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Morphometric changes in growth of the rat pelvis after papain administration.

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THE ANATOMICAL RECORD 235312-318 (1993)
Morphometric Changes in Growth of the Rat Pelvis
After Papain Ad minist ration
ANDREW D. DIXON AND PETER T. GAKUNGA
School of Dentistry and Dental Research Institute, University of California Los Angeles,
Los Angeles, California
ABSTRACT
The proteolytic enzyme, papain, was given systematically
to evaluate the short- and long-term effects of inhibition of endochondral
bone formation on pelvic growth, with emphasis on the innominate bone.
Ninety-eight Lewis-strain male rats, used concurrently for craniofacial
growth studies, were divided into two groups. Thirty rats from Group I
(n = 48) received 2% crude papain i.p. daily from 25-40 days-of-age and were
euthanized at 40, 54, and 70 days-of-age. Thirty-five rats from Group I1
(n=50) were given papain at the same dose from 25-70 days-of-age and
were euthanized at 26, 40, 54, 70, and 120 days. The remaining animals in
both groups were the controls. Standardized dorsoventral pelvic radiographs were taken of all 98 animals. Ten linear dimensions were measured
on each and the data evaluated statistically. A reduction both in size and
rate of growth of the bony pelvis was found. All the anteroposterior and
most of the transverse pelvic dimensions were significantly shorter, to a
greater extent in the prolonged papain group. Bi-ischial width was increased, perhaps to compensate for pelvic shortening and to accommodate
the pelvic contents. The findings may contribute to our better understanding of abnormal endochondral bone growth in the pelvis.
0 1993 Wiley-Liss, Inc.
Key words: Rats, Pelvic growth, Parenteral papain, Radiographs, Morphometrics
The morphology and growth of the pelvis in animal passed their peak growth velocity before the nutrimodels has been the subject of a number of studies tional insult became severe, recovered and caught up.
(Payton, 1953; Harrison, 1958,a,b, 1961, 1968; Hughes Retardation of growth after 2 months-of-age may have
and Tanner, 1970, 1973; Hughes, 1982). Harrison had some permanent effects (Dickerson, et al., 19721,
(1958a, 1968) showed that the length of the rat innom- although animals undernourished from 49-70 days-ofinate bone, and the ilium and ischium as individual age were better able to recover fully from the same
bones, increased rapidly up to 80 days-of-age, with degree of growth deficit (Hughes, 1982).
Following the demonstration by Thomas (1956) that
some growth still being detectable at the end of 1year.
a single intravenous injection of crude papain in rabGrowth of the acetabular region decelerated by 60-70
days-of-age, coincident with the disappearance of the bits produced a reversible collapse of the ears associpubo-ischial flange of the acetabular, epiphysial carti- ated with depletion of cartilage matrix, i t soon was
lage complex that lies between the ilium, ischium, and established that the enzyme inhibited endochondral
pubic bones. Ossification of the acetabular complex be- bone formation at epiphysial growth plates, particugins 70 to 80 days after birth in the epiphysial cartilage larly in young, growing animals. Radiographically,
adjoining the ilium. Synostosis of the three pelvic longitudinal growth was reduced, epiphysial plates
bones begins about 100 days-of-age, with persisting is- closed prematurely, the pelvic bones were shorter, and
lands of cartilage seen along their margins up to 170 their synchondroses disappeared (Hulth, 1958a). All
days-of-age (Harrison, 1958). Hughes and Tanner cartilaginous growth plates did not display the same
(1970, 1973) reported t h a t pelvic length in male rats level of susceptibility. Wider ones, such a s those of the
was greater a t all ages and significantly so after 70 distal end of the femur and proximal tibia, showed a
days-of-age. The velocity of growth in length peaked at more rapid longitudinal growth and higher resistance
50 days-of-age and the major sex difference was one of
size and not of shape.
