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The correlation between craniofacial and long bone growth An experimental investigation in normal rabbits.

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THE AMERICAN JOURNAL OF ANATOMY 177:519-525 (1986)
The Correlation Between Craniofacial and Long Bone Growth:
An Experimental Investigation in Normal Rabbits
PER ALBERIUS AND PER-ERIK ISBERG
Departments ofAnatomy (PA.) and Statistics (PE.I.),
University of Lund Sweden
ABSTRACT
The present study was undertaken to elucidate the relationships between craniofacial and long-bone growth. Nine male New Zealand
white rabbits received spherical tantalum bone markers in the tibial epiphyses
and in the nasal, frontal, and parietal bones. The animals were followed from
30 to 143 days of age. Growth changes were calculated with a roentgen
stereometric system, and the results statistically evaluated. Except for the
final interval when all variables varied at random, high correlations between
tibial and frontonasal or coronal sutural growth were demonstrated; and the
respective linear regression lines were homogenously assembled. The relationship between the tibia and the sagittal suture displayed great variations
between individual animals as well as between the suture’s parts,. although
growth at the interfrontal suture was clearly correlated to tibial growth upon
exclusion of the time factor. The first principal component of the three neurocranial sutures was calculated and seemed accurately correlated to long-bone
growth. The present study concluded that growth at the frontonasal and
coronal sutures normally seems to parallel general somatic development, while
growth at the sagittal suture appears individually displaced in time. Nevertheless, when the principal component of the combination of the coronal suture
and the neurocranial section of the sagittal suture was computed, this was
highly correlated to body growth.
The mechanisms regulating enchondral
and intramembranous bone growth are not
yet fully understood. Several factors, such as
heredity, age, species, nutritional status, and
endocrine responses seem to affect growth in
general. Other factors have localized effects,
e.g., blood-flow changes (Wray and Goodman,
1961; Sunden, 1967) and oxygen tension
(Persson, 1968) in long bone growth, as well
as soft-tissue expansion (neural mass growth)
causing bone separation at neurocranial sutures (Moss and Young, 1960; Moss, 1975).
These examples and others lead us to assume
that the growth process is regulated by an
intricate interaction between manifold systemic, regional, and local influences.
The skull and the long bones grow in response to both cartilaginous tissue growth
and desmal bone growth. Cranial development is determined by growth of all its components, but is essentially characterized by
differential growth between the neurocranium and splanchnocranium. The greater facial growth may contribute to orthocra-
0 1986 ALAN R. LISS, INC.
nialization in some species, which process
has been studied mainly in rats (e.g., Baer,
1954; Moss, 1958; Hoyte, 1971; Moss and Vilmann, 1978). Moreover, the facial skull has
shown differential growth of its splanchnocranial components (the respiratory and
masticatory components; Pucciarelli, 1981).
So far, few investigations using concomitant registrations of long bone and craniofacia1 bone growth have been conducted. Young
(1959) used tibial length as a skeletal indicator for comparisons between experimental
and control animals when studying the influence of cranial contents on skull growth in
rats. This was due t o the tendency of the
experimental animals t o lag behind controls
in general somatic development and to the
existance of variations in skeletal maturation between control animals of the same
age. Hinrichsen and Storey (1968) used heliAddress reprint requests to Dr. Per Alberius, Hjalmshultsgatan 1, 5-252 41 Helsingborg, Sweden.
Received January 28, 1986. Accepted July 13, 1986.
520
P. ALBERIUS AND P.-E. ISBERG
cal torsion springs to elucidate the effect of
abnormal compressive and tensile forces
across the midsagittal suture and across the
proximal tibial epiphyseal plate in guinea
pigs. A procedure with direct clinical consequences has also been presented. As a result
of the close temporal relationship between
pubertal somatic growth and that of facial
dimensions, the evaluation of enchondral
skeletal maturation by wrist radiography
was introduced by Greulich and Pyle (1950)
in order to identify the onset of the pubertal
growth spurt in man. This relationship was
further investigated by Bjork (1972), and the
technique has facilitated orthodontic treatment planning.
