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Journal of Reproduction and Development, Vol. 46, No.

4, 2000
Accepted for publication: April 14, 2000
The Microvasculature of the Ovary: A Review by SEM of Vascular
Corrosion Casts
Guido MACCHIARELLI
Department of Anatomy, University of Rome La Sapienza, Via A. Borelli 50,
Rome 00161, Italy
Abstract. The vascular changes of the ovary were studied by scanning electron microscopy of
vascular corrosion casts in estrous, pseudopregnant (stimulated with human chorionic
gonadotropin hCG) and pregnant rabbits. The results demonstrated that ovarian cycle and
pregnancy may induce both structural and functional changes in the ovarian vessels. In fact the
ovarian blood vessels adapted their structure to the temporary functional needs of the recruited
follicles or corpora lutea. These changes involved both larger ovarian blood vessels (supplying the
hilus and the medulla) and cortical blood vessels (supplying the luteo-follicular complexes). Hilar
and medullary blood vessels also displayed morphological devices for the continuous control of the
blood flow (spiral arteries) and for the local recirculation of endocrine products (artero-venous
contacts). Such contacts, may likely sustain a "countercurrent mechanism" which was also shown in
ovaries of other species. Scanning electron microscopy of vascular corrosion casts even
demonstrated that cortical blood vessels are subjected to continuous remodeling. SEM showed
different morphological types of vascular plexuses which supplied antral follicles (Types 12),
atretic follicles (Types 34), peri-ovulatory follicles (Type 5), growing pseudopregnant corpora lutea
(Type 6) regressing pseudopregnant corpora lutea (Type 7) and pregnant corpora lutea (Type 8). In
estrous rabbit, growing to mature follicles (Types 12) showed a gradual enlargement and
proliferation of the theca capillaries. These changes, associated with capillary hyper-
permeabilization were observed in ovulatory and post-ovulatory follicles (Type 5), after hCG
stimulation. The corpus luteum formation (Type 6 and 8) was accompanied by additional capillary
dilation, diffuse angiogenetic sprouting and organization of conspicuous venous drainage which
appeared more enhanced in pregnant (type 8) than in pseudopregnant (type 6) corpora lutea. The
regression of the corpus luteum (Type 7) was characterized by the appearance of avascular areas
within the gland and by regression of vascular dilatation. Finally, in estrous rabbit the atretic
follicles (Types 34) wall showed large interruptions (avascular areas) and focal invasion of the
central cavity by newly formed capillaries arranged randomly. The hCG stimulation did not affect
consistently the interstitial microvasculature. It is concluded that the gradual increase of ovarian
blood flow occuring during follicle growth and corpora lutea formation is provided by a functional
adaptation of major ovarian vessels and by capillary functional (vasodilation) and structural
(angiogenesis) support as well.
Key words: Ovary, Blood vessels, Capillary, Corrosion casts, Angiogenesis, Scanning electron
microscopy, Rabbit.
(J. Reprod. Dev. 46: 207225, 2000)
ndocrine and ovulatory activities of the ovary
have strict and continuous relationship with
Review
blood vessels changes. In fact, during the
reproductive period, the whole ovarian vascular
bed undergoes specific alterations induced by the
cyclic changes in the size and in the morphology
208 MACCHIARELLI et al.
of the ovary. These modifications, both functional
and structural in nature, mainly involve the ovarian
microvasculature supplying the luteo-follicular
complex (LFC) [15]. In addition, the vessels
forming the ovarian pedicle and running in the
hilus have structural characteristics of relevant
functional significance during the ovarian cycle [6
8].
Historical Background
The above considerations suggest that a fine
evaluation of the morphology and distribution of
ovarian vessels, especially if studied by a three-
dimensional (3D) approach, gains deep significance
to the understanding of whole ovarian function.
In the past, 3D studies of ovarian vascularization
were performed by light microscopic observations
of serial sections of dye-injected samples [912],
followed by graphic reconstruction and drawings.
Angiography [13, 14], diaphanoscopy [15, 16] and
microangiography of sectioned ovaries [15, 17] have
also been usefully applied to the study of the
anatomy and topography of the ovarian vessels.
In addition, direct observation of corroded or
clarified vascular casts, after injection of colored
latex [18, 19], Micropaque

[20], vinylite [21, 24] or


other plastic compounds [14] into the ovarian artery
of various mammals including humans revealed
fine details of vasculature. However, the
occurrence of peripheral filling defects, the
difficulty of adequately casting the venous tree,
and/or the limitations related to the naked eye
observation of these casts have certainly left several
problems unexplored.
At present, scanning electron microscopy (SEM)
of vascular corrosion casts allows the best
morphological 3D reconstruction of the vascular
supply, including its finest ramifications, in both
normal and experimental conditions, as observed
in ovary of rodents [2541], horses [42], cows [43,
44] and sheep [45, 46]. This technique allowed
significant information on the ovarian cycle, and
bet t er cl ari f i ed t he rol e of vascul ar
morphodynamics in the development of the LFC
[37, 4749]. In addition [8, 50, 51], the ovarian
vascular pedicle and its proximal ramifications
have been investigated by applying this technique.
In this review the most salient finding on the
blood vessels changes during stimulated cycles and
pregnancy as seen by vascular corrosion cast in
rabbit will be described.
Methods
Experimental protocol
Adult female New Zealand white rabbits
(Oryctolagus cuniculus), weighing 45 Kg, were
used. The animals were caged separately for 3
weeks and kept under controlled conditions (14
hours light/10 hours dark, 2022 C) with free access
to food and water. Control rabbits were in estrous.
Pseudopregnancy was induced by an i.v. injection
of 70100 I.U. of human chorionic gonadotropin
(hCG), through the external ear vein. Rabbits were
then sacrificed 1012 hours, 1271417 days after
hCG injection. Ovulation was assumed to occur
about 1012 hours after hCG administration [52].
Reflex ovulation was induced in other rabbits by
mating. The day one of pregnancy was taken to
be the following day after mating. These animals
were sacrificed at day 10 of pregnancy [8, 37].