The effects of undernutrition and subsequent rehabilitation on skeletal growth revealed that the length
Received January 10, 1992; accepted June 24, 1992.
of the skull and limbs recovered their normal size, but
Address reprint requests to Dr. Andrew D. Dixon, Hilgard Avenue,
the length of the spine and the dimensions of the pelvis School
of Dentistry, 63-090 CHS, University of California Los Angedid not (Dickerson and Hughes, 1972). Bones that had les, Los Angeles, CA 90024-1668.
0 1993 WILEY-LISS, INC
MORPHOMETRIC CHANGES IN RAT PELVIC GROWTH
313
to the effects of papain (Hulth, 1958b). The generalized
skeletal stunting was equated with human achondroplastic dwarfism (Hulth and Westerborn, 1959).
The work on epiphysial cartilage has pertinence for
the study of skull growth. Irving and Ronning (1962)
showed similarities in the responses by skull base synchondroses in rats. Ronning (1971) analyzed the effects
of papain on various dimensions of the rat skull. There
was a lag in longitudinal growth so that the skull became brachycephalic. A coincident increase in neurocranial width was hypothesized as a compensatory
mechanism for decreased cranial base length.
The findings on skull growth suggested that a morphometric study of the effects of papain on major components of the pelvic skeleton, where growth cartilages
are a prominent feature, would contribute to our
knowledge of the role of cartilage in pelvic growth.
MATERIALS AND METHODS
Ninety-eight 21-day-old Lewis-strain male rats,
which were used concurrently for the effects of papain
on craniofacial growth, were divided randomly into two
groups and maintained on standard laboratory chow
and water ad libitum until the papain regimen was
begun. Thirty animals from Group I (n = 48) were given
daily intraperitoneal injections of 2% crude papain
(Type 1, activity 1-2 units/mg solid, Sigma Chemical
Co., St. Louis, MO) in normal saline, 100 mg/kg, with
a n injection volume of 0.5 m1/100g, from 25 to 40 daysof-age. The remaining 18 animals served as untreated
controls. Papain-treated and control animals were euFig. 1 . Linear dimensions measured in the study. They are defined
thanized by pentobarbital sodium, 100 mg/kg i.p. a t 40, in the text.
54 and 70 days-of-age. Thirty-five animals from Group
I1 (n = 50) received daily intraperitoneal injections of
2% crude papain (Sigma Chemical Co., St. Louis, MO,
(caudal) point on the ischial tuberosity of the same
Type 1)from 25 to 40,54, and 70 days-of-age. The other
side.
15 animals were the controls. Group I1 animals were
H. Obturator-acetabulum distance: The distance beeuthanized at 26, 40, 54, 70, and 120 days.
tween
the most posterior (caudal) point on the obtuStandardized dorsoventral pelvic radiographs of all
rator foramen and the deepest point in the acetabu98 animals were taken. A portable radiographic unit
lum of the same side.
(Oralix 70, Philips Medical Systems, Inc., Shelton,
I. Obturator foramen length: The maximum anteroCT) and dental occlusal film (Eastman Kodak, Rochesposterior
(rostro-caudal) dimension of the obturator
ter, NY) were used. Radiographic settings were conforamen.
stant (70 kVp, 5 mA), with a target-film distance of
J. Obturator-ischial distance: The distance between
24.5 cm. Photographic enlargements ( x 4) were made
the most posterior (caudal) point on the obturator
and ten linear dimensions measured on each print (Fig.
foramen
and the most posterior (caudal) point of the
1):
ischial tuberosity of the same side.
The means of the data for each dimension were anA. Bi-iliac width: The distance between the most latalyzed statistically using Student’s t test for differences
eral, everted points on the iliac crests.
B. Iliac length: From the anterior (rostral) border of between papain-treated and control groups. Dried pelthe iliac crest to the midpoint of the ilio-ischial junc- ves from both experimental and control rats were prepared for gross morphological comparison.
tion of the same side.
