SCVMJ, XVII (1) 2012
133
Histogenesis of uterine body and horns of the one-humped
camel (camelus dromedarius)
Farouk, S. M., Osman, A. H. K. and Eidaroos, H.
Cytology and Histology dept., Faculty of Veterinary Medicine, Suez Canal
University.
Abstract
The current study has been achieved to clarify the prenatal
histological changes associated with the morphogenesis of the
uterus of the dromedary camel with special reference to the
morphological evidence of epithelio-mesenchymal interaction. The
developing uterus was differentiated into a corpus uterus (body) and
two unequal horns at 135 mm CVRL stage. During 210 - 300 mm
CVRL stage, the uterine wall became differentiated into three
sharply demarcated layers; an inner endometrium (mucosasubmucosa), middle myometrium (musculosa) and an outer
perimetrium. At 330 mm CVRL stage, the lining epithelium of the
uterine body showed shallow invaginations in certain areas
penetrating
into the underlying stroma. The endometrial
undulations in the uterine horns appeared at 480 mm CVRL stage.
The lamina propria-submucosa became well-differentiated into two
zones; a superficial, mainly cellular, narrow zone and a deeper, less
cellular, wider one. From 640 mm CVRL on, the endometrium was
distinctly thrown into polymorphic folds of different size. The
primordia of the uterine glands were first observed in the uterine
body at 640 mm CVRL stage and in the uterine horn at 870 mm.
They were in the form of solid cellular sprouts invaginating from
the lining epithelium into the most superficial level of the prorpriasubmucosa. Pronounced coiling of the uterine adenomeres was
noticed at the 1230 mm stage.
Key words: camel, organogenesis, fetal uterus, uterine
adenogenesis.
Introduction
Uterine development and function
depend on epithelio-mesenchymal
interactions (Cunha et al, 1983).
Interactions between epithelium and
mesenchyme are of fundamental
importance during organogenesis,
insofar as epithelial morphogenesis
and differentiation are induced and
specified by the mesenchyme
(Haffen et al, 1987). These
interactions provide local control
and
coordination
of
morphogenetically important cell
134
behaviors, including movement,
adhesion,
differentiation,
and
proliferation
(Sharpe
and
Ferguson,
1988).
During
morphogenesis,
specific
mesenchymal cells build up an
extracellular matrix that might
provide the positional identity of
that tissue or organ through its
molecular structure (Hockel et al,
2005).
Material and methods
The current study was carried out
on the uterine horn and body of 41
female camel fetuses collected from
El-Basateen (Cairo) and Belbes (ElSharqeya) slaughter-houses. All
samples were freshly collected
directly after slaughtering the
pregnant she-camels and evacuation
of their uteri. The crown vertebral
rump length (CVRL) of the
collected specimens ranged from
135 mm to 1230 mm. The collected
specimens were immersed directly
as a whole into 10% neutral
buffered formalin for 4 weeks. The
formalin-fixed
material
was
continuously transferred to freshly
prepared fixative every week.
Following fixation, the specimens
were then preserved in 70% ethyl
alchol.The
preserved
samples
dehyderated into a graded series of
ethanol (75%, 80%, 90%, 95%,
absolute alchol I , II and III ),
cleared in 3 changes of xylene and
then embedded in paraffin wax
(melting point 60º C). The uterine
specimens were serially sectioned at
5 – 7 µm thickness. The prepared
Farouk et al
sections were stained using the
following
stains:
Harris
heamatoxylin and Eosin, Masson's
trichrome, Gomori's stain, PeriodicAcid Schiff (PAS) technique,
Alcian blue technique, pH 2.5,
Combined Alcian blue – PAS
technique,
Combined
aldhyde
fuchsin – alcian blue method,
Toluidine blue, Best's carmine
method and Verhoeff's method.
Freshly collected specimens of the
uterine horn and body were taken
and immersed in liquid nitrogen (196'C), put in cryostat at -20'C and
cut into 10 um thick sections, then
subjected to the following reactions
for detection of enzymes and lipids;
Nitro-blue
tetrazolium
(NBT)
method, Gomori's lead method for
detection of acid phosphatase,
Calcium cobalt method, Modified
method (ATPase) and Sudan blackB. The afore-mentioned histological
techniques were followed as
outlined after, Bancroft et al (1990)
and
Churukian
(2009).
Representative photomicrographs
were taken using Olympus BX41
research optical photomicroscope
fitted with an Olympus DP25 digital
camera, Japan.
Result
At 135 mm CVRL stage, the
developing uterus was differentiated
into a corpus uterus (body) and two
unequal horns. The uterine wall was
comprising three ill-differentiated
zones;
an
inner
epitheliomesenchymal
zone,
a
middle myogenic zone and an outer
mesenchymal covering (Fig. 1). The
SCVMJ, XVII (1) 2012
inner zone was differentiated into
the uterine lining epithelium and the
subjacent
mesenchyme.
