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Developmental changes of the cranial bone thickness in the human fetal period.

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Developmental Changes of the Cranial Bone Thickness in
the Human Fetal Period
FUMIO OHTSUKI 2
Department of Anatomy. The Jikei Uniuemity School of Medicine,
Nishishinhashi, Minato-ku, Tokyo 105, Japan
KEY WORDS Fetus Cranial bone . Growth of thickness
Allometric analysis . Bilateral difference.
ABSTRACT
The description of the developmental changes of cranial bone
thickness in the fetal period is the primary aim of this paper.
The materials utilized in this study consisted of the two series. One is those of dry
bones of 62 Japanese fetuses ranging from the fifth month to term and the other is
those of 56 Japanese fetuses ranging from the fourth month to term.
The first series is mainly used for the tests of bilateral difference in the thickness
of cranial bones. No statistical significance could be found. Allometry technique
was then applied for the analysis in the growth of the thickness of cranial bones and
an extremely positive allometric coefficient was obtained. This required us to study
another material, i.e., the second series. The materials of the second series were
first measured for crown-rump length, head length, head breadth and head circumference. The heads were then carefully dissected and the left side of individual
bones of the cranium were removed to take further measurements for the arc
length. The thicknesses at the ossification centers and midpoints were successively
measured by a micrometer readable to 0.01 mm. The results of the second series
were investigated from the viewpoint of absolute and relative growth. By
allometric analysis, vertical and transverse arc lengths were found to be isometric
with two exceptions, while every measurement of thickness shows an extremely
positive allometry. This coincides with the results of the first series.
Gross structural and quantitative
changes of the skeleton in human pre- and
circumnatal periods have been described
in detail. Studies confined to the development of fetal cranial bones were undertaken by Augier ('13, '311, LaCoste ('311,
Inman ('341,Inman and Saunders ('371, Noback ('431, Moss ('551,Moss et al. ('561,fino
('571, Nishida ('591, Misaki ('59a,b1, Koura
and Yokota ('601, Kobayashi and Inoue
('61), Moss ('641, Ohtawa ('671, Kawarada
('681 and others. These researches are
generally concerned with the determination of the normal number and the time of
appearance of ossification centers and/or
the developmental anatomy of one or more
individual bones.
AM. J. PHYS. ANTHROP., 46; 141-154.
Functional anatomists have stressed that
the morphology of the head is the resultant
not only of bone growth but of the integral
growth of all its components, namely,
brain, meninges or viscera (Inman, '341.
Therefore, isolated cranial growth data
become meaningful only in the context of
correlation with the growth of other structure (Moss et al., '56; Moss and Young, '611.
The literature, however, reveals a
dearth of information on the thickness of
cranial bones. In this paper developmental
' A part of this paper was read before the 77th Annual
Meeting of Japanese Association of Anatornistr in Kagoshima
on March 1972.
Present address Faculty of General Education, Tokvo
University of Agriculture. and Technology. Ilarumiclo,
Fuchushi, Tokyo 183,Japan.
141
142
FUMIO OHTSUKI
changes of cranial bone thickness and
bilateral difference of them in the fetal period are described.
MATERIALS AND METHODb
The materials utilized in this study consisted of two series. One is the dry bones of
62 Japanese fetuses ranging from the fifth
month to term (subsequently termed "dry
bone series") and the other is 56 Japanese
fetuses ranging from the fourth month to
term (subsequently termed "fresh hone
series"). In both series sexes are combined
because sexual differences in the fetal cranial region are rare (Koura and Yokota,
'60). Age of the dry bone series was estimated by the method of Morita et al., ('73)
from a given long bone. The thickness at
the ossification center (OC) of the frontal
and parietal bones was measured with a
micrometer readable to 0.01 mm (fig. la,b).
The thickness of the temporal bone at the
midpoint (MP) between porion and the
highest point of squamo-temporalis was
also measured on both sides (fig. Id). The
results thus obtained were investigated
from the viewpoints of bilateral difference
and relative growth (Huxley, '32).
Fresh bone series were obtained in a
fresh condition from various hospitals and
preserved in 10% formalin solution. Investigations prove that formalin preservation
for a period over six months leads to no
great change in the external dimensions of
the body (Schultz, '19; Patten and Philpott,
'21, and Scammon and Calkins, '29).