Trunk length or long bone registrations
often have been executed for comparative
reasons in studies on the effects of nutritional stresses on craniofacial growth. Interestingly, Riesenfeld (1974) noted that relative
face length in rats reacted with greater intensity than the trunk to both growth depression and growth-promoting factors, irrespective of whether the etiological cause was
nutritional or hormonal; and Riesenfeld also
observed that these factors had limited effects on neurocranial growth. Similarily, Alberius (1983a) reported that, during a brief
period of reduced food and water intake, the
rabbit frontonasal suture (a splanchnocrania1 suture) and the tibia immediately reacted
with reduced growth rates followed by catchup periods. Conversely, mean growth at the
coronal suture was only minimally affected,
even though increased growth rates were
registered in individual animals after resumption of eating. Also, van der Werf(1984),
who biometrically investigated the response
of cranial and long-bone growth in rabbits to
early weaning, found that these growth sites
follow identical patterns.
No attempt has yet been made, however, to
elucidate the specific relationships between
neurocranial and facial skeletal growth to
long-bone growth under normal circumstances; do these growth sites coincide in general
development, and what are their mutual relationships? The purpose of this presentation
was to investigate these issues biometrically
over a n extended period of time in a n animal
model.
21°C (40% relative humidity), with light from
0600 to 1800 hr and with standard pellets
and water provided ad libitum. The rabbits
were followed until age 143 days.
Operative technique
The animals were anesthetized by intramuscular neuroleptanalgesia (Hypnorm vet.@:
Fluanizon and Phentanyl, 10 and 0.2 mglml,
respectively; 0.6 m l k g body weight). The
rabbit’s head was shaved, after which the
surgical area was cleaned with alcoholic
chlorhexidine (5 mg/ml). A para-midline skin
incision from the parietal to the nasal region
was made. The skin and underlying tissues
were reflected laterally, and the calvarial sutures were identified (Fig. 1). Spherical tantalum bone markers (0.8 mm in diameter)
were implanted in the nasal, frontal, and
parietal bones with a specially constructed
instrument (Aronson et al., 1974).Each bone
segment received a t least two implants,
thereby enabling control of marker stability.
The spheres were implanted along bilateral
rostral-caudally oriented lines paralleling the
median plane, the line connecting each bilateral marker pair being at a right angle to
the midline (Fig. 1). Care was taken to minimize periosteal manipulation. After the implantation of bone markers the incision was
closed with interrupted 410 Dexon@(polyglycolic acid) sutures and covered with Nobecutan@spray. Thereafter, tantalum balls (0.5
mm in diameter) were percutaneously, under
fluoroscopic control, implanted in the proximal and distal tibial epiphyses bilaterally by
means of a n angiographic needle with a n
outer diameter of 0.97 mm. The animals were
left to recover on a warm electric blanket.
The postoperative period was uneventful.
MATERIALS AND METHODS
Animals
We used nine 30-day-oldmale New Zealand
white rabbits. The animals were kept at 20-
Fig. 1. Relevant anatomy of the rabbit calvarium and
principles of bone-marker positioning. Bones: 1,nasal; 2,
frontal; 3, parietal. Sutures: 4, internasal; 5, frontonasal;
6, interfrontal; 7, coronal; 8, interparietal.
521
CRANIOFACIAL RELATIVE TO LONG BONE GROWTH
Roentgen stereophotogrammetry
Roentgen stereometric analysis was undertaken with a system developed by Selvik
(1974).The animals were examined in a glass
calibration cage equipped with tantalum reference markers of known internal positions
lying in two parallel planes (Fig. 2). This
cage defines a three-dimensional (3-D) laboratory coordinate system. Two simultaneously exposing roentgen tubes were positioned with an approximate focus-to-focus distance of 0.4 m and a focus-to-filmdistance of
near 1.0 m. The maximal radiation dose for
one examination was 0.6 mGy (Alberius and
Selvik, 1983). Skeletal shape was generally
disregarded.
Initial stereoroentgenograms were obtained on the day of implantation and thereafter at regular intervals on the days indicated in Table 1. The films were digitized in
a precision instrument for aerial photogrammetry (Wild Autograph A8). Three-dimensional coordinates of the bone markers were
obtained by computer processing (Sperry
1100/81) and further analyzed by computer
to ascertain distance changes. Longitudinal growth was calculated by a program using the 3-D Pythagorean theorem.
Growth rate values for the tibia and the frontonasal and coronal sutures represent means
of the right and left side. The accuracy (1
S.D.) is 21.0 pm for each growth registration;
thus, 3 pmlday for a 2-week period (Alberius
and Selvik, 1983).