The
epithelial lining was made up of
densely packed cells with an
average height about 20.484 µm in
the horn (Table 1) and 22.023 µm in
the
body
(Table
2).
The
epitheliocytes were surrounded by
indistinct boundries, their faintly
easionophilic cytoplasm was PAS
positive and non-alcianophilic. The
euchromatic nuclei were oriented in
2 to 4 levels and they showed many
mitotic
figures.
The
wide
subepithelial mesenchymal layer
was predominantly cellular. The
polymorphic mesenchymal cells
were
associated
with
high
proportion of fine, argyrophilic
fibers and thin-walled blood
vessels. Collagenic and elastic
fibers were not encountered. The
intercellular amorphous matrix was
still alcianophilic (Fig. 2). The
myogeneic zone was made up few,
loosely arranged, circularly oriented
smooth myocytes (Fig. 1). The
spindle-shaped
or
vermiform
mocytes
were
arranged
in
discontinuous
thin
bundles
separated by irregular areas of
mesenchymal
masses.
The
mononucleated myocytes acquired
an eosinophilic and PAS positive
cytoplasm.
The
uterine
mesenchymal covering was formed
of an outer mesothelial layer and a
subjacent mesenchymal layer (Fig.
1, 2). The latter layer varied in
thickness from an area to another
and was separating the mesothelial
135
layer from the myogenic zone. In
addition
to
the
numerous
mesenchymal
cells,
the
mesenchymal layer was housing
many thin-walled blood vessels,
argyrophilc and elastic fibers (Fig.
3). The outermost mesothelial
limiting layer was in the form of a
single layer of flattened cells resting
on a distinct basal lamina.
During 210 - 300 mm CVRL stage,
the
uterine
wall
became
differentiated into three sharply
demarcated layers; an inner
endometrium (mucosa-submucosa),
middle myometrium (musculosa)
and an outer perimetrium (Fig. 4).
The uterine endometrium was
differentiated into the uterine lining
epithelium and the subjacent
mesenchymal propria-submucosa.
The epithelium was pseudostratified
columnar with an average height
about 25.917 µm in the horn (Table
1) and 25.037 µm in the body
(Table 2). Marked carboxylated
(alcianophilic) mucins were found
among the argyrophilic basement
membrane (Fig. 5, 6). The epithelial
lining
showed
slight
acid
phosphatase reaction (Fig. 7) and
strong sudanophilia (Fig. 8). The
propria-submucosa
was
still
predominantly
cellular,
characterized by the presence of an
appreciable amount of fine reticular
fibers. The intercellular matrix
showed moderate alcianophilic
reaction. The myometrium was
increased in thickness, and the
developing smooth myocytes were
mainly of circular orientation (Fig.
136
4). The muscle bundles were
interposed by loose fibrocellular
stromal
elements
comprising
fibroblasts, mast cells and reticular
fibers (Fig. 6), fine elastic fibers,
moderate acid phosphatase (Fig. 7)
and
strongly
alcianophilic
amorphous matrix. The outer
fibrous
layer
forming
the
vascularized perimetrium (Fig. 9,
10) exhibited an increase of the
fibroblasts on the expense of the
undifferentiated mesenchymal cells.
In addition to the reticular and
collagenic fibers, occasional fine
elastic fibers were noticed (Fig. 11).
The involuted mesonephric duct
was found in this layer (Fig. 4, 9).
The outermost border of the
perimetrium was lined by a single
layer of flattened squamous cells
(Fig. 11).
At 310 mm CVRL stage, the three
layers, endometrium, myometrium
and outer perimetrium, forming the
wall of the uterine body and horn
were sharply demarcated. The
endometrial epithelial lining was
still pseudostratified columnar (Fig.
12). Strong PAS and Best's carmine
positive granular reaction of the
epithelial lining was noticed (Fig.
13). The predominantly cellular
propia-submucosa had an extensive
capillary network with haemopiotic
cells. Large numbers of fibroblasts,
lymphocytes, histocytes, plasma
cells and mast cells (Fig. 14). The
thickness of the propria-submucosa
was greater in the horn (311.947
µm) in comparison to its
counterpart in the body (169.36 µm)
Farouk et al
(Table 1, 2) . The myometrium was
increased in thickness with the
advanced age particularly in the
body. The developing positive PAS
smooth myocytes were mainly of
circular orientation. Large network
of thin- walled blood vessels were
observed forming a vascular layer
separated the myometrium and the
alcianophilic perimetrium (Fig. 15).