Sampling and electron microscopy
The animals were anaesthetized with an i.v.
injection of Nembutal

(Abbot U.S.A.) (50 mg/kg
body weight). The chest was opened and the
thoracic aorta was cannulated. After washing out
the blood with physiological saline (room
temperature), a Mercox

(Okenshoji Co. Ltd.,


Tokyo, Japan) resin (50 cc) was slowly injected until
polymerization started [53]. The resin-injected
ovaries were placed for 34 hours in a warm water
bath to complete polymerization, corroded in a 10%
NaOH solution for 2448 hours at 60 C, and gently
washed for a few hours under tap water. Then,
they were immersed in distilled water for 23 days
at 60 C to completely remove macerated tissues,
and washed again under running tap water.
Ovarian vascular casts were exposed under
stereomicroscopic magnifications. Half of the
samples were frozen at 18 C and cut with a
cooled razor blade, to allow the visualization of
the internal structures of the casts. All samples
were air dried, mounted on aluminum stubs and
coated with gold or platinum [31, 3435]. SEM
observations were performed at low accelerating
voltage (37 kV), in Hitachi FE S-4000 and S2R or
Cambridge Stereoscan 150 scanning electron
microscopes.
209 THE MICROVASCULATURE OF THE OVARY
Results and Discussion
Vascolarization of the hilus and medulla
The supply of blood to the ovary in the rabbit is
different to that of other species such as the rat,
guinea pig and hamster [18, 19], primates and cattle
[3]. In these species the uterus and ovary share
common arteries and veins. A branch of the uterine
artery anastomoses with the ovarian artery to form
the ovarian branch of the uterine artery. In the
rabbit, the ovarian blood supply is largely
independent of the uterine artery [18]. The utero-
ovarian anastomosis in the rabbit is long and thin
and it is therefore not likely to be a significant
source of blood. In rabbit, the ovarian artery, after
branching from the aorta below the origin of the
renal artery divides into two branches. The caudal
branch serves the uterine tube and the uterine horn,
and the cranial branch mainly supplies the ovary
[8, 10, 18]. The venous drainage follows the same
pathway of the arterial flow.
In all samples, we observed the proper ovarian
branch of the ovarian artery (ramus ovaricus) entered
the ovarian hilus near the caudal pole of the organ
and run parallel to the major axis of the hilus. The
extraovarian venous drainage was formed by
several vessels emptying into a distal large vein
(Figs. 1, 2). The ramus ovaricus showed various
degrees of coiling and branched in the medulla
(Fig. 3). The coiling of the ramus ovaricus and its
ramifications was maintained in all samples. A
venous meshwork and/or flat vein branches closely
enveloped the arterial coils found in the hilus and
outer medulla (Fig. 4). At this level numerous
arterio-venous contacts were demonstrated in all
samples [8, 54]. The venous drainage followed the
modifications of the arterial supply.
The ramus ovaricus and its ramifications
We observed that the ramus ovaricus, e.g. the
proper ovarian branch of the ovarian artery, usually
entered the ovarian hilus as a single vessel near
the caudal pole of the organ. This seems to be the
more common situation in the rabbit [21]. The
course of ovarian arteries appears quite different
from that of veins; in fact, several collecting veins,
draining different portions of the ovary, are
normally present just outside the organ (Figs. 12)
[35].
In the specimens studied, the ramus ovaricus,
when approaching the hilus, characteristically
showed various degrees of coiling. The coiling
was also present in the hilar portion (and its
Figs. 1, 2. View of the surface of a vascular corrosion cast of the rabbit ovary. The proper ovarian branch of the ovarian
artery (ramus ovaricus) (OA) and several veins (vv) are seen in the hilus. Numerous vascular plexuses of follicles
of varying size are present. Fp= pre-antral follicles, Fa= antral follicle, OV= ovarian vein. SEM: 24 Fig. 2:
From Macchiarelli et al., 1993 (Fig. 1).
210 MACCHIARELLI et al.
juxtamedullary branches) that run parallel to the
major axis of the ovary (Fig. 3). SEM studies of
vascular corrosion casts showed that spiral arteries
had a tightly coiled configuration in pig and
monkey, in the ovarian hilus as well as in the
medulla and in the cortex. On the contrary, the rat
ovary showed only straight or slightly undulated
ovarian arteries [50]. Our observations showed
that the vascular pattern of the rabbit ovary seems
to have intermediate configurations. These
differences among mammals were attributed to
differences in length of the menstrual cycle, e.g.
the arterial pattern being more complex and coiled
in animals (such as monkey) in which the
menstrual cycle is longer [50].
Spiraling of ramus ovaricus was previously
demonstrated in rabbit vinilyte-injected corroded
casts [21]. According to Reynolds [6, 55], the spiral
arteries may exert four haemodynamic functions:
a. they can "force" the blood throughout the ovary
Fig. 3. Vascular corrosion cast of rabbit ovary 12 h after hCG stimulation. The ramus ovaricus (OA) is seen entering the
ovary at its caudal pole. Isolated arterial loops are seen around one of the veins draining the ovary (vv). aa=
coiled artery running close to the ovarian hilus, F= capillary plexuses of the follicles. SEM: 15. Bar = 1 mm.
From Nottola et al., 1997 (Fig. 3).
Fig. 4. Vascular corrosion cast of rabbit ovary at 10 days of pregnancy. Note the tight spiraling of the artery (aa) and
its further ramifications (a) running close to the ovarian hilus. Close artero-venous contacts can be seen in the
same area (arrows). vv, Hilar vein. SEM: 30. Bar = 1 mm. From Nottola et al., 1997 (Fig. 4).
Fig. 5. Vascular corrosion cast of rabbit estrous ovary. Several veins are seen draining the ovary and emptying into a
larger vein (OV). Artero-venous contacts are seen between hilar vessels (arrows). OA= ramus ovaricus, aa= coiled
arteries branching close to the ovarian hilus, F= capillary plexuses of the follicles. SEM: 40. Bar = 1 mm. From
Nottola et al., 1997 (Fig. 1).
Fig. 6. Vascular corrosion cast of rabbit ovary 12 h after hCG stimulation. Small follicles (F) supplied by an arteriole
(a) directly stemming from a coiled hilar artery (A) and drained by venules (v) emptying into branches of a large
hilar vein (V) in close contact with the arterial coils are seen. SEM: 80. Bar = 300 m. From Nottola et al., 1997
(Fig. 7).