The formalin preserved fetuses were
first measured for crown-rump length,
head length, head breadth and head circumference. The heads were then carefully dissected and the left side of individual bones of the cranium only were
removed for further investigation. Observation on the dry bone series proves no
statistically significant difference between
the right and left sides.
To demonstrate the general size of each
bone, vertical and transverse arc lengths
were measured on frontal, parietal and occipital bones and the vertical arc only on
temporal bones.
Methods of measurement in frontal and
temporal bones were those of Misaki
('59a,b), parietal bones of Koura and
Yokota ('60) and occipital bones of Nishida
('59). In the frontal bone, vertical arc
length is from the supraorbital edge to the
highest point of squama and transverse arc
length is the maximum one (fig. la). In the
parietal bone, transverse arc length is parallel to the Frankfort horizontal plane (FH)
and passes through the center of this bone;
the vertical arc is at right angles to the
transverse arc at the center of the bone
(fig. lb). In the occipital bone, the maxiinum vertical arc length and the maximum
width as a transverse arc were measured
(fig. lc). In the temporal bone, the arc
crossing at right angle to FH from uppermost point of porion to supratemporal
border was measured as the vertical arc
length (fig. Id). The instrument used was a
measuring tape readable to 1mm.
After the arc length of each bone had
been taken, the thickness at the same
points as dry bone series were measured.
Besides, the thicknesses of occipital hone
at the ossification center (OC)and the midpoint (MP) between the ossification center
and the highest point of squamo-occipital
were measured (fig. lc).
The results thus obtained were investigated from the viewpoint of absolute and
relative growth (Huxley, '32). Detailed
statistical procedures of allometric analysis
are given by Sholl ('48,'50) and Sagami
('69). In the allometric equation (y = bx.1,
crown-rump length is the abscissa (XI and
arc length and thickness of each cranial
bone are the ordinates (yl. The allometric
equation transformed into logarithms, log y
= a log x log b, means that any values in
this formula plotted on the double logarithmic grid fall along straight lines.
In the equation, a is the allometric
coefficient and log b is the initial growth
coefficient (Huxley and Tessier, '36). The
value of a gives the ratio between the
specific growth rates of the dimensions x
and y. When this value is 1.00, the slope of
the line is 45"and the specific growth rates
of x (the abscissa1 value) and of y (the ordi-
+
143
FETAL CRrZNIAL BONE THICKNESS
la
lb
lc
Id
@ : O S S I F I C A T I O N CENTER
(OC)
El : M I D D L E
POINT
(M PI
V :VERTICAL ARC LENGTH
T :TRANSVERSE ARC LENGTH
Fig. 1 Schematic rcpresentation of the vertical and transverse arc lengths measured for each
bone: frontal (la], parietal (lbl,occipital (lc) and temporal (Id).OC is the ossification center. MP is
the middle point between the ossification center and the highest point of squamo-occipital of occipital
bone (Ic),and that between porion and the highest point of squamo-temporalis of temporal bone (Id),
respectively. FH, Frankfort horizontal plane.
nate value) are equal, that is, isometry. by sides and the bilateral differences
When the value of a is less than 1.00,the tested in the frontal, parietal and temporal
slope of the line is less than 45" and the bones. No statistical significance could be
ratio favors the abscissa1value (XI, negative found, namely, a's in the regression equaallometry; when the value of a is greater tion, y = ax+b, taking C-R length as
than 1.00, the slope of the line is greater abscissa, of the right and left frontal bones
than 45" and the ratio favors the ordinate are 0.27 and 0.28, of parietal bones both
value (y), positive allometry.
0.29 and temporal bones 0.27 and 0.28, respectively
(table 1).