C. Bi-acetabular width: The distance between the
RESULTS
deepest point in the concavity of each acetabular
By 40 days-of-age, papain-treated animals had both
fossa.
D. Interobturator width: The distance between the shorter and narrower pelves and this general reduction
most posterior (caudal) points on the obturator fo- in pelvic size was maintained throughout the experiment (Fig. 2). Superimposition of the pelvic outlines of
ramina.
E. Bi-ischial width: The distance between the most papain-treated and control animals at the level of the
acetabulum showed the shorter ilium and ischium, pelposterior (caudal) points on the ischial tuberosities.
F. Acetabular diameter: The maximum antero-pos- vic narrowing, and a lateral inclination or flaring of
the ischial region (Fig. 3). This appearance was more
terior diameter of the acetabulum.
G. Ischial len&h: The distance between the midpoint pronounced in Group I1 rats that had received papain
of the ilio-ischial junction and the most posterior for 45 consecutive days (Fig. 4). The treated animals
314
A. D. DIXON AND P. T. GAKUNGA
Fig. 3. Superimposition of short-term papain-treated (shaded) and
control (dotted outline) pelves at 54 days-of-age. The papain-treated
pelvis is shorter, narrower, and the ischial tuberosities are flared
outwards.
Fig. 2. Dried pelves of papain-treated (right) and control rats (left)
at 40, 54, and 70 days-of-age. The pelves of papain-treated rats are
smaller and show a lateral flaring of the ischial bones.
had a concave-shaped ischium, unlike the typically
convex form of control ischia. Other features were a
lateral displacement of the ischial tuberosities, a concavity of the caudal border of the ischial ramus, a more
acute suprapubic angle, and a n increase in the subpubic angle. Tables 1 and 2 give the percentage changes
and levels of significance for the ten pelvic dimensions
measured in Group I and 11, respectively.
Anteroposterior Dimensions
By 40 days-of-age, iliac length was significantly
shorter in the papain-treated animals (Figs. 2-4). Iliac
length plotted against age showed a steady increase in
the control length until 54 days-of-age, when i t began
to level off (Fig. 5a). At 54 days-of-age iliac length was
12.34% shorter in Group I and more than 22% shorter
in Group 11. The growth pattern for ischial length was
very similar (Fig. 5b). By 54 days-of-age it was shorter
by 7.47% in Group I and by about three times as much
in Group I1 (Table 2).
The antero-posterior diameter of the acetabulum in
the papain groups was shorter a t first but then showed
a small increase (2.65%) in Group I by 54 days-of-age,
when the diameter was shorter by over 20% in Group
11. Obturator foramen length also was shorter at first
but by 54 days-of-age was greater in Group I1 compared
to the controls. At 70 days-of-age the length was
shorter again by 10%.
Transverse Dimensions
Bi-iliac width in papain-treated rats was less than in
controls a t all stages of the experiment; for example, by
4.86% in Group I and by 10% in Group I1 at 54 daysof-age (Tables 1, 2; Fig. 4). At 70 days-of-age, the narrowing was statistically significant in Group I1 (Table
2). Bi-acetabular width was affected significantly by
papain only in Group 11, where it was 26% less than in
the control a t 54 days-of-age (Fig. 5c). This was particularly evident when the superimpositions of dried pelves were compared (Figs. 3, 4). Interobturator width
had increased by 5.67% and 6.48% in Group I a t 54 and
MORPHOMETRIC CHANGES IN RAT PELVIC GROWTH
,
I
,--,
\
315
was a mirror image of the control curve, with a sharp
drop in velocity between 40 and 54 days-of-age.
Bi-ischial width growth rate peaked a t 54 days-ofage both in papain-treated and control animals (Fig.