211 THE MICROVASCULATURE OF THE OVARY
acting by intermittent pulsatility; b. they can adapt
the blood supply to the changes in size of the ovary;
c. they can reduce the high blood pressure present
in the ovarian artery (3050% of abdominal aortic
pressure) and prevent the turbulence of the blood
flow increasing the diameter of the coils; d. they
can equalize the arterial flow in the ovarian hilus.
In the rabbit, the helical spirals of the ramus ovaricus
undergo a re-orientation [21], e.g. an extension
of the loops, when the size of the ovary is increased
by injection of hCG, providing the enlarging gonad
with an adequate blood supply [21, 23]. A complete
restoring of the spiral configuration of the ovarian
artery was described by Reynolds [21] to occur no
earlier than the sixth day of pseudopregnancy. In
our study, we did not observe significant structural
changes in the spiral arrangement of the ovarian
artery in the hilus and its juxtamedullary branches,
in both estrous and hCG-stimulated animals. In
particular, we observed that arterial segments or
branches in juxtamedullary position were spiraled
in both groups (Figs. 3 and 5). Presumably, the
changes in the spiraling degree reported by
Reynolds [21] involve the vessel running in the
mesovarium and not systematically studied in our
specimens, trimmed for the SEM observation,
whereas the arterial segments close to the medulla
and their first ramifications appear substantially
unaffected by hCG, being capable of a sort of
sectorial regulation of the blood flow [8, 54].
In pregnant ovaries we originally observed that
the ramus ovaricus, very long and thick, showed a
tight, although irregular, spiraling (Fig. 4) [8]. This
well correlates with the general overwhelming
vascularization shown by the whole rabbit ovary
that houses several, voluminous corpora lutea
when pregnancy is established [37].
The spiraling of the juxtamedullary portion of
the ramus ovaricus and its principal ramifications
appeared in our samples independent from hCG
stimulation and well maintained also during
pregnancy. This suggests that an adaptation of
the blood supply to the needs of the ovary may
occur in two ways: 1. cyclically (distal arterial
segments), in relation to the periovulatory events,
as previously reported [6, 21, 23]; 2. continuously
(proximal arterial segments), according to the focal,
districtual ovarian activities that involve the
follicles at various developmental stages, the
corpora lutea during growth and regression as well
as the stromal compartment.
We observed [8] small arterioles directly
stemming from the coiled arteries found in the hilus
and supplying outer cortical small follicular baskets
without running in the medullary and inner cortical
areas, as usually occurs. The same follicular baskets
showed a satellite venous drainage (Figs. 6, 7).
These follicles, for their dimensions, location and
pattern of vascularization seem actually excluded
from a full functional development [56]. On the
other hand, these follicles showed an individual
and well recognizable, although peculiar,
vascularization. Presumably they underwent
recruitment from the resting primordial pool [31],
but were stopped in their further growth and
destined to form a reservoir of steroid-synthetic cells
for the interstitial gland [35], being in any case
active in modulating a districtual control of ovarian
activities.
In fractured samples, we observed that the
arteries running in the medulla still showed
pronounced coiling (Fig. 8). The arteries branched
profusely as they course through the medulla but,
in the rabbit, we could not demonstrate the
presence of a true plexus in the cortico-medullary
region reported in other mammals [50]. Small
cortical arteries, radially oriented, arose from the
coiled and branching inner medullary arteries,
giving off arterioles which penetrate the thecae of
follicles (Fig. 9). Rich follicular capillary plexuses
were formed from these cortical arteriolar twigs
and drained by small collecting venules (Figs. 10,
11) [8, 34, 35].
The Countercurrent-Exchange Mechanism and
Its Morphological Bases Inside the Ovary
The ovarian vasculature in the rabbit receives a
modest supply from the uterine vasculature,
lacking both a prominent utero-ovarian arterial
anastomosis and a common utero-ovarian vein in
close contact with the ovarian artery, as instead it
is found in other mammals [3, 20, 57]. In these
animals, such a vascular organization permits the
local utero-ovarian transfer of a luteolytic factor,
identified as the prostaglandin (PG) F
2
, that may
directly pass into the arterial supply of the ovary
by a countercurrent veno-arterial mechanism,
thanks to the close anatomical contacts shown by
the utero-ovarian vein and the ovarian artery [7].
This local transfer, and the related ipsilateral, short-
212 MACCHIARELLI et al.
circuiting control of the luteolysis uterus-dependent
[6, 7], was not demonstrated in the rabbit [3]. Thus,
according to both anatomical characteristics and
functional behavior shown by the rabbit ovarian
vascularization, only a general, systemic regulation
of the luteolysis through the utero-pituitary-ovarian
route was considered efficient in this species [18].
Our observations confirm that, in the ovarian
vascular pedicle, although the ramus ovaricus and
the main venous vessel draining the ovary show a
common course, nevertheless close associations
between them are only rarely observed (Fig. 12)
[18]. This means that for the rabbit there is a lack
of a further general countercurrent-exchange
mechanism involving an intrinsic ovarian control.
Such a venous-arterial transfer, hypothesized (and
in a few cases demonstrated) in other species, could
allow the recirculation in the ovary of substances
(steroids, aminoacids, peptides with low molecular
wieght) discharged by the ovary itself into the
venous blood [7, 58]. Although the diffusion
distance in the walls of the ovarian vessels seems
Fig. 7. Vascular corrosion cast of rabbit ovary 12 h after hCG stimulation. Artero-venous contacts are seen between hilar
and outer medullary vessels. Note the presence of a relatively thin venous plexus (V) enmeshing the arterial coils
(A). Two small peripheral follicular baskets (F) are directly drained by venules (v) emptying into the hilar plexiform
veins. SEM: 60. Bar = 400 m. From Nottola et al., 1997 (Fig. 6).
Figs. 8, 9. Vascular corrosion casts of rabbit estrous ovary; fractured samples. The arteries (ma) maintain a spiral configuration
in the medulla, often becoming straight when they enter the cortex (ca). Capillary nets (arrowheads) can be seen
around these arteries. cv= venous ramifications in the cortex; F= follicular wall. SEM: 55. Bar = 450 m. From
Nottola et al., 1997 (Figs 11, 12).