RESULTS
To investigate the specific growth rate of
Dry bone series
each cranial bone thickness, allometric
The data of dry bone series were pooled analyses were carried out (table 2). (The
144
FUHIO OHTSUKI
TABLE 1
a- and b-values in the regression equation, y = ax+b, C-R length
being represented by x and the others by y
ltems
Side
a1
11
R
L
R
L
R
L
0.27+ 0.06
- 35.61
- 37.02
- 23.47
- 25.31
- 42.65
- 46.90
Frontal bone thickness (OC)
Parietal bone thickness (OC)
Temporal bone thickness (MP)
I
0.28 f 0.07
0.29k 0.08
0.292 0.09
0.272 0.08
0.28+ 0.09
Significant difference wrisriot toiu~dbetween right and left ndes
TABLE 2
a-
and log b - d u e s in the regression eqwtion, log y = a log x + log b,
C-R length being represented by x and the others by y
Side
a
log b
F-test
2.052 0.45
Parietal hone thickness (OC)
R
L
R
Temporal bone thickness (MP)
R
- 3.43
- 3.23
- 2.07
- 4.55
- 4.55
- 4.77
P
P
P
P
P
P
Items
Frontal bone thickness (OC)
1.96+ 0.46
1.56_+0.44
1.61i 0.25
2.452 0.75
2.54+ 0.64
L
L
OC and hlP are the abbreviations as identified in figure 1.
,'l positive allometry
procedure of analysis by this technique will
be given later.) The a values approximate 2
in all the cases. The a's of right and left
frontal bones are 2.05 and 1.96,of parietal
bones 1.56 and 1.61 and of temporal bones
2.45 and 2.54, respectively. The results
here obtained were not immediately accepted, since no other study of skeletal
growth shows such an exceedingly positive
allometry. This required us to study
another material, i.e. fresh bone series.
Fresh bone series
Absolute growth
Table 3 presents the mean and standard
deviation of arc length for each bone by
fetal age in months. For the frontal bone,
transverse length exceeds vertical length
in the fetuses of four to five months; however, this relation is reversed at six months
and thereafter vertical length is greater
than transverse length in an absolute value.
For the parietal bone, vertical length leads
throughout the latter half of fetal period.
The two dimensions grow proportionally
keeping the same difference as that at the
initial age in this study. In the occipital
bone, contrary to the parietal bone, transverse length is greater than vertical length
throughout the period studied. Even
though not strictly the same measurement,
the results here obtained are in agreement
with those of Misaki ('59a) in the frontal
bone, of Koura and Yokota ('60) in the
parietal bone, of Nishida ('59) in the occipital bone and of Misaki ('59b) in the
temporal bone.
Table 4 presents the mean and standard
deviation of cranial bone thickness by fetal
age in months. At the age of four to five
months, the order of thickness among cranial bones is as follows; occipital bone at
ossification center, occipital bone at midpoint, parietal bone at ossification center,
frontal bone at ossification center and temporal bone at midpoint. This ranking is
nearly constant until the tenth month, except that the position of the occipital bone
at midpoint and parietal bone at ossification center are reversed at seven months.
13
13
10
10
10
N
22.50
34.38
43.90
50.70
55.00
h.1
SD
23.25
29.31
36.80
41.80
45.00
M
N
13
13
10
10
10
M
6.75
14.31
24.90
29.30
39.60
oc
SD
3.40
7.03
6.60
5.70
9.52
Frontal
Abhseviations are as identified in table 3.
7
8
9-10
6
4-5
Age in
months
38.50
45.62
57.30
70.00
76.30
M
SD
TABLE 4
35.75
45.00
56.20
67.40
73.70
M
4.50
4.85
6.88
5.10
5.54
SD
Parietal bone
Tsansv.
5.20
4.43
4.83
5.73
4.16
Vert.
SD
24.00 3.92
29.77 5.59
41.50 3.59
50.60 3.92
57.10 3.76
M
M
9.50
21.69
41.70
49.60
54.30
SD
1.73
9.47
9.23
12.19
13.46
Parietal
OC
M
30.00
67.08
135.90
157.20
165.40
oc
SD
19.92
30.10
42.56
26.98
26.32
Occipital
M
14.50
34.80
39.90
51.70
66.20
MP
3.70
12.17
15.99
9.33
13.52
SD
30.00
36.15
46.50
57.60
60.60
M
4.83
5.01
4.45
4.62
2.68
SD
Occipital hone
Vest.
Transv.
Numbers of materials, means and standard deviations of cranial bone thickness
by fetal uge in months 10-2 mm
1.50
3.33
3.19
3.05
2.71
SD
Frontal bone
Tsansv
9.29
3.28
3.78
3.40
3.53
Vest.
N, numl,rrs of' the rnatrrials (sexes comhinedl.
M, rneans.
SD, standard deviations.