An important notice to be
mentioned, at 330 mm CVRL stage,
the lining epithelium of the uterine
body showed shallow invaginations
in certain areas penetrated into the
underlying stroma. These epithelial
invaginations were composed of
densely packed cells having the
same
morphological
and
histochemical criteria of the
endometrial lining epithelium.The
uterine lumen irregularity was
gradually
increased,
due
to
progressive epithelial invaginations
forming epithelial clefts (Fig. 16).
At 465 – 630 mm CVRL stage, a
marked increase in the number and
size of the endometrial undulations
of the uterine body. The latter were
created as a result of progressive
invagination of the epithelial lining
into the superficial layer of the
underlying
propria-submucosa
(Fig. 17).
The endometrial
undulations in the uterine horns
appeared at 480 mm CVRL stage.
The epithelial lining of the uterine
horn showed slight reaction to acid
phosphatase (Fig. 18), and it
showed moderate PAS and Best's
carmine positive reaction (Fig. 19).
The uterine body showed moderate
SCVMJ, XVII (1) 2012
alkaline phosphatase (Fig. 20) and
moderate ATPase reaction in its
epithelial lining (Fig. 21). There
was a gradual increase in the total
thickness of the uterine wall in both
uterine horns and body. The total
thickness of the uterine wall in the
horns ranged between 512.532 to
534.7 µm (Table 1), meanwhile in
the body, it ranged between 567.653
to 591.621 µm (Table 2). The
lamina propria-submucosa became
well-differentiated into two zones; a
superficial, mainly cellular, narrow
zone and a deeper, less cellular,
wider one (Fig. 17, 22). The
superficial zone comprised a
predominance of mesenchymal
cells, fibroblasts and many fine
argyrophilic fibers (Fig. 23). The
deeper
zone
comprised
a
predominance of fibroblasts and
fine collagenic bundles, which were
comparatively denser towards the
myometrium (Fig. 17, 22). It also
comprised numerous thin-walled
blood vessels of different size and
orientation.
The
intercellular
alcianophilia in both zones was
considerably reduced. Moderate
alkaline phosphatase reaction was
noticed
(Fig.
20).The
The
myometrium
was
markedly
increased in thickness (Table 1, 2)
as a result of the gradual increase in
the number and thickness of the
circularly disposed smooth muscle
bundles (Fig. 17). In some areas,
the myometrium tended to be
incompletely differentiated into two
layers separated
by stromal
elements (Fig. 22). The myocytes
137
showed moderate reaction to acid
phosphatase (Fig.
18), ATPase
(Fig. 21) and SDH (Fig. 24). The
submesothelial
layer
of
the
perimetrium showed a pronounced
increase in its content of collagenic
fibers (Fig. 22) and developing
vascular
elements,
including
arteries, veins and lymph vessels
(Fig. 25).
From 640 mm CVRL stage on, the
endometrium was distinctly thrown
into polymorphic folds of different
size. Each fold comprised an
epithelial cap and a stromal core
derived from the superficial portion
of the propria-submucosa. The
tapered summit and sides of the
primary fold, in the uterine body
and to a lesser extent in the horn,
acquired shallow invaginations
giving it a serrated appearance (Fig.
26). The uterine epithelial lining
showed a gradual decrease in
height. It was made up of
intermingled patches of simple and
pseudostratified columnar profiles.
The epithelial lining the uterine
body showed strong reaction to both
acid and alkaline phosphatase. The
epithelial lining of the uterine horn
showed
strong
sudanophilic
reaction and a slight reaction to
SDH. The primordia of the uterine
glands were, firstly, observed in the
uterine body at 640 mm CVRL
stage and in the uterine horn at 870
mm. They were in the form of solid
cellular sprouts invaginating from
the lining epithelium into the most
superficial level of the prorpriasubmucosa (Fig. 26, 27). There was
138
no visible basal lamina surrounding
the glandular bud allowing a direct
communication
with
the
surrounding
loosely
disposed
stroma. With advancing age, the
glandular primordia were increased
in number and became gradually
canalized acquiring a simple tubular
appearance. Occasional simple
tubular branched adenomeres were
also observed at the 890 mm CVRL
stage in the uterine body (Fig. 28).
The canalized tubular adenomeres
were lined with a simple columnar
epithelium having basally located,
euchromatic nuclei with many
mitotic
figures,
and
faintly
eosinophilic,
PAS
positive
supranuclear cytoplasm (Fig. 29).
Pronounced coiling of the uterine
adenomeres was noticed at the 1230
mm CVRL stage (Fig. 29).The
endometrial propria-submucosa was
similar to that described in the
previous stages, however, the
Farouk et al
highly cellular superficial zone was
housing
the
developming
adenomeres. The deeper zone
showed a gradual increase in its
vascular and fibrous elements in
addition to a marked increase in the
number of mast cells. The
myometrium, particularly in the
body, showed a gradual increase in
thickness and became differentiated
into an inner circular and outer
longitudinal layers. The latter layer
was made up of interrupted bundles
separated by fibrocellular stromal
elements and numerous vascular
structures
(Fig.
