the eyes and
within the face, the nose, and the mouth.
This agrees with the recent findings of Bailey
(1986) who measured genetic variation of
shape of the mandible in CXB strain of mice.
This study was based on a two-dimensional
multivariate analysis of MLDs (minimal linear distances) between anatomical points
and revealed that genetic control is organorientated, e.g., for the lower incisor area.
This also agrees with the findings of Kraus
et al. (1959) for bony craniofacial characteristics, as shown in cephalometric radiographs
in six sets of triplets.
The findings in this study provide some
support for Buschang et al.’s concept of a
craniofacial developmental gradient between
the cranium and middle third of face, but the
continuation of the gradient to the lower
third of face is supported only in boys by the
developmental pattern of the one parameter
(9), which is the only parameter to be contained entirely within this part of the face.
The results do, however, support the concept
that genetic control is organ orientated, and
further analysis may help to clarify the
position.
ACKNOWLEDGMENTS
The authors wish to thank Mr. L.F.H.
Beard, formerly Director, Department of
Medical Illustration, University of Cambridge, for his sustained help over many
years with stereophotogrammetry. They wish
287
to acknowledge, with gratitude, funding from
the United Cambridge Teaching Hospitals
Board, University of Sheffield, and the Medical Research Council of the U.K. They are
also grateful for the commercial plotting services provided by Fairey Surveys Ltd. and
Clyde Surveys Ltd.
Finally, they wish to thank the children in
the study for their patience.
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