4-5
6
7
8
9-10
Age in
months
Numbers of materials, means and standard deoiutions of arc length
bv fetal age in months mm
TABLE 3
M
3.75
9.85
17.60
21.00
32.80
SD
1.26
1.93
2.36
2.11
2.35
2.22
4.74
5.19
4.71
12.20
SD
Temporal
MP
9.25
11.31
16.70
19.00
24.20
M
Temporal bone
Vert.
146
FUMIO OHTSUKJ
The thickness of occipital bone at ossification center is distinguished above all
others. As far as the author is aware, other
data for the cranial thickness in fetuses are
not available.
distinguished among them, gentle and
steep ones. The slopes are generally gentle
for arc length and rather steep for bone
thickness, which means a differing specific
growth rate predominated by the thickness of cranial bone.
This trend, apparent from the figures, is
more reliable by the result of the F-test for
a values given in table 5, namely, the difference between each a value and 1.00.
Where the a value is significantly greater
than 1.00, it is categorized as positive
allometry and vice versa as negative one.
On the other hand, when a is not significantly different from 1.00, it is isometry
(Huxley and Tessier, '36). Graphic representation of a values are given in figure 6.
RelatiGe growth
Analysis of allometry was undertaken in
the following way. The values for arc
length and bone thickness were plotted on
log-log papers by each cranial bone with
crown-rump length as abscissa. Subsequently the usual methods of allometric
technique were utilized (Sholl, '48, '50;
Sagami, '69). Table 5 presents the results of
analysis by this technique for vertical arc
length, transverse arc length and thickness
by each cranial bone. The results of external head measurements are additionally
presented. In table 5, a is the allometric
growth coefficient or the slope of the
regression line, and log b is the initial
growth coefficient considered only the y
intercept of the regression line.
Then, the lines were drawn on each plot
(figs. 2-51 and two kinds of slope may be
DISCUSSION
Growth
The skull may be regarded as a complex
of relatively separate functional components such as cerebral capsule, ear capsule,
orbit, etc. (Van der Klaauw, '48-'52). Furthermore, within a given cranial bone are
three functionally independent compo-
TABLE 5
a
und log b-values in regression equation, log y = a log x + log b,
C-R length being represented h y x and the others by y
Item
Frontal bone
Thickness (OC)
Vertical arc
Transverse arc
Parietal bone
Thickness (OC)
Vertical arc
Transverse arc
Occipital bone
Thickness (OC)
Thickness (MP)
Vertical arc
Transverse arc
Temporal bone
Thickness (MP)
Vertical arc
Head length
Head breadth
Head circumference
a
loe b
F-te5t
2.48 & 0.47
1.13+ 0.17
0.97 f 0.08
-
-
4.48
1.02
- 0.68
P
I
I
2.38k 0.39
1.0810.08
1.08f 0.10
- 4.05
- 0.77
- 0.78
P
I
I
2.492 0.53
2.03i 0.36
1.37k 0.14
1.12r 0.12
- 3.83
- 3.18
P
2.65+ 0.51
1.48r 0.14
1.06? 0.09
1.02+ 0.08
1.10+ 0.08
- 5.02
P
- 2.27
P
- 0.59
- 0.59
- 0.21
P
OC and MP are as identified in figure 1.
F-test, significant at the level of 0.01; P, positive allonietry, I, isometry.
1.60
- 0.96
-
P
P
I
1'
P
FETAL CRAKIAL BONE THICKNESS
1 o-hmw
60
-
FRONTAL
/
BONE
50 -
40
.
. . ..
.
..
30 -
-
20
-
15
-
60
50
40 -
25
Ohm
30
80
1 0;m
90
80
70
70
60
60
50
50
40
40
30
30
25
25
20
20
1 fm,r
90
25
20
15
Thickness
15
10 8
147
-
10
T/
6 -
mm
50
40
20
"F
mm
-
90
80
70
60
30
Transverse A r c
25
20
50
30
40
40
20
I
I
,
125 150
I
200
(
1
30
,
250 300350
C-R L E N G T H mm
Fig. 2 Logarithmic plots of arc length and thickness for the frontal bone against C-R length. Fitting
lines are drawn on each item.