26).
The
perimetrium showed a gradual
increase in the thickness of its
subserosal layer, which was
continuous with the stromal
elements extending into the
overlying myometrium. There was a
considerable increase in the
perimetrial vascular, neural and
fibrous elements (Fig. 30).
SCVMJ, XVII (1) 2012
139
Fig. (1) A photomicrograph of the uterine horn of 135 mm CVRL camel
fetus showing epithelial lining (E), epithelio-mesenchymal zone (I); myogeni
zone (M); outer mesenchymal covering (O). (Masson's trichrome)
Fig. (2) A photomicrograph of the uterine body of 145 mm CVRL camel
fetus showing the alcianophilic intercellular amorphous matrix (I). Uterine
epithelium (E); outer mesenchymal covering (O). (Alcian blue)
Fig. (3) A photomicrograph of the uterine horn of 150 mm CVRL camel
fetus showing epithelial lining (E); myogenic zone (M). The uterine
mesenchymal covering housing appreciable amount of elastic fibers
(arrows). (Verhoeff's method)
Fig. (4) A photomicrograph of the uterine horn of 245 mm CVRL camel
fetus showing pseudostratified epithelium lining the uterine horn (E). Note
propria-submucosa (PS); myometrium (M) and vascularized (arrowhead)
perimetrium (P). involuted mesonephric ducts (arrow). (H&E)
Fig. (5) A photomicrograph of the the uterine horn of 250 mm CVRL camel
fetus showing marked carboxylated (alcianophilic) mucins were found
among the basement membrane of the uterine epithelium (arrows). Note the
alcianophilic perimetrium (P). (Combined aldhyde fuchsin - Alcian blue)
Fig. (6) A photomicrograph of the uterine horn of 285 mm CVRL camel
fetus showing argyrophilic basement membrane (thick arrow); organization
of reticular fibers within the muscular zone (blue arrows). (Gomori's
reticulin)
Fig. (7) A cryostat section of the uterine body of 240 mm CVRL camel fetus
showing slight acid phosphatase reaction of the basal cell layer of the surface
epithelium (arrow) and moderate reaction of the muscular layer (M).
(Gomori's lead)
Fig. (8) A cryostat section of the uterine body of 240 mm CVRL camel fetus
showing strong sudanophilia in the surface epithelial lining (E) and the outer
fibrous layer of the perimetrium (P). (Sudan black-B)
Fig. (9) A photomicrograph of the uterine body of 290 mm CVRL camel
fetus showing strong PAS reaction of the basement membrane of its
epithelial lining (arrowhead). Note blood vessels (thin arrows) in the
perimetrium (P). Myometrium (M); involuted mesonephric ducts (thick
arrow) (PAS)
140
Farouk et al
Fig. (10) A photomicrograph of the uterine horn of 260 mm CVRL camel
fetus showing PAS positive basement membrane (thick arrow) of its
epithelial lining (E). Myometrium (M). Note the highly vascularized
(arrows) perimetrium (P). (Combined Alcian blue-PAS)
Fig. (11) A photomicrograph of the uterine horn of 260 mm CVRL camel
fetus showing (E); fine elastic fibers ( thick arrows) separated the
myometrium (M) from the perimetrium (P); mesothelium (thin arrows).