TABLE 1. Examination Drotocol
Intervals
1
Age(days)
30-45
15
Lengthof
examination
oeriod (days)
2
3
4
5
6
7
45-59
14
59-73
14
73-87
14
87-101
14
101-115
14
115-143
28
sc ss
170
-60
-50
‘1
i ...
-LO
300
- 30
......
-20
-10
Stereo
Examinations
Fig. 2. Stereometric examination. The rabbit’s head
is positioned on a support in the calibration cage and is
simultaneously radiographed by two roentgen tubes (focus 1 and 2). Cage reference markers in the upper and
lower planes are indicated.
-
5b
t
f
IOO
?
t
t
t
days
t
t
Fig. 3. Illustration demonstrating mean craniofacial
and tibia1 growth rates (pmlday) during the period investigated (days 30-143). T, tibia; SFN, frontonasal suture;
SC, coronal suture; SS, sagittal suture (internasal, IN;
interfrontal, IF; interparietal, IP).
522
P. ALBERIUS AND P.-E. ISBERG
RESULTS
The rabbits exhibited parallel successive
reductions in growth rate for the tibia, the
frontonasal, and coronal sutures (Fig. 3, Table 2). During the initial interval, the frontonasal suture demonstrated diminished
growth activity. Growth at all parts of the
sagittal suture gradually increased and
peaked between days 59 and 73, after which
a slow deceleration in growth activity was
registered. The latter suture obtains the
greatest coefficients of variation (S.D./M).
Linear regressions were calculated for all
animals and are presented on an individual
basis for all craniofacial variables relative to
TABLE 2. Mean (SD)growth rates ( p d d a y ) for investigated growth regions as well as
for the first principal components: CF = craniofacial (frontonasal + internasal sutures)
and NC = neurocranial (coronal + interfrontal + interparietal sutz~resi.
For the tibia and the transverse sutures (frontonasal + coronal),
means of the left and right sides are presented
Tibia
662.5
(43.7)
Frontonasal 231.2
(14.7)
suture
47.9
Coronal
(8.6)
suture
Internasal
19.2
(9.2)
suture
Interfrontal
7.3
(6.7)
suture
5.3
Interparietal
suture
(4.2)
CF
0.96
(0.73)
NC
0.43
(1.28)
628.7
(60.11
250.8
(18.5)
44.0
(10.1)
23.0
(7.3)
11.1
(7.6)
9.7
(3.2)
1.43
(0.63)
1.21
(1.12)
Age intervals
4
5
3
2
1
587.7
(61.8)
220.7
(28.7)
40.0
(7.7)
23.5
(8.5)
15.0
(3.2)
10.9
(4.2)
1.16
(0.94)
1.59
(0.91)
495.1
(46.9)
166.7
(18.9)
30.1
(5.7)
14.0
(6.8)
8.1
(4.4)
8.2
(3.7)
-0.08
(0.56)
0.20
(0.89)
I,
T
6
377.0
(29.4)
126.5
(11.0)
22.5
(2.4)
12.6
(3.61
3.8
(2.6)
6.6
(3.0)
-0.64
(0.37)
-0.71
(0.61)
7
295.4
(26.1)
90.4
(11.2)
15.7
(4.3)
10.7
(3.5)
3.5
(2.0)
4.8
(2.4)
-1.14
(0.37)
-1.24
(0.39)
160.5
(22.6)
61.1
(8.41
12.2
(1.6)
6.5
(1.4)
2.6
(1.9)
1.4
(1.4)
-1.78
(0.17)
-1.91
(0.30)
T
600-
500-
LOO
LOO-
3001
300-
200
sc
SFN
I00
200
-7
10
303
20 30 40
50 60
1
603
0
500
Loo
303
200
100
P
10
M
30
10
20
30
Fig. 4. Linear regressions of individual tibia1 and craniofacial growth (day 30-143). A: Tibia
(T) relative to frontonasal suture (SFN). B: T - coronal suture (SC). C: T - internasal suture (IN).
D: T - interfrontal suture (IF). E: T - interparietal suture (IP). Ordinates and abscissae in find
day.
523
CRANIOFACIAL RELATIVE TO LONG BONE GROWTH
ative t o tibia indicated linearity for most
intervals (Table 4). Terminally, though, all
investigated variables varied a t random.
Plots that included every conducted cranial
measurement relative to tibial growth (not
presented) disclosed initial spreading of all
variables, except for the tibia-interparietal
(T-IP) relationship, which was in constant
disarray throughout the observation period.