Fig. 10. Vascular corrosion cast of rabbit estrous ovary; fractured sample. Note the presence of a straight arteriole (a)
supplying a follicular basket (F). SEM: 125. Bar = 200 m. From Nottola et al. , 1997 (Fig. 13).
213 THE MICROVASCULATURE OF THE OVARY
segments of coiled arteries and veins located in
the hilus and outer medulla (Fig. 7, 1315). These
have the morphological requisites for the
establishment, at this level, of a countercurrent-
like system allowing a veno-arterial exchange of
small molecules through the wall of the apposed
vessels, lacking between the extraovarian larger
vessels [8].
A countercurrent exchange may occur to some
extent between any closely apposed pair of arteries
and veins, and this efficiency mainly depends on
four factors: 1. area of contact, 2. difference in
concentrations between the two tubes; 3. flow rate
in the tubes; 4. resistance against the transfer [7,
58]. Thus, the equalization of blood flow suggested
by Reynolds [55] may be tuned not only by sectorial
adaptation of the vascular tree but also by the
establishment of different degrees of concentration
of solutes. The latter factor may modulate
redistribution, recirculation, and sectorial
concentration of substances involved in ovarian
physiology [14]. For example, ovarian steroid
hormones reabsorbed by branches of the ovarian
artery can locally regulate the formation of their
precursors, controlling their final production by a
negative feed-back system. However, the degree
of exchange of endogenous products may vary
throughout the cycle and/or pregnancy [7] and
their transfer needs to be evaluated under various
different and specific conditions.
It has been recently suggested that a
countercurrent exchange mechanism in the ovary
may permit a temperature gradient between
follicles and stroma. In fact, pre-ovulatory follicles
are cooler than stroma in humans and other species,
thus creating an adequate environment for meiosis
resumption [62]. On the basis of this results, it
should not be excluded that the existence of such a
temperature gradient may affect not only oocyte
maturation, but also ovulation, atresia and
ultimately fertility.
Therefore, as it results by our observations, a
countercurrent exchange may occur not only
between the utero-ovarian vein and the ovarian
artery (uterus-to-ovary control) and between the
ovarian vein and the ramus ovaricus (ovary-to-
ovary control), as above discussed, but even
between the hilar juxtamedullary and medullary
vessels. In this way, an additional vascular
morphodynamic regulation of the numerous and
complex ovarian functions is suggested,
Fig. 11. Vascular corrosion cast of rabbit estrous ovary. An
undulated arteriole (a) supplying a follicular
basket (F) is seen. v= venules. SEM: 125. Bar =
140 m. From Nottola et al., 1997 (Fig. 14).
Fig. 12. Vascular corrosion cast of rabbit ovary 12 h after
hCG stimulation. Several veins are seen draining
the ovary and emptying into a large vein (OV).
The ramus ovaricus (OA) is relatively distant from
this vein in the ovarian pedicle. aa= coiled artery
branching close to the ovarian hilus, F= capillary
plexuses of the follicles. SEM: 30. Bar = 1 mm.
From Nottola et al. , 1997 (Fig. 2).
to be considerable [59], nevertheless a local thinning
of the apposed walls of the vessels has been
reported in some mammals [60, 61].
We observed close structural relations between
214 MACCHIARELLI et al.
emphasizing a vascular role in the local, districtual
control of some paracrine activities of the ovary.
The location of a countercurrent system in the hilus
and outer medulla seems even more suitable than
the others, thanks to the reduced caliber of the
vessels involved [54].
Vascularization of the cortex
The rabbit cortical microvasculature is arranged
in differently sized vascular plexuses (VP)
supplying follicles or corpora lutea, and
surrounded to by a fine network of thin interstitial
capillaries (Fig. 16)
Intersitial stromal tissue capillaries were diffusely
distributed in the cortex among the follicular
plexuses. They were often arranged in a large
rounded-meshed network, likely supplying
primordial or primary follicles: e.g. the follicles
which are not provided with a proper techal
vascularization. The interstitial capillary
Figs. 13, 14. Vascular corrosion casts of rabbit ovary 12 h
after hCG stimulation. Note the presence of flat
venous processes covering the arterial spirals in the
juxtamedullary area. A= artery, V= vein. Fig 13,
SEM: 35; Bar = 750 m. Fig. 14, SEM: 200. Bar
= 140 m. From Nottola et al., 1997 (Figs 8, 9).
Fig. 15. Vascular corrosion cast at 10 days of pregnancy.
Hilus of the ovary. Close artero-venous contacts
are maintained during pregnancy (arrow). V= hilar
vein, A= hilar spiral artery, v= small vein draining
a peripheral cortical follicle (F) directly into the
large hilar veins. SEM: 25. Bar = 1 mm. From
Nottola et al., 1997 (Fig. 10).
morphology was poorly affected by hCG
stimulation [34].
According to the various shape and size the
following eight different morphological types of
vascular plexuses were identified 1. Early antral
follicles 2. Mature follicles 3. Small atretic follicles,
4. Large atretic folllicles 5. Peri-ovulatory follicles
6. Growing pseudopregnant corpora lutea, 7.
Regressing pseudopregnant corpora lutea 8.
Pregnant corpora lutea. The main fetaures of these
structures are briefly summarized in Table 1.
Vascular supply of developing follicles
Early antral follicles (observed in estrous rabbit)
were supplied by VP (Type 1) showing a diameter
ranging from 100 to 250 m [3436]. They were
formed by a network of thin capillaries continuous
with the surrounding stromal capillary plexus that
delimited a small empty central cavity (Figs. 16
19). The capillaries were not of sinusoidal type
215 THE MICROVASCULATURE OF THE OVARY
and formed a polygonal-mesh network similar to
that found in the interstitial stroma (Fig. 20) [34].
Mature follicles were supplied were vascular
plexuses larger than 250 m (Type 2). These were
observed in estrous rabbits and showed a more
complex organization of the their vascular bed
(Figs. 16; 2125). Their wall, in fact, was made up
of a multilayered plexus. The inner layer delimited
a large empty cavity and was formed by dilated
and tortuous typical sinusoid capillaries having
numerous angiogenetic figures (Figs. 22 and 24).
The sinusoidal capillary layer was surrounded by
numerous tortuous vessels of capillary, venular and
arteriolar nature (Figs. 2123 and 25).