(Verhoeff's method)
Fig. (12) A photomicrograph of the uterine body of 310 mm CVRL camel
fetus showing the epithelial lining (E), Propria submucosa (PS),
Myometrium (M) and Perimetrium (P). (H&E)
Fig. (13) A photomicrograph of the uterine body of 330 mm CVRL camel
fetus showing Best's carmine positive granular reaction of the epithelial
lining (arrow). (Best's carmine)
Fig. (14) A photomicrograph of the uterine horn of 370 mm CVRL camel
fetus showing presence of mast cells (arrows) in the subepithelial propriasubmucosa. (Toluidine blue)
Fig. (15) A photomicrograph of the uterine horn of 315 mm CVRL camel
fetus showing large network of thin-walled blood vessels (thick arrows)
formed a vascular layer separated the myometrium (M) and the perimetrium
(p). Mesothelial layer (thin arrows) (Masson's trichrome)
SCVMJ, XVII (1) 2012
141
Fig. (16) A photomicrograph of the uterine body of 415 mm CVRL stage
showing folded mucosa (arrow); myometrium (M); involuted mesonephric
ducts (arrows) and perimetrium (P). (H&E)
Fig. (17) A photomicrograph of the uterine body of 535 mm CVRL camel
fetus showing progressive invagination of the epithelial lining into the
underlying propria-submucosa. Folded mucosa (arrow). superficial zone (S)
and deeper one (D) of the propria-submucosa. Circularly disposed smooth
muscle bundles (M). (Masson's trichrome)
Fig. (18) A cryostat section of the uterine horn of 630 mm CVRL camel
fetus showing slight acid phosphatase reaction of the surface epithelium
(arrow) and moderate reaction in the muscular layer (M). (Gomori's lead)
Fig. (19) A photomicrograph of the uterine horn of 480 mm CVRL camel
fetus showing an epithelial invagination (thick arrow). Best's carmine
positive reaction (glycogen) in the epitheliocytes (thin arrow). (Best's
carmine)
Fig. (20) A cryostat section of the uterine body of 630 mm CVRL camel
fetus showing moderate alkaline phosphatase reaction in the epithelial lining
(arrow) and in the propria-submucosa (PS). (Calcium cobalt)
Fig. (21) A cryostat section of the uterine body of 630 mm CVRL camel
fetus showing moderate ATPase reaction in the epithelial lining (arrow) and
myometrium (M). (Modified ATPase)
Fig. (22) A photomicrograph of the uterine horn of 565 mm CVRL stage
showing progressive invagination of the epithelial (arrow) lining into the
underlying propria-submucosa. Superficial zone (S) and deeper one (D) of
142
Farouk et al
the propria-submucosa. Circularly disposed smooth myocytes (M). A
pronounced increase of collagenic fibers in the perimetriun (P). (Masson's
trichrome)
Fig. (23) A photomicrograph of the uterine body of 495 mm CVRL camel
fetus showing condensation of argyrophilic fibers in the superficial zone (S)
of the lamina propria-submucosa while these fibers not included in the
deeper one (D). (Gomori's reticulin)
Fig. (24) A cryostat section of the uterine horn of 740 mm CVRL camel
fetus showing moderate SDH reaction in the myometrium (M). Epithelial
lining (E). (Nitro-blue tetrazolium)
Fig. (25) A photomicrograph of the uterine horn of 475 mm CVRL camel
fetus showing the developing vascular elements (blue arrows) within the
perimetrium (P); myometrium (M) and mesothelium (arrows). (H&E)
Fig. (26) A photomicrograph of the uterine body of 640 mm CVRL camel
fetus showing uterine gland primordia (arrows). The endometrium (EN) was
distinctly thrown into polymorphic folds. Myometrium differentiated into an
inner circular (C) and outer longitudinal (L) layers. (H&E)
Fig. (27) A photomicrograph of the uterine horn of 950 mm CVRL camel
fetus showing solid cellular sprouts invaginating from the lining epithelium
into the most superficial level of the prorpria-submucosa giving the future
uterine gland (arrows). (H&E)
SCVMJ, XVII (1) 2012
143
Fig. (28) A photomicrograph of the uterine body of 890 mm CVRL camel
fetus showing uterine gland (arrows). Ocasional simple tubular branched
adenomeres (thick arrow). (Gomori's reticulin)
Fig. (29) A photomicrograph of the uterine body of 1230 mm CVRL camel
fetus showing moderate PAS reaction of uterine gland (G). The endometrial
epithelial lining (E) also showing moderate reaction to PAS. (PAS)
Fig. (30) A photomicrograph of the uterine horn of 1230 mm CVRL camel
fetus showing distribution of fine elastic fibers (thin arrows) in the
perimetrium. Vascular elements (thick arrows). (Verhoeff's method)
Table (1): Means (M) ± standard errors (SE) of the thickness (µm) of
epithelium, endometrium, myometrium and whole wall of the uterine horn.
CVRL
(mm)
Epithelium
Endometrium
Myometrium
Uterine wall
135
20.484±3.54
285.497±11.95
42.304±6.85
402.009±26.26
200
21.204±4.59
289.713±9.52
44.82±6.33
429.599±24.71
230
24.958±6.81
298.629±17.62
50.014±9.12
446.113±23.55
250
25.917±5.35
308.661±16.72
52.932±7.55
461.672±34.79
270
27.608±6.89
311.182±20.33
58.581±8.59
466.516±35.88
285
27.395±4.52
316.968±16.68
59.087±10.44
483.285±32.65
310
25.175±3.58
320.054±19.95
59.615±10.86
492.769±36.99
350
24.51±4.36
336.457±22.32
59.662±9.58
496.308±37.44
420
20.704±5.87
337.61±24.38
62.805±8.32
510.364±37.09
470
20.581±5.25
337.75±20.29
63.483±11.54
512.532±38.91
520
20.715±3.74
342.199±23.88
66.69±9.43
523.206±37.79
630
19.24±4.22
344.647±18.69
69.501±8.99
534.7±33.38
770
18.836±3.93
346.23±22.24
72.6±10.18
537.025±35.79
890
17.492±3.22
350.08±17.63
76.922±13.38
537.716±34.98
990
17.025±3.29
354.621±20.69
76.983±9.328
542.29±39.08
1230
16.351±2.67
356.288±21.28
79.692±10.55
545.163±37.30
144
Farouk et al
Table (2): Means (M) ± standard errors (SE) of the thickness (µm) of
epithelium, endometrium, myometrium and whole wall of the uterine horn
the uterine body.