The analyzed cranial variables were divided into a craniofacial (CF = frontonasal
suture + internasal suture) and a neurocrania1 (NC = coronal -t interfrontal + interparieta1 sutures) group. To investigate the relationship between the tibia and these groups
the first principal component was calculated
for each group. This concept signifies the linear combination of used variables that explains most of the variation observed. The
principal component is a standardized measure with zero mean and unit variance. The
relationship was plotted displaying initial
dispersion and subsequent linearity. Linear
regressions generally had similar intercepts
high correlation coefficients, and smaller ra
ranges (Table 3). Calculated mean values of
all principal components disclosed a n increasing tendency extending to the second
(CF) or third (NC) intervals, whereafter they
diminished successively. The NC group was
slightly more scattered as evidenced by the
standard deviation computations (Table 2).
When the time factor was excluded, the correlation coefficients for the CF group deteriorated due to T-IN instability. The neurocranial suture combination, however, demonstrated a linear appearance with stability
within intervals as well as improved correlations for most periods.
TABLE 3. Coefficients o f determination, I", (medians
and ranges) for the cranial variables and for the first
principal components (see Table 2) relative to the tibia
r2
Variables*
Median
Range
0.978
0.944
0.605
0.641
0.568
0.905
0.865
0.850-0.986
0.878-0.990
0.141-0.876
0.078-0.895
0.200-0.885
0.512-0.946
0.476-0.966
T-SFN
T-SC
T-IN
T-IF
T-IP
T-CF
T-NC
*T, tibia; SFN, frontonasal suture; SC, coronal suture; IN,
internasal suture; IF, interfrontal suture; IP, interparietal
suture; CF = SFN + IN; NC = SC + IF + IP.
the tibia (Fig. 4a-e). The diagrams clearly
demonstrate the homogeneity of frontonasal
and coronal sutural expansion relative to tibial growth. Furthermore, the close approximation of these variables is reflected in the
respective coefficients of determination (r2 ;
Table 3). Conversely, growth a t the sagittal
suture relative to tibial growth did not demonstrate similar linearity. Investigated relationships were found to vary greatly between
different individuals as well as between the
suture's sections. Plotted individual equations were situated at varying levels, having
various inclinations and intercepts. Also, no
particular pattern between the registered r2
for various cranial to tibial combinations was
observed, i.e., a high r2 for the frontonasal
and coronal sutures did not imply any specific trait of r2 for the various parts of the
sagittal suture. When omitting the time factor, thereby investigating each interval per
se, the correlation coefficients for the frontonasal, coronal, and interfrontal sutures rel-
TABLE 4 . Pearson correlation coefficients of long-bone (tibia) growth relative to
craniofacial growth and to the calculated first principal components
(see Table 21 for each interval
Variables'
T-SFN
T-SC
T-IN
T-IF
T-IP
T-CF
T-NC
Age intervals
4
1
2
3
0.742
0.806"
-0.050
0.856*
0.850*
0.083
0.911**
0.706"
0.529
0.051
0.744*
-0.273
0.242
0.570
0.771*
0.647
0.667
0.511
0.280
0.781"
0.553
0.850**
0.487
-0.465
0.762"
0.587
-0.204
0.803**
5
6
7
0.463
0.705
0.587
0.209
0.409
0.608
0.456
0.815"
0.549
0.724
0.204
-0.108
0.815*
0.244
-0.025
0.210
-0.309
0.127
-0.132
-0.221
0.040
'T, tibia; SFN, frontonasal suture; SC, coronal suture; IN, internasal suture; IF, interfrontal suture;
IP, interparietal suture; CF = SFN + IN; NC = SC + IF + IP.
*p < 0.050.
**p < 0.010.
524
P. ALBERIUS AND P.-E. ISBERG
DISCUSSION
The purpose of the present study was to
characterize and analyze the growth relationships between the long bones and the
craniofacial skeleton. To perform any such
assessment, it is essential to obtain reliable
biometric raw data. We used a roentgen stereophotogrammetric system developed by Selvik, which enables longitudinal growth
registrations and offers superior technical accuracy provided distinct measurement points
are available (Selvik, 1974; Selvik et al.,
1983). Tantalum balls were therefore implanted into the relevant bones, a t least two
in each bone. Hereby, control of marker stability was made possible a t each stereo examination. The tantalum bone markers have
been previously shown to become completely
integrated into bone tissue (Alberius, 1983b).