5f). This was followed by deceleration in both groups
up to 70 days-of-age, much more so in the controls. The
velocity curve for bi-acetabular width in control rats
was similar to the curve for iliac length, peaking at 54
days-of-age. The papain-treated animals showed a
large drop in velocity a t this age but recovered almost
to the control rate by 70 days-of-age.
DISCUSSION
Fig. 4. Superimposition of long-term papain-treated (shaded) and
control (dotted outline) pelves a t 54 days-of-age. The papain-treated
pelvis is considerably smaller than the Group I pelvis shown in Figure
3 and the subpubic angle is flattened.
70 days-of-age, respectively. The width was less in
Group I1 rats a t these ages.
In the short-term papain Group I, bi-ischial width
increased significantly, by 42.32% and 35% at 54 and
70 days-of-age, respectively (Table 1,Fig. 5d). In Group
I1 the increase was not significant a t 54 days-of-age but
had increased by 18.51% at 70 days-of-age (Table 2).
These changes were matched by the ischial flaring
seen in dried specimens (Figs. 3 and 4).
Other Dimensiohs
At 40 days-of-age, the obturator-acetabulum distance was shorter in both experimental groups. The
decrease at 70 days-of-age was 18.13% in Group I and
6.94% in Group 11. But in Group I1 this dimension was
about 20% shorter at 120 days-of-age.
The obturator-ischial distance increased by 59% in
Group I and by about one third in Group I1 (Tables 1
and 2). At 70 days-of-age, the increase was 21.40% in
Group I. In contrast, there was a significant decrease of
16.95% in Group 11.
Rates of Growth
Iliac length growth rate peaked at 54 days-of-age
both in the controls and the papain-treated groups,
with the control animals having the higher growth velocity (Fig. 5e). Ischial length rate peaked earlier, at 40
days-of-age, and the curve for papain-treated animals
Dimensions were selected for measurement that
would give maximum information about changes in
length of the individual components of the innominate
bone and alterations in pelvic width. A number of the
dimensions related to the inner pelvis and were indicators of any altered morphology in and around the
acetabular region, such a s might result from the effects
of papain on the Y-shaped, triradiate growth cartilage,
which unites the three parts of the hip bone and is
synchondrosal in nature. We were aware that papain
affects the length of the cranial base through interference with endochondral bone formation at its synchondroses (Dixon et al., 1987).
Both the amount and rate of stunting of pelvic dimensions were clearly dependent on whether papain
was given over the shorter or longer period, with the
more pronounced effects usually resulting from prolonged administration. Comparative information from
previous studies is limited. Hulth (1958a) gave papain
intravenously to rabbits up to four times over a 2-week
period and observed in whole-body radiographs that
the synchondroses between the separate pelvic bones
had disappeared. Although he did not comment on it,
shortening and flaring of the ischial region is obvious
in one of his radiographs. He showed that pelvic length
in papain-treated rabbits was significantly shorter, by
9.4-28.5%, depending on the initial age and length of
the follow-up period (Hulth, 1958b). Our short-term
data, when iliac and ischial lengths were summed,
were in the same range.
There was a conspicuous difference in the size of our
dried pelvic specimens between the papain-treated and
control animals. As expected, the reduction in the overall size of the pelves was more pronounced in Group 11.
The retardation in growth caused by papain was evident not only in the anteroposterior direction, but in
most transverse measurements as well. This emphasized the dramatic effects of papain on pelvic skeletal
dimensions. Even though some measurements were affected more than others, in keeping with earlier reports
of the effects of nutritional deficit on the skeleton
(Hughes, 1982), systemically administered papain apparently influenced all the cartilaginous areas of the
pelvis to some degree, contributing in toto to the size
reduction.