125 150
200 250 300350
L E N G T H mm
Fig. 3 Logarithmic plots of arc length and thickness for the parietal bone against C-R length. Fitting
lines are drawn on each item.
nents: an outer plate, a diploe and an inner
plate. Growth of the outer plate is correlated with the increasing demands of the
scalp tissues in general and of cranial muscles in particular. The inner plate on the
other hand is sensitive to alterations in
cerebral morphology, that is, the state of
adjacent soft tissues (Dyke et al., '33; Ross,
'41; Noback, '45; Noetzel, '49; Fischgold
and Metzger, '51; Lefebvre, '51; Lefebvre
et al., '53; Kehre, '55; Lefebvre et al., '55;
Schiffer, '56; Schiffer and Korn, '56; Kimura et al., '69). Dissociated by the result
of this osseous differentiation of the two
bony plates, an intervening diploe appears.
Kawarada ('68) suggested that the time of
formation of three components within the
parietal bone is at about two years of age.
From the viewpoint of functional anatomy,
the time of diploe formation and any connection between it and high allometric
coefficients in the thickness of cranial bone
are of great concern to us.
The allometric analysis of thickness in
fresh bone series of fetuses (table 5 ) fundamentally coincides with that in dry bone
series (table 2). This confirms both the results as not artificially obtained.
C-R
148
FUMIO OHTSUW
10;1rnr
OCCIPITAL
250
BONE
/
I QXllIl
250
1
fhm
Oj:II??
60
TEMPORAL
BONE
50
200 -
200
150 -
.I
60
50
40
40
30
30
150
25
25
100 90 80 -
100
90
80
20
20
70 60 -
70
15
15
60
50 -
50
40
-
40
30
-
/-' J
10
8
25 20 15
-
mm
6
70
60
5
50
mm
15
40
mm
i
!
70
60
50
40
Transverse Arc
30
25
I
'
0
1
30
o m
30
lo
I.
1
I
25
0 0 B"o0
Vertical Arc
125 150 200 250 300350
C - R L E N G T H mm
Fig. 5 Logarithmic plots of arc length and thickness for the temporal bone against C-H length. Fitting
lines are drawn on each item.
weight and areal growth of fetal parietal
bone (Ohtsuki, unpublished) and the a
values in table 3 for one dimension, head
length, breadth and circumference aplines are drawn on each item.
proximate 1, or isometry. Taking this into
consideration, the present results are
In a previous report, a values were 3.21 peculiar as one-dimensional outcomes.
for body volume and 3.17 for body weight Something must be taking place in the
in the human fetuses (Morita and Hattori, growth of individual bone.
'69). However, a values approximating 3
The following outline of the growth
are generally for volumetric or weight process of cranial bone in the fetal period
growth, 2 for areal growth, and 1 for the is useful for consideration of the cause of
growth of one dimension. For example, the high a values obtained: Ossification of
3.74 and 2.20 are found for the a values of membrane bones commences as a thin net1 2 5 150
C-R
200
250 300350
LENGTH mm
Fig. 4 Logarithmic plots of arc length and thickness for the occipital bone against C-R length. Fitting
149
FFTAI> CII4NI.4L RONE 'l~HI(:KNESS
GRAPHIC REPRESENTATION OF
08
ITEMS
1
I
FRDNlAl
Vertiral
25
I
I
iOC)
Arc
BONE
tOC1
Thickness
0
Arc
VprtiLal
I
Transverse
0
Arc
-------.
BONE
OCCIPITAL
Thickness
(OCI
ThicknPss
(MF)
Arc
Vertical
Transverse
Arc
BONE
Thickness
Vertical
2
Arc
Transverse
TEMPORAL
15
I
-VALUES
BdbF
Thickness
PARIETAL
___-
Q
iMPi
Arc
HEAD
LENGlH
HEAD
RREADlH
HE A U
C I P C IJ M F E R F N L E
0 : Positive Ailornetry
0
: Isometry
Fig. 6 Graphic reprcwntation of allornetry coefficients. Numerals indicated in the first row of the
figure are allorrietric coefficients. Note that all the a values of the thickness at OC and MP deviatcr far
from the vertical line of the figure, i.e. extremely positive ;illoinetr). Thea values of arc lrngth and external head dirrtrmsion locate new this line. i.e. isometry.
work of bone in the region of the future
eminence. Growth o c c ~ mby the formation
of the long thin bony trabeculae laid down
radially from the primary ossification center. Later a few secondary trabeculae
arise, fuse with each other and increase the
size of the original bony network.