In this study, instability was infrequent and
did not interfere with experimental evaluation. The registered growth data were thus
considered valid for further treatment.
Tibia1 growth as well as growth at the
transverse sutures (the frontonasal and coronal sutures) generally decreased during the
observation period, while all three parts of
the sagittal suture accelerated slowly and
peaked between days 59-73 of age, after
which a uniform deceleration was monitored.
Growth activity at the frontonasal suture,
however, seemed markedly diminished during the initial interval, possibly due to effects
of the surgical procedure (bone-marker insertion), e.g., reduced food intake postoperatively or posttraumatic growth inhibition (see
Alberius and Selvik, 1984). Interestingly,
only a facial suture thus displayed a period
of consistent pronounced growth reduction,
implying that during development the facial
skeleton is rather vulnerable. This interpretation is supported by Riesenfeld's (1974) previously mentioned observation in rats, that
the splanchnocranium seems more susceptible to external influences than both the
neurocranium and body skeletal length.
Speculatively, this sensitivity t o general
health fluctuations indicates that even small
disturbances, especially when extended for
long periods of time, could aggravate potential facial skeletal abnormalities and, conversely, that these defects might partly
reflect previous periods of non-health.
Comparisons of normal growth data from
other biometric investigations have already
been published in detail (Alberius, 1983a; Al-
berius and Selvik, 1983, 1986) and are thus
omitted here.
All variables were plotted and showed initial spreading, with values thereafter tending to approximate a line. Individual linear
regressions for the two transverse sutures
(frontonasal and coronal), were homogenously assembled; and the coefficients of determination, r2, were generally near 1.0.
Also, when excluding the time factor, the
correlation coefficients for both sutures principally showed linearity except during the
last interval, when all investigated variables
varied haphazardly. Normally, these sutures
thus seem to parallel closely general somatic
development during the period investigated,
showing limited interindividual variations;
and definite differences between the two
could not be discerned.
Growth rates at the sagittal suture, on the
other hand, varied substantially, and the relationship between the syndesmosis and the
tibia was not linear. The coefficients of determination differed greatly, and great disparity between individual animals as well as
between the suture's different growth sites
were registered. The plotted linear regressions were positioned on varying levels, having diverging inclinations and intercepts.
Thus, growth a t this suture, including each
of its parts, seems to exhibit temporal displacement of growth phases. This phenomenon is hard to explain on a functional
anatomic basis as the suture covers both facial and neural structures, and growth at the
transverse sutures seemed unaffected. Hypothetically, the variation in growth rates
might reflect asymmetric and uncoordinated
transverse cerebral expansion as well as a
normal biological variation in growth velocity a t a particular age. Moreover, the small
growth rates, a t period approaching the technical error, may induce doubts as to whether
monitored values are correct. However, investigated intervals were compensatorily extended to minimize this risk.
Nevertheless, when the time factor was
ruled out, the interfrontal suture displayed
high correlation coefficients for most intervals. This part of the sagittal suture has previously showed great plasticity, rapidly
reacting to growth disturbances. Unilateral
coronal suturectomy (Alberius et al., 1984)
and bilateral coronal suture immobilization
(Alberius and Selvik, 1984) have been found
to change growth significantly at the interfrontal suture. Evidently, this suture, cover-
CRANIOFACIAL RELATIVE TO LONG BONE GROWTH
525
nial sutural immobilization in rabbits. J. Neurosurg.,
ing the frontal cerebral lobes, which are
6Or166-173.
surrounded only by a narrow skeletal casing, Alberius,
P., and G. Selvik 1986 Long-term analysis of
is more easily affected by growth derangecalvarial growth in rabbits. Anat. Anz., 162:153-170.
ments than the posteriorly situated interpari- Alberius, P., G. Selvik, and L. Ekelund 1984 Roentgen
stereophotogrammetric analysis of neurocranial sutureta1 suture. The latter suture, on the other
ectomy in rabbits. J. Neurosurg., 60:158-165.
hand, overlies a substantially greater mass Aronson,
A.S., L. Holst, and G. Selvik 1974 An instruof neural tissue with inherent possibilities of
ment for insertion of radiopaque bone markers. Radiolcompensatory growth at several areas of the
ogy, 113r733-734.
Baer, M.J. 1954 Patterns of growth of the skull as reneurocranium.
vealed by vital staining. Human Biol., 26:80-126.