According to the previous SEM studies on
ovarian vascular casts [31, 48] and to electron
microscopic data on unstimulated rabbit ovaries
[2], Types 1 and 2 VP corresponded to the theca
microvasculature of growing follicles in the
evolutive phase, from primary to preovulatory
stages [2628, 31, 34, 3749]. This VP, in fact,
displayed a gradual increase of the wall thickness,
and a development of the inner vascular layer from
a polygonal-meshed network of thin capillaries
(Type 1 VP) to a rounded-meshed network of thick
sinusoids (Type 2 VP). Therefore, the present data
clearly showed that both angiogenesis and dilation
of existing capillaries characterize the development
of a proper microvascular bed in growing follicles.
Vascular supply of atretic follicles
Small atretic follicles were supplied by
irregularly rounded or ovoid VP (Type 3) having a
diameter of about 100 to 300 mm and formed by a
polygonal-meshed network of thin capillaries that
invaded the central cavity (Figs. 26, 27). Generally,
the meshes of the network appeared larger than
those seen in the evolutive follicle (types 12) and/
or in the corpora lutea (types 67).
Large atretic follicles showed VP with a diameter
larger than 250 m (Type 4). They had a
plurilayered capillary wall with large gaps
(avascular areas) delimiting a central cavity which
was partially occupied by newly formed vessel (Fig.
28). The inner layer capillaries were not
morphologically homogeneous due to the
contemporary presence of thin straight capillaries
(45 m in diameter) and tortuous-dilated
capillaries (612 m in diameter) (Figs. 29, 30).
Types 3 and 4 VP showed significant
morphological differences from the VP of
Fig. 16. View of a freeze-fractured vascular cast of the
rabbit ovary. Medullar (M) and cortical (C) zones
are seen. Medullary vessels (arrows) and their
cortical branches supplying the follicle vascular
plexuses are exposed. Fp= pre-antral follicles, Fa=
antral follicles. SEM: 20. From Macchiarelli et al.,
1993 (Fig. 2).
216 MACCHIARELLI et al.
developing follicles. According to our observations
[35] the Type 3 VP belongs to follicles in the
degenerative type of atresia consisting in regression
and final obliteration of the follicle structures. In
fact, Type 3 plexuses were devoid of a central cavity
since it was as invaded by thin capillaries related
to the inflammatory process occurring during the
follicle regression [63]. We considered Type 4 VP
as supplying follicles in the luteinizing or
hypertrophic type of atresia according to the
observation of Guraya and Greenwald [64, 65],
since these plexuses showed tortuous and thick
capillaries, resembling sinusoids, that
characteristically supply ovarian structures with
endocrine activity [48, 56]. Therefore, Type 4 VP
are involved in the formation of the "interstitial
gland " that is known to be mainly sustained by
theca cells belonging to the so called luteinized
atretic follicles [6466]. In addition, the changes
we observed in Type 3, 4 VP were primarily
characterized by an invasion of the follicular cavity
as typically seen during inflammatory reaction. It
has been suggested that the inflammatory stimulus
can be induced by alterations in the permeability
of the follicular basal lamina [67]. Furthermore,
also the vascular changes seen in preovulatory
follicles have been considered as part of an
inflammatory event [4]. Therefore, we have reasons
to believe that the changes found in our study likely
represent a consequence of the degenerative
process, rather than an active cause of atresia [56].
As a consequence, although our data confirm
indeed the occurrence of significant vascular
changes in both luteinizing and obliterant atretic
follicles in rabbit; nevertheless, they do not fully
support the ischemic theory.
Vascular changes induced by ovulation (ovulatory
follicles and corpora lutea)
At the time of ovulation (12 hrs after hCG
stimulation), large VP (Type 5) supplied the pre-
ovulatory follicles. These VP were ovoid,
plurilayered, with large avascular areas located on
the apical pole (Fig. 31). The inner capillary
network was clearly enlarged having a sinusoidal
shape and showing numerous round resin blebs
(leakages) projecting into the inner cavity (Fig. 32).
Pseudopregnant corpora lutea were supplied by
irregular plexuses (Types 67) made of a network
of thick vessels (Figs. 33). The inner capillary
plexus was thicker, richly anastomosed and
plurilayered. Capillaries were enlarged and, in
early developing phase (Type 6) showed enhanced
sinusoidal formations with numerous resin
leakages as well as blind protrusions invading
centrum of the follicular cavity (Fig. 34).
Pregnant coprora lutea were supplied by very
rich VP (Type 810 days after matingpregnant
corpora lutea). These plexuses were large and
ovoid in shape. They presented a outer surface
made up of several thick venules, draining a dense
capillary network by tightly spiralized arteries
penetrating the body of the gland (Fig. 35). The
glandular tissue was supplied by a continuous
dense network of moderately dilated capillaries,
mainly sinusoidal in shape which seemed to
converge towards a central areas occupied by two
or three large cut venules [37].
Our observations clearly showed that hCG
stimulation induced a quick functional and
structural vascular reaction which appeared more
evident in Type 5 VP (belonging to periovulatory
Table 1. Classification of ovarian vascular plexuses
Type stage Experimental phase Size in m
1 Early antral follicles All phases 100250
2 Mature follicles > 250
3 Small atretic follicles 100300
4 Large atretic follicles > 250
5 Periovulatory follicle 1024 hrs after hCG > 800
6 Developing 27 days after hCG > 1000
Pseudopregnant CL
7 Regressing 17 days after hCG 4001200
Pseudopregnant CL
8. Pregnant CL 10 day after mating 2000
217 THE MICROVASCULATURE OF THE OVARY
Fig. 17. Rabbit ovary. Vascular corrosion cast of pre-antral follicles. The capillaries forming the follicular vascular baskets
(F) are thin. Interstitial tissue capillaries (i) form a rough reticule. SEM: 70 From Kikuta et al., 1991 (Fig. 6).
Fig. 18. Vascular corrosion cast of estrous rabbit ovary. Type 1 of vascular plexuses. View of the outer surface of the
microvasculature of a pre-antral follicle. Several thin capillaries are drained by thicker venules. SEM: 230. From
Macchiarelli et al., 1993 (Fig. 4B).