CVRL
(mm)
Epithelium
Endometrium Myometrium
135
22.023±4.68 184.287±19.16
200
23.817±5.80 195.557±25.64 51.885±11.18
230
25.11±7.99
207.638±22.3
53.067±9.32
483.08±40.6
250
25.037±3.57 196.541±21.88
55.586±9.99
498.291±35.41
270
24.457±4.96 196.003±20.37 58.902±13.38
526.671±39.11
285
24.281±3.33 193.534±20.55
61.991±12.5
542.36±41.63
310
24.22±3.60
192.337±21.8
74.483±10.77
544.892±34.34
350
22.952±4.94 192.312±19.89
77.818±9.99
557.136±38.67
420
22.368±3.06 196.574±26.77 80.641±12.84
567.002±45.77
470
21.914±3.95
201.218±27.3
86.772±10.4
567.653±40.83
520
20.809±4.63 218.771±23.37
89.58±16.68
574.84±45.02
630
18.864±5.93 235.417±29.44
90.325±9.33
591.621±44.93
770
17.277±5.60 237.905±20.26 93.358±11.64
592.079±39.73
890
17.213±3.31 246.752±27.53
96.309±10.1
596.11±41.82
990
17.19±3.819
96.873±14.02
596.642±48.55
1230
16.825±3.74 267.413±25.84 98.522±13.63
598.083±42.67
250.59±27.27
51.227±8.1
Uterine wall
432.907±36.91
473.816±45.39
SCVMJ, XVII (1) 2012
Discussion
At 135 mm CVRL camel fetus, the
developing uterus was differentiated
into a corpus uterus (body) and two
unequal horns. The uterine wall was
comprising three ill-differentiated
zones;
an
inner
epitheliomesenchymal , a middle
myogenic and an outer mesthelial
covering. By the onset of the 4th
developmental month (7cm CVRL),
Marei (1990) have cleared that the
uterine horns and body could be
recognized,
which
presenting
smooth lumina without any
irregularities in buffalo fetuses.
In 75 days, bovine fetuses,
Moustafa and Hafez (1971) and in
20 – 25 cm CVRL camel fetuses,
Awad et al (1988) recorded the
presence
of
pseudostratified
columnar cells constructing the
endometrial
epithelium.
This
finding was similar to that observed
in our work at 210 mm CVRL
stage. Meanwhile, Konishi et al
(1987) in human fetuses; Atkinson
et al (1984) in bovine fetuses and
Wiley et al (1987) in ovine fetus
have
described
the
uterine
epithelium to be a simple columnar
type. In buffalo, Marei (1990)
stated that the simple columnar
epithelium was only noticed at the
4th month of the fetal life (20 cm
CVRL). In camel, Maria et al
(1990) stated that the uterine
surface epithelium changed from
cubical to columnar type at 8-12
weeks of fetal age.
In ruminants, Taylor et al (2000)
mentioned that the uterine wall is
145
comprised of two functional
compartments, the endometrium
and
the
myometrium.
The
endometrium is the inner mucosal
lining of the uterus and is derived
from the inner layer of ductal
mesenchyme. Histologically, the
endometrium consists of two
epithelial cell types, luminal
epithelium
and
glandular
epithelium, in addition to two
stratified stromal compartments,
including a densely organized
stromal zone (stratum compactum)
and a more loosely organized
stromal zone (stratum spongiosum).
Our findings recorded that the
lamina propria-submucosa became
well-differentiated with advanced
stages into two zones; a superficial,
mainly cellular, narrow zone and a
deeper, less cellular, wider one. The
superficial zone comprised a
predominance of mesenchymal
cells, fibroblasts and many fine
argyrophilic fibers. The deeper one
comprised a predominance of
fibroblasts and fine collagenic
bundles, which were comparatively
denser towards the myometrium.