Thus, in a cross-section of any individual
cranial bone, a comparatively large unossified or vacant area is observed among bony
trabeculae (fig. 7 ) . The behavior of this
area rnay hold a key to interpreting the
present a values of cranial bone thickness,
that is, any high speed extension of vacant
area, not of bone s~il~stance
itself. is presumably in the dynamic growing process
within an individual bone. The quantitative
analysis of the cross-sectional tissue of cranial bone is requisite to the next step.
Finally the positive allometry in the vertical arc length for temporal and occipital
bone? is of' interest for the one-dimensional
outcomes. Nishida ('59) and Ohtawa ('67)
also described a relatively high growth
rate in the latter half of the fetal period for
vertical arc length in temporal and oc-
150
FUMIO Olf'SUKI
Fig. 7 Saniples of parietal lmne tissue of a fetus cross-sectioned at ossification center, 7a of the sixth month
and 7t)of the seventh month, respectively. Note the vacant area in proportion to that filled with bone substance.
x 50.
FETAL CRANIAL BONE THICKNESS
cipital bones respectively, which supports
the present results. It is common knowledge that the cranial bones are of dual origin, membranous and endochondral; occipital and temporal bones have a complicated structure composed of both parts.
Moss ('55) demonstrated the singular behavior of the cartilagenous part in occipital
bone growing relatively faster than any
cranial and postcranial bone. Since his
series of human fetuses are from 14 mm to
175 mm C-R (55 to 133 days of menstrual
age), earlier in growth stage than the present materials, some alternative or compensatory changes in the growth rate favoring
the membranous portion may have been
possible in the later fetal period in response to the rapid growth of underlying
soft tissues. However, it is hasty to present
any conclusion based on fragmentary information; estimating the whole from knowledge of a part is also dangerous here. The
study of the growing process for a membranous portion in close connection to a
cartilagenous portion is certainly necessary
for clearer analysis of the present results.
151
more active metabolism in the brain and
makes the left inner plate narrower than
the right side by a strong inner pressure
upon it adjusting to the expansion of the intra-cranial contents. Attention may be
called thereby to the functional independence of inner and outer plates in cranial
bones (Van der Klaauw, '46; Delattre and
Fennart, '54; Simon, '55; Kimura et al., '69);
that is, the inner plate responds primarily
to the underlying brain.
No difference b y side in the thickness
of cranial bone for postnatal preadults
(Roche, '53) and prenatal samples (the
present study) would not thoroughly refute
the hypothesis of Hackl ('661, because it is
presumably taking a long term until any
changes of soft tissue (brain) bring corresponding changes in the cranial bone. It
seems, however, scientifically unsound to
take two morphological and/or behavioral
events, e.g., cerebral dominance and bone
thickness changes and assign a causal relationship between them. There should be
some intermediate steps which need to be
considered before jumping from brain
morphology to bone shape or thickness.
Bilateral d gference
Besides, few studies on the growth of
Studies of the bilateral difference in the brain are decisive for the validity of
thickness of cranial bone are rare. Roche Hackl's interpretation. The anatomic dif('53)investigated a postnatal subadult sam- ference between the dominant and the
ple (3-21 years) and found no significant minor cerebral hemisphere is uncertain exbilateral difference at euryon. Hackl ('661, cept that the occipital horn of the lateral
on the other hand, observed adult crania ventricle is usually larger and the sulcus
(under 50 years) and found asymmetry in lunatus more prominent on the left side
the thickness near stephanion. His sexes (Adams and Mohr , '70).
Whether heredity or learning is responcombined data showed that 71 out of 100
cases dominant in the right side, 16 cases sible for hand preference is still controversial.
left side and 13 c a e s were symmetric,
ACKNOWLEDGMENTS
Of the general population, the ratio of
right-sided dominance in the upper limbs
The author is deeply indebted to Profesis approximately 90-95%, the remainder sor S . Morita, the director of the Departleft-sided and 10-2096 partially left- ment of Anatomy, The Jikei University
handed, that is, preferring neither hand School of Medicine, for his cordial direccompletely but favoring one hand for more tion throughout the study, without whom
complicated tasks (Adams and Mohr, '70). this study would not have been possible.
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