Fig. 19. Vascular corrosion cast of estrous rabbit ovary, fractured sample. Type 1 of vascular plexuses: pre-antral growing
follicle. Note the monolayered capillary wall and the central avascular cavity. SEM: 230. From Macchiarelli et
al., 1993 (Fig. 4A).
Fig. 20. Vascular corrosion cast of rabbit ovary. Interstitial-stromal capillary plexus of the inner cortex. The vascular network
shows a square mesh (asterisks). SEM: 200 From Kikuta et al., 1991 (Fig. 15); From Macchiarelli et al., 1991,
(Fig. 7).
218 MACCHIARELLI et al.
follicles) and Type 6 VP (belonging to growing
pseudopregnant corpora lutea). This reaction,
stabilized after a few days as seen in type 7 VP.
The present data morphologically confirm the
assumption that the follicular growth requires an
increase of the intraovarian blood flow likely
mainly related to two factors: 1) intraovarian
growth of new vessels (angiogenesis) and 2)
vasodilatation of existing capillaries [6, 48, 56].
The corpus luetum is indeed an endocrine gland
whi ch however pr es ent a pecul i ar
morphodynamics. In our studies the postovulatory
follicles and PPCL appeared vascularized by
straight or slightly undulated vessels. This aspect
Fig. 21. Vascular corrosion cast of rabbit ovary: small antral follicle. The follicular vascular basket is multilayered and
is formed by an inner capillary plexus surrounded by an outer layer of capillaries, arterioles and venules. SEM
90 From Macchiarelli et al., 1992a (Fig. 3A).
Fig. 22. Vascular corrosion cast of rabbit ovary. Inner aspect of the capillary plexus of an antral follicle. Capillaries run
sinusoidally (s), forming typical round meshes (asterisks). Blind ends, related to angiogenetic sprouts, are present
(arrows). SEM: 275 From Macchiarelli et al., 1992a (Fig. 3B).
Fig. 23. Vascular corrosion cast of rabbit ovary. Inner aspect of the capillary plexus of a large antral follicle. The outer
vascular layer, formed by large vessels (arrowheads), is also seen. SEM: 40 From Macchiarelli et al., 1992a (Fig.
3C).
Fig. 24. Vascular corrosion cast of rabbit ovary. Inner aspect of the capillary plexus of a large antral follicle. Note capillary
thickening and the capillary sprouts. SEM: 345 From Macchiarelli et al., 1992a (Fig. 3D).
219 THE MICROVASCULATURE OF THE OVARY
is similar to the vascular architecture found in
corpora lutea of late diestrous rats [31] and not-
pregnant pigs and monkeys [50]. Small, flat
venules were seen forming on the surface of these
PPCL through the confluence of several sinusoidal
capillaries [36]. Numerous small cortical veins
originated from the venous drainage of follicles
and PPCL and converged in large medullary veins.
These veins proceed toward the ovarian hilus and
become extraovarian, as above described.
During pregnancy, the morphology of the vessels
supplying and draining the corpora lutea appeared
greatly affected by the functional load to which
the ovary is subjected. In fact, as also reported for
the large vessels, and according to the general
enlargement of the organ, the arteries destined to
the PCL plexuses appeared as voluminous, long
vessels still showing a high degree of spiraling.
The presence of a rich venous drainage of PCL
and of the pregnant ovary itself is functionally
relevant. It is a common knowledge that there is a
large increase in total ovarian blood flow during
pregnancy in the rabbit, and that this blood flow is
mainly distributed to the highly steroid-synthetic
corpus luteum tissue [68]. Recently, to explain this
high rate of flow, it has been shown that luteal
blood capillaries are maximally dilated and
incapable of autoregulation, offering minimal
resistance to flow [69]. Therefore, according to this
view, the corpus luteum is subjected to acute
regulation of perfusion only through changes in
extra-luteal vessels. Thus, the high degree of
spiraling shown during pregnancy by the arteries
supplying the corpora lutea may be considered,
accordi ng to Reynol ds model s [55], a
morphodynamic protective device capable of
reducing the otherwise dramatically high pressure
of the blood flow destined to the corpus luteum [8,
37].
On the basis of all these data, it should be
emphasized that an adaptation of the nurse
artery (accompanied by an adequate adaptation of
t he venous dr ai nage) t o t he cycl i c
morphofunctional changes of the LFC does occur,
in both physiological and pharmacologically
induced phases of the ovarian cycle.
Concluding Remarks
Indeed, vascular corrosion cast clearly showed
Fig. 25. Vascular corrosion cast of rabbit ovary. Type 2
vascular plexuses. Outer surface of the vascular
plexus of a large (antral) follicle. Outermost thin
capillaries (arrows), larger median venule or
arterial vessels (asterisk), and innermost sinusoids
(s) can be recognized. SEM: 120 From Kikuta et
al. 1991 (Fig. 12).
Fig. 26. Vascular corrosion cast of rabbit estrous ovary.
Type 3 vascular plexuses: degenerative type of
atresia. The follicle is irregularly rounded, well
isolated from the surrounding structures and
presenting a polygonal-meshed network of thin
capillaries. SEM: 250 From Kikuta et al., 1991 (Fig.
16).
220 MACCHIARELLI et al.
Fig. 27. Vascular corrosion cast of rabbit ovary. Type 3 vascular plexuses. Outer surface of an ovoid vascular
plexus made of thin capillaries. SEM: 120 From Macchiarelli et al., 1993 (Fig. 6B).
Fig. 28. Vascular corrosion cast of rabbit ovary. Type 4 of vascular plexuses. Large, round fractured vascular plexus
showing an inner wall made of differently arranged capillaries. Note avascular areas in the inner wall
(asterisks). SEM: 230 From Macchiarelli et al., 1993 (Fig. 7A).
Fig. 29. Vascular corrosion cast of rabbit ovary. Type 4 of vascular plexuses. Higher magnification of Fig. 28; note
the occurrence of sinusoids (s) and thinner capillaries (c). SEM: 1400 From Macchiarelli et al., 1993 (Fig.
7B).
Fig. 30. Vascular corrosion casts of rabbit ovary. Type 4 of vascular plexuses. A round fractured vascular plexus
showing very dilated inner vessels. SEM: 180 From Macchiarelli et al., 1993 (Fig. 7C).