At 135 mm CVRL stage, our
investigation has clarified that the
uterine wall was comprising three
ill-differentiated zones; an inner
epitheliomesenchymal , a middle
myogenic and an outer mesthelial
covering. The myogeneic zone was
made up of loosely arranged,
circularly
oriented
smooth
myocytes. The spindle-shaped or
vermiform mocytes were arranged
in discontinuous thin bundles
146
separated by irregular areas of
mesenchymal masses. Concerning
the myometrial differentiation,
Marei (1990) stated that the foetal
mesenchyme which becomes the
endometrium and myometrium of
the adult in Egyptian water buffalo
has begun its differentiation by the
day 78th of gestation, where it was
made up of two distinct cell layers;
an inner layer of densely packed
cells and an outer loose one. Many
investigators recorded the initiation
of the mesenchymal differentiation
during fetal life in other species,
including cow (Atkinson et al,
1984), horse (Ginther, 1992), sheep
(Wiley et al, 1987), guinea pig
(Gulino et al, 1984).
In camel, Marai et al (1990) stated
that the endometrium was clearly
distinguished from the myometrium
at 16-20 weeks of foetal age. In
bovine foetal uterus, Moustafa and
Hafez (1971) mentioned that the
smooth muscle fibers appeared at
75 days (11 cm), and form
discontinuous circular layer at 101
days. Marei (1990) revealed that
the first evidence for the
differentiation of smooth muscle
among the buffalo foetal uterine
mesenchyme was noticed in 123
day old fetuses (22 cm CVRL). In
human, smooth muscle cells were
seen in the wall of the foetal uterus
just before the middle of
intrauterine life (Valdes-Dapena,
1979). Davies and Kusama (1962)
stated that well differentiated
smooth muscle was found in the
human uterine corpus at 108 mm
Farouk et al
CVRL. Konishi et al (1984b) have
demonstrated that smooth muscle
differentiation begins at 18 weeks
of gestation, and by 31 weeks, the
myometrium is formed in the outer
mesenchymal layer of the uterine
wall. Wiley et al (1987) in bovine
fetal uterus recorded that in day 90
– 100, a band of distinctly
eosinophilic cells was visible
beneath the intermediate loose layer
and were suggested to represent
differentiating smooth muscle cells
destined to develop into the inner
circular layer of the myometrium.
Our results had revealed that a
muscular zone could be noticed at
135 mm CVRL stage, it was made
up few, loosely arranged, circularly
oriented smooth myocytes. At 640
mm CVRL stage, the myometrium
became differentiated into inner
circular and outer longitudinal
layers. Gray et al (2001b) clarified
that the myometrium is the smooth
muscle component of the uterine
wall and includes an inner circular
layer derived from the intermediate
layer of ductal mesenchymal cells
and an outer longitudinal layer
derived
from
subperimetrial
mesenchyme.
The primordia of the uterine glands
were firstly observed in the uterine
body at 640 mm CVRL and in the
uterine horn at 870 mm CVRL
stage. It was increased in number
and became gradually canalized
acquiring
a
simple
tubular
appearance. In contrast, Awad et al
(1988) in she-camel fetuses, stated
that the uterine glands began to
SCVMJ, XVII (1) 2012
appear as stratification in the
endometrial epithelium at 50 – 55
cm CVRL and some were canalized
at 60 – 65 cm CVRL of the
intrauterine life. El-Tayeb (1981)
described
the
primordia
of
endometrial glands during the
CVRL 15 – 28 cm of intrauterine
life of camel fetus. Moustafa and
Hafez (1971) stated that the bovine
endometrial glands did not develop
during the first eight months of fetal
life. Bazha-Nova (1975) recorded
that the bovine uterine glands begin
to develop around the 4th
developmental month. Atkinson et
al (1984) claimed that the formation
of the bovine uterine glands was
initiated during the last month of
the fetal development as indicated
by the appearance of short epithelial
invaginations. Wiley et al (1987)
have described that the bovine
uterine glands were entirely absent
in the intercaruncular areas until
the early neonatal period, however,
simple coiled tubular glands had
begun to develop and were regular
feature of the intercaruncular area in
day 14 and older neonatal uteri. In
buffalo, Marei (1990) elucidated
that the uterine glands were entirely
absent from the buffaloes fetal
endometrium up to 9.5 month of
gestation (58 cm CVRL). In human
fetus, Witschi (1970) and ValdesDapena (1979) have mentioned that
the development of the uterine
glands was initiated between the 5th
and 7th month of gestation. Bal and
Getty (1970) have described the
presence of slight epithelial
147
invaginations in the newborn pigs
and
extensive
glandular
development by one month.
Atkinson et al (1984) mentioned
that during mid to late gestation, the
bovine endometrial epithelium was
uniformly columnar in all regions
with no undulations or glands.
Occasional simple tubular branched
adenomeres were observed at the
890 mm CVRL stage. Abdalla
(1968) postulated the tendency of
the uterine glands to divide and
recorded that the branched uterine
glands were observed at 100 – 105
CVRL of camel fetus.