The ratio of ischial to iliac length was constant
throughout the period of the experiment, a s were ratios
for most of the transverse dimensions (bi-iliac to biacetabular width, bi-iliac to bi-ischial width), both for
the papain-treated and control animals. This was consistent with results reported by Harrison (1958a1, who
316
A. D. DIXON AND P. T. GAKUNGA
TABLE 1. Dimensional changes in Group I (P< 0.001, unless indicated), expressed
as a percentage decrease or increase ( +) compared with the controls
Iliac length
Ischial length
Acetabular diameter
Obturator foramen length
Bi-iliac width
Bi-acetabular width
Interobturator width
Bi-ischial width
Obturator-acetabular distance
Obturator-ischial distance
*P<0.05; n.s.
**P<O.Ol.
=
40
12.69
13.05
6.31**
6.37
7.17**
7.69 n s .
12.11 n.s.
3.82 n s .
9.16**
1.14*
Days-of-age
54
12.34**
7.47 n.s.
+ 2.65 n.s.
+ 2.89 n.s.
4.86 n.s.
1.93 n.s.
+ 5.67 n s .
+42.32**
9.45*
+ 59.00
70
11.76
10.08
+ 1.97 n.s.
15.47
0.75 n.s.
1.01 n.s.
+ 6.48*
+ 35.00
18.13
+21.40
not significant.
TABLE 2. Dimensional changes in Group I1 (P< 0.001, unless indicated), expressed as a percentage decrease or
increase ( + ) compared with the controls
Davs-of-aee
Iliac length
Ischial length
Acetabular diameter
Obturator foramen length
Bi-iliac width
Bi-acetabular width
Interobturator width
Bi-ischial width
Obturator-acetabular distance
Obturator-ischial distance
*P<0.05; n.s.
**P<0.01.
=
40
12.69
13.05
6.31**
6.37
7.17**
7.69 n s .
12.11 n.s.
3.82 n.s.
9.16**
1.14*
54
22.66
23.12**
21.19*
+ 14.50**
10.00
26.04
3.25*
0.90 n.s.
14.31**
+31.35
70
23.36**
18.28**
9.46**
10.50**
17.67
24.88
10.57**
+ 18.51
6.94*
16.95**
120
16.73
i9.76
+ 8.29
44.40**
8.03*
18.35
18.35
+ 4.70*
21.35*
3.50 n.s.
not significant.
opined that pelvic growth was regulated by general
growth factors.
Further experiments are required to differentiate
the specific contributions to pelvic growth made by various cartilaginous growth sites, particularly in the acetabular region. Administration of papain directly into
selected areas, such a s the hip joint cavity and the vicinity of the triradiate cartilage, would be two possibilities. Tingey and Shapiro (1982) injected papain unilaterally into the temporomandibular joint of growing
rabbits and found a significant decrease in vertical
growth of the mandibular ramus, as a result of inhibited cartilaginous bone growth at the condyle. Cuenin,
Dixon, and Hoyte (1991) showed that localized injection of papain a t the septosphenoidal synchondrosis in
the cranial base of young rats, a bone-cartilage junction whose structure is comparable to a pelvic growth
cartilage, caused shortening of the snout. This demonstrated the importance of a specific region of the cranial base for facial growth.
The outward displacement of the ischial tuberosities
that gave the ischial rami a laterally concave form in
papain-treated rats was confirmed by the measured increase in bi-ischial width. This consequence may have
been a compensatory mechanism to maintain the normal volume of the lesser pelvis despite the reduction in
ischial length. It is assumed that papain did not affect
the development and growth of the soft tissues (e.g., the
genito-urinary system) bounded by the ischial bones. If
the normally expanding pelvic contents led to ischial
widening, this has its parallel in the functional matrix
concept used to explain growth of the craniofacial complex (Moss, 1962). Growth of soft tissues such as the
brain and eyeball seem to dictate three-dimensional
growth of surrounding bones.
Similar conclusions have been drawn with respect
to the growth of the neurocranium following papain
administration. Volumetric requirements of the growing brain in brachycephaly induced by papain seemed
to dictate a compensatory increase in skull width and
height (Ronning, 1971; Schramm et al., 1974; Kvinnsland, 1974a,b). Further study to compare the volume
of the lesser pelvis before and after papain injection
would help clarify this hypothesis for pelvic growth.