221 THE MICROVASCULATURE OF THE OVARY
Figs. 31, 32. Vascular corrosion cast of rabbit ovary. Ovulatory follicles 12 h after hCG stimulation. The apex of a
follicle (Fig. 31) and the inner aspect of the capillary plexus of another follicle (Fig. 32) are shown. Resin
leakages (arrows) are also seen. SEM: 65 From Macchiarelli et al., 1992a (Figs. 4B and 4C).
Fig. 33. Vascular corrosion cast of rabbit ovary 48 h after hCG stimulation, growing pseudopregnant corpus luteum
(PPCL). Type 6 vascular plexus. SEM: 540 From Macchiarelli et al., 1995 (Fig. 7).
222 MACCHIARELLI et al.
the occurrence of changes related to the adaptation
of the microvaculature to the functional needs of
developing follicles. In fact follicular
microvasculature first becomes independent from
the interstitial tissue vascolarization with the
formation of capillary plexuses arranged in
characteristics baskets [31]. Following this, peculiar
changes in such capillary plexuses gradually take
place. These changes consist of the development
of many sinusoids, angiogenesis (proved by the
presence of numerous capillary blind ends or
angiogenetic sprouts), the formation of an avascular
area in the apex of the preovulatory follicles (the
stigma), capillary functional changes, characterized
by increased vascular permeability. As a matter of
fact, the capillary gradually adapt their structure
and distribution not only to the incoming ovulation
(stigma formation and capillary permeabilization)
but also to the developing thecal steroidogenic
function (capillary dilation and sinusoid formation).
These morphodynamic changes reflect the
transformation of a capillary net originally
supplying a simple epithelium (those of primary
follicles) in a typical sinusoidal network supplying
an endocrine gland (thecal gland of secreting
follicle and then corpora lutea).
Finally, it may be concluded that SEM of vascular
corrosion cast allowed a detailed reconstruction of
the dynamic vascular changes occuring during
ovarian cycle. The functional and structural
changes we have demonstrated, however deserve
a deep insight through correlated morpho-fuctional
studies. In particular, we believe that relevant
information may be gained through the correlation
of biochemical data on the several growth factors
which are expressed at the time of angiogenesis
with the angiogenetic figures we have depicted.
Indeed, functional evaluation of the paracrine and
vein-artery exchanges should also be further
approached. The aim of this review would be fully
realized if our morphological approach will be of
stimulus for further correlated studies in this vein.
Fig. 34. Vascular corrosion cast of rabbit ovary 12 h after
hCG stimulation. Inner surface of a postovulatory
follicle transforming into a pseudopregnant corpus
luteum (PPCL). A slightly coiled artery (a) can be
seen supplying this structure. b, Resin blebs. SEM:
45. Bar = 600 m. From Nottola et al. 1997 (Fig.
15).
Fig. 35. Vascular corrosion cast of rabbit ovary at 10 days
of pregnancy. Note the complex vascularization of
the pregnant corpus luteum (PCL). a, long, tightly
coiled artery; v, venous drainage. SEM: 25. Bar
= 1 mm. From Nottola et al. 1997 (Fig. 18).
References
1. Bjersing L, Cajander S. Ovulation and the
mechanism of follicle rupture. VI. Ultrastructure of
theca interna and the inner vascular network
surrounding rabbit graafian follicles prior to
induced ovulation. Cell Tissue Res 1974; 153: 3144.
2. Cherney DD, DiDio LJA, Motta P. The
development of rabbit ovarian follicles following
copulation. Fertil Steril 1975; 26: 257270.
3. Ellinwood WE, Nett TM, Niswender GD. Ovarian
vasculature: Structure and function. In: Jones RE
223 THE MICROVASCULATURE OF THE OVARY
(ed.), The Vertebrate Ovary. Comparative Biology
and Evolution. Plenum Press, New York, 1978, pp
583614.
4. Espey LL. Ovulation as an inflammatory reaction.
A hypothesis. Biol Reprod 1980; 22: 73106.
5. Meyer GT. Ultrastructural dynamics during corpus
luteum development and growth. In: Familiari G,
Makabe S, Motta PM (eds.), Ultrastructure of the
Ovary. Kluwer Academic Publishers, Boston, 1991,
pp 161176.
6. Reynolds SRM. Blood and lymph vascular systems
of the ovary. In: Greep RD, Astwood EB (eds.),
Handbook of Physiology, sect 7, vol II: Female
Reproductive System, part 1. American Physiology
Society, Washington, 1973, pp 261316.
7. Einer-Jensen N. Countercurrent transfer in the
ovarian pedicle and its physiological implications.
Oxford Rev Reprod Biol 1988; 10: 348381.
8. Nottola SA, Macchiarelli G, Motta PM. The
angioarchitecture of estrous, pseudopregnant and
pregnant rabbit ovary as seen by scanning electron
microscopy of vascular corrosion casts. Cell Tissue
Res 1997; 288: 353363.
9. Basset DL. The changes in the vascular pattern of
the ovary of the albino rat during the estrous cycle.
Am J Anat 1943; 73: 251291.
10. Burr JH, Davies JI. The vascular system of the
rabbit ovary and its relationship to ovulation. Anat
Rec 1951; 111: 273297.
11. Gillet JY, Koritk JG, Muller P, Juliens C. On the
microvascularization of the rabbit ovary. Compt
Rend Soc Biol 1968; 162: 762766.
12. Gillet JY, Maillet R, Gautier C. Blood and lymph
supply of the ovary. In: Motta PM, Hafez ESE
(eds.), Biology of the Ovary. Martinus Nijhoff
Publishers, London, 1980, pp 8698.
13. Janson PO, Svendsen P. Angiographic studies of
the extrinsic vasculature of the rabbit ovary. J
Reprod Fertil 1975; 42: 175178.
14. Bendz A, Hansson HA, Svendsen P, Wiqvist N.
On the extensive contact between veins and arteries
in the human ovarian pedicle. Acta Physiol Scand
1982; 115: 179182.
15. Rodr i gues M, Di as O, Fer r ei r a AS.
Microcirculation artrielle de lovaire humain: Note
prliminaire. Bull Assoc Anat (Nancy) 1984; 68: 67
71.