The first principal component was com- Bjork,
A. 1972 Timing of interceptive orthodontic meaputed in an attempt to differentiate further
sures based on stages of maturation. Trans. Eur. Orbetween neurocranial and craniofacial thod. SOC.,48:61-74.
growth. This statistical concept amalga- Greulich, W.W., and S.I. Pyle 1950 Radiographic Atlas
of Skeletal Development of the Hand and Wrist. Stanmates information concerning two or more
ford University Press, Stanford.
variables, describing the existing covariation Hinrichsen, G.J., and E. Storey 1968 The effect of force
between investigated variables. This implies
on bone and bones. Angle Orthod., 38:155-165.
that the calculation may be used as an index Hoyte, D.A.N. 1971 Mechanisms of growth in the cranial
vault and base. J. Dent. Res., Suppl6; 5Or1447-1461.
for cranial growth. In this study, the princi- Moss,
M.L. 1958 Rotations of the cranial components in
pal components of the two cranial compothe growing rat and their experimental alteration. Acta
nents generally conformed to and, moreover, Anat., 32:65-86.
elucidated and compressed the information Moss, M.L. 1975 Functional anatomy of cranial synostosis. Child's Brain, Ir22-33.
obtained in the previously discussed anal- Moss,
M.L., and H. Vilmann 1978 Studies on orthoceyses. The pattern of the neurocranial suture
phalization of the rat head. I. A model system for the
group, however, was more homogenous and
study of adjustive cranial growth processes. Gegenconstant in appearance. Conversely, the reg- baurs Morpb. Jb., 124.559-579.
M.L., and R.W. Young 1960 A functional approach
istered instability of the internasal suture- Moss,
to craniology. Am. J. Phys. Anthrop., 18:281-292.
to-tibia relationship disrupted the craniofa- Persson, B.M. 1968 Growth in length of bones in change
of oxygen and carbon dioxide tensions. Acta Orthop.
cia1 suture combination when evaluated for
Scand., Suppl. 117.
each interval. A seemingly haphazard variaH.M. 1981 Growth of the functional compotion was observed; and consequently, growth Pucciarelli,
nents of the rat skull and its alteration by nutritional
at the frontonasal suture alone appears to
effects. A multivariate analysis. Am. J. Phys. Anmore accurately parallel genera1 somatic throp., 56:33-41.
Riesenfeld, A. 1974 Endocrine and biomechanical congrowth increments.
trol of craniofacial growth: an experimental study. HuTo conclude, frontonasal and coronal su- man
Biol., 46531-572.
ture growth or the first principal component Selvik, G. 1974 A Roentgen Stereophotogrammetric
of neurocranial suture expansion (coronal
Method for the Study of the Kinematics of the Skeletal
System. Thesis, University of Lund, Lund, Sweden.
interfrontal
interparietal sutures) exhibit
G., P. Alberius, and A.S. Aronson 1983 A roenthigh and uniform correlations relative to Selvik,
gen stereophotogrammetric system. Construction, callong-bone (tibia) growth.
ibration and technical accuracy. Acta Radiol., (Diagn.),
+
+
LITERATURE CITED
Alberius, P. 1983a Pattern of membranous and chondral
bone growth. A roentgen stereophotogrammetric analysis in the rabbit. Acta Anat., 116r37-45.
Alberius, P. 1983b Bone reactions to tantalum markers.
A scanning electron microscopic study. Acta Anat.,
115:310-318.
Alberius, P., and G. Selvik 1983 Roentgen stereophotogrammetric analysis of growth at cranial vault sutures
in the rabbit. Acta Anat., 117:170-180.
Alberius, P., and G. Selvik 1984 Roentgen stereophotogrammetric analysis of restricted periods of neurocra-
24:343-352.
Sunden, G. 1967 Some aspects of longitudinal bone
growth. An experimental study of the rabbit tibia.
Acta Orthop. Scand., Suppl. 103.
Werf, F. van der 1984 Response of the longitudinal
growth of cranium and long bones to early weaning in
the rabbit. Acta. Morphol. Neer1.-Scand., 223-16.
Wray, J.B., and H.O. Goodman 1961 Post-fracture vascular phenomena and long-bone overgrowth in the immature skeleton of the rat. J. Bone Jt. Surg., 43A:10471055.
Young, R.W. 1959 The influence of cranial contents on
postnatal growth of the skull in the rat. Am. J. Anat.,
105r383-410.
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