There are other possibilities. The divergence of the
ischial bones may have been a direct result of disruption
of the triradiate cartilage by papain that, for example,
could prompt a reduction in bone formation on the lateral aspect of the acetabular region. If such a restriction
in cartilage growth occurred it conceivably could lead to
“constriction” of acetabular growth, by inhibition of either the triradiate or cup-shaped parts of the acetabular
cartilage, or both. Atypical differential growth within
its different parts could lead to a n everted ischium.
317
MORPHOMETRIC CHANGES IN RAT PELVIC GROWTH
30
22
1
T
h
E
E
v
5
m
20
-
C
4
--O-
1 0 1 .
I
.
I
.
I
.
I
80
60
40
Controls
Papain
.
I
100
120
.
I
20
140
40
60
80
100
120
140
Age (days)
22
7
m-
-
18
1
20
-
18
h
h
E
16V
5
22
-
-
12
lo
8
1
16
-
5
14-
is
Controls
Papain
.
E
v
.
-
d
P
14:
* Controls
1
20
.
1
40
.
I
60
.
I
.
80
I
100
Papain
.
,
120
12
. ,
140
-
101
30
.
,
.
I
40
'.
50
Age (days)
I
.
.
I
70
60
I
80
Age (days)
500
500
f
* Controls
400
mx
U
h
s
-
Papain
300
a,
m
U
r,
2W
s
100
0
I
20
40
60
80
100
120
140
Age (days)
1
0
40
60
80
100
120
140
Age (days)
Fig. 5. Dimensional changes and growth rates in papain-treated and control rats over time. a, iliac
length; b, ischial length; c, bi-acetabular width; d, bi-ischial width (short-term, Group I); e, iliac length
growth rate; f, bi-ischial growth rate. In a d , vertical bar ? S.E.
Again, the influence of papain would not have excluded the cartilage of the fermoral head. If it were
smaller in papain-treated rats, then this in turn would
lead to a smaller acetabulum, with the ultimate effect
on ischial position we found. While we did not measure
the femoral head, our data showed that the diameter of
318
A. D. DIXON AND P. T. GAKUNGA
the acetabulum actually increased by a small amount
initially, then decreased and increased again by more
than 8% at the end of the long-term (Group 11) experiment.
However, the femoral head still may be a prime contributing factor, for Harrison (1961) removed one or
both heads in rats and found the innominate bones
became laterally concave and medially rotated around
their long axes. He concluded that the phenomenon
was due to the collapse of the acetabular cup, possibly
leading to a directional change in the growth of the
more medially placed triradiate cartilage. Our initial
histological findings show significant changes both in
the thickness and internal structure of the acetabular
cartilage, which indicate its probable demise as a
growth site after papain is administered.
The superimposition of the outlines of short-term papain-treated and control pelves at 54 days-of-age is remarkably similar to a text-figure in Harrison’s (1961)
study, which showed superimposed tracings of normal
and experimental pelves 144 days after bilateral removal of the femoral heads. The flaring and shortening
of the ischia is virtually identical in both studies. Thus,
the overall effects of papain may equate with acetabular dysplasia and lend support to Harrison’s contention
that normal acetabular development and growth depends on a normally placed and growing femoral head.
Finally, our results suggest that besides giving clues
to normal growth processes, the papain model provides
another valuable method for study of the effects of cartilage dysplasia a t the hip joint, devoid of the variables
that surgical trauma may introduce (Kuba et al.,
1985).
ACKNOWLEDGMENTS
We wish to thank Ms. Irene Petravicius for the line
drawings and Mr. Richard Friske and Ms. B. J. Coburn
for their photographic skills. The study was supported
by a grant from the USPHS, RR-05304.
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morphometric, pelvic, papain, change, growth, administration, rat
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