The current findings revealed that
the uterine gland primordia were in
the form of solid cellular sprouts
invaginating from the lining
epithelium into the most superficial
level of the prorpria-submucosa.
There was no visible basal lamina
surrounding the glandular buds
allowing a direct communication
with the surrounding loosely
disposed mesenchymal stroma.
Similar finding was also recorded
by Bernfield et al (1984) and Marei
(1990) who suggested that the
presence of some sort of interaction
between the epithelial depressions,
which contributed the gland
primordia and the underlying
mesenchyme which required for the
initiation of glandular development.
Atkinson et al (1984) in bovine
fetus mentioned that the basal
profile of the epithelial cells in the
deeper portions of the developing
glands
formed
cytoplasmic
processes, which extended into the
148
underlying stroma, and they
claimed that some type of
epitheliomesenchymal interaction is
necessary to initiate glandular
development. Ovine uterine gland
development is initiated between
Postnatal Day (PND) 1 and PND 7,
when
shallow
epithelial
invaginations appear along the
endometrial luminal epithelium
(LE) in presumptive intercaruncular
areas (Taylor et al, 2000).
In contrast to our results, in several
mammalian species, including cattle
(Saverwein, 1954), buffalo (Tiwari,
1972), pig (Becky et al. 1999),
sheep (Bartol et al. 1988b; and
Hayashi and Spencer, 2006),
mouse (Bigsby and Cunha, 1985)
and rat (Branham and Sheehan,
1995), the uterine endometrial
glands are absent at birth and begin
to develop during the first stages of
neonatal life.
Statistical analysis to randomly
selected uterine specimens (body
and horns) revealed that, with
increasing age, the mucosal
epithelial heights were increased
followed by the gradual decline. In
the same time, the endometrial and
myometrial thickness as well as, the
whole uterine wall thickness was
increased with advanced age.
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‫‪SCVMJ, XVII (1) 2012‬‬
‫التطور النسيجى لرحم الجمل الدروميدرى‬
‫سامح فاروق‪ ،‬عبد الحميد كامل عثمان ‪ ،‬حسين عيداروس‬
‫قسم الخلية واآلنسجة‪ ،‬كلية الطب البيطري‪ ،‬جامعة قناة السويس‬
‫استهدف هذا العمل دراسة التغيرات النسيجوكيميائيه لرحم الجمل وحيد السنام فى مراحله الجنينية‬
‫المختلفة‪ .‬ولقد اجري هذا البحث على رحم ‪ 14‬جنينا والتى تتراوح اطوالها ما بين ‪ 415‬مم –‬
‫‪ 4311‬مم والتى تم جمعها من مجزر البساتين اآللى بالقاهرة ومجزر بلبيس بالشرقية‪ .‬تم اعداد‬
‫قطاعات شمعية وقطاعات مجمده لألجنة الصغيرة و لرحم األجنة األكبر حجما و تم صباغتها و‬
‫تجهيزها للفحص بالميكروسكوب الضوئى‪ .‬و لقد اظهرت نتائج تلك الدراسه ان جدار الرحم يتكون‬
‫من ثالثة طبقات مختلفة ؛ طبقة داخلية تحوى الصفيحة الطالئية المكونة من عدة خاليا كثيفة مالصقة‬
‫لبعضها البعض و طبقة خارجية يتوسطهما طبقة عضلية مرتبة بطريقة دائرية‪ .‬مع تطور العمر ‪،‬‬
‫هناك زيادة تدريجية فى سمك الطبقه العضلية الوسطى للرحم‪ .‬عند طول ‪ 165‬مم ‪ ،‬أظهرت بطانة‬
‫الرحم بعض النتوءات ا لضحلة المتوغلة الى اسفل الصفيحة الطالئية والتى تزداد تدريجيا مع زيادة‬
‫طول الجنين‪ .‬وفي هذه المرحلة‪ ،‬هناك تمايز للنسيج الميزنشيمى اسفل الصفيحة الطالئية الى‬
‫منطقتين‪ ،‬منطقة سطحية تحتوى على خاليا ميزينشيمية كثيفة و اخرى اعمق اقل كثافة‪ .‬وقد ظهرت‬
‫الغدد الرحمية في جسم الرحم عند مرحلة ‪ 611‬مم و في قرن الرحم عند ‪ 071‬مم‪ .‬ظهرت هذه الغدد‬
‫في شكل براعم خلوية صلبة من بطانة التجويف الرحمى إلى مستوى أكثر سطحية من الطبقة‬
‫الطالئية‪ .‬و قد أظهرت الطبقة العضلية زيادة تدريجية فى السمك وأصبحت متباينة إلى الطبقات‬
‫الداخلية الطولية و الطبقات الخارجية الدائرية و استمرت تلك العملية حتى اكبر األجنة موضع‬
‫الدراسة‪.‬‬