16. Esperanca-Pina JA, Camisao Soares ONeill MA.
Microvascularisation artrielle de lovaire chez la
lapine en priode dovulation. Bull Assoc Anat
(Nancy) 1985; 69: 247253.
17. dos Santos-Ferreira A, Motta P, Esperanca-Pina
JA, Di Di o LJA, Cherney DD. Art eri al
microcirculation of the ovary. Int Surg 1974; 59:
100102.
18. Del Campo CH, Ginther OJ. Vascular anatomy of
the uterus and ovaries and the unilateral luteolytic
effect of the uterus: guinea pigs, rats, hamsters and
rabbits. Am J Vet Res 1972; 33: 25612578.
19. Hossain M, OShea JD. The vascular anatomy of
the ovary and the relative contribution of the
ovarian and uterine arteries to the blood supply of
the ovary in the guinea-pig. J Anat 1983; 137: 457
466.
20. Esperanca-Pina JA, Reis AM. Arterial component
of the angioarchitecture of canine ovary. Acta Anat
1984; 120: 112116.
21. Reynolds SRM. Adaptation of the spiral artery in
the rabbit ovary to changes in organ size after
stimulation by gonadotrophins: effect of ovulation
and luteinization. Endocrinology 1947; 40: 381387.
22. Reynolds SRM. Distortion of the spiral artery in
the ovary associated with corpus hemorrhagicum
cysts. Endocrinology 1947; 40: 388394.
23. Delson B, Lubin S, Reynolds SRM. Vascular
patterns in human ovaries. Am J Obstet Gynecol
1949; 57: 842853.
24. Wydrzynski M. Les artres du msovaire dans le
dveloppement ontognique de la femme. Bull
Assoc Anat (Nancy) 1988; 72: 3739.
25. Ahari nej ad SH, Lamet schwandt ner A.
Microvascular Corrosion Casting in Scanning
Electron Microscopy. Techniques and Applications.
Springer-Verlag, Wien, New York, 1992.
26. Kardon RH, Kessel RG. SEM studies on vascular
casts of the rat ovary. Scanning Electron Microsc.
1979; III: 743750.
27. Kanzaki H, Okamura H, Okuda Y, Takenaka A,
Morimoto K, Nishimura T. Scanning electron
microscopic study of rabbit ovarian follicle
microvasculature using resin injection-corrosion
casts. J. Anat. 1982; 134: 697704.
28. Kikuta A, Ohtsuka A, Ohtani O, Murakami T.
Microvascularization of endocrine glands as
studied by injection-replica SEM method. In: Motta
PM (ed.), Ultrastructure of Endocrine Cells and
Tissues. Martinus Nijhoff Publishers, Boston, 1984, pp
314320.
29. Kitai H, Yoshimura Y, Write KH, Santulli R,
Wallach EE. Microvasculature of preovulatory
follicles: comparison of in situ and in vitro perfused
rabbit ovaries following stimulation of ovulation.
Am J Obstet Gynecol 1985; 152: 889895.
30. Spanel-Borowski K, Amselgruber W, Sinowatz F.
Capillary sprouts in ovaries of immature
superstimulated golden hamster: a SEM study of
microcorrosion casts. Anat Embryol 1987; 176: 387
391.
31. Murakami T, Ikebuchi Y, Ohtsuka A, Kikuta A,
Taguchi T, Ohtani O. The blood vascular wreath
of rat ovarian follicle, with special reference to its
changes in ovulation and luteinization: a scanning
electron microscopic study of corrosion casts. Arch
Histol Cytol 1988; 51: 299313.
224 MACCHIARELLI et al.
32. Yoshimura Y, Dharmarajan AM, Gips S, Adachi
T, Hosoi Y, Atlas S, Wallach EE. Effects of
prostacyclin on ovulation and microvasculature of
the in vitro perfused rabbit ovary. Am J Obstet
Gynecol 1988; 159: 977982.
33. Okamura H. Morphological observations on
ovulation. In: Motta PM (ed.), Developments in
Ultrastructure of Reproduction. Alan R Liss Inc,
New York, 1989, pp 7990.
34. Macchiarelli G, Nottola SA, Vizza E, Kikuta A,
Murakami T, Motta PM. Ovarian microvasculature
in normal and hCG stimulated rabbits. A study of
vascular corrosion casts with particular regard to
the interstitium. J Submicrosc Cytol Pathol 1991; 23:
391395.
35. Macchiarelli G, Nottola SA, Vizza E, Familiari G,
Ki kut a A, Mur akami T, Mot t a PM.
Microvasculature of growing and atretic follicles
in the rabbit ovary: a SEM study of corrosion casts.
Arch Histol Cytol 1993; 56: 112.
36. Macchiarelli G, Nottola SA, Vizza E, Correr S,
Motta PM. Changes in ovarian microvasculature
in hCG stimulated rabbits. A scanning electron
microscopic study of corrosion casts. It J Anat
Embryol 1995; 100 (suppl 1): 469477.
37. Macchiarelli G, Nottola SA, Picucci K, Stallone T,
Motta PM. The microvasculature of the corpus
luteum in pregnant rabbit. A scanning electron
microscopy study of corrosions casts. In:
Macchiarelli G, et al. (eds.), New Trends in
Microanatomy of Reproduction, Il Sedicesimo,
Firenze. It J Anat Embryol 1998; 103 (suppl 1): 191
201.
38. Forsman AD, McCormack JT. Microcorrosion casts
of hamster luteal and follicular vasculature
throughout the estrous cycle. Anat Rec 1992; 233:
515520.
39. Patan S, Alvarez MJ, Schittny JC, Burn PH.
Intussusceptive microvascular growth: A common
alternative to capillary sprouting. Arch Histol Cytol
1992; 55 (suppl): 6575.
40. Shimoda K, Sato E, Tanaka T, Takeya T, Toyoda
Y. Morphol ogi cal di fferenti ati on of the
microvasculature during follicular development,
ovulation and luteinization of mouse ovaries.
Develop Growth Differ 1993; 35: 431437.
41. Loseke A, Spanel-Borowski K. Simple or repeated
induction of superovulation: A study on ovulation
rates and microvessel corrosion casts in ovaries of
golden hamsters. Ann Anat 1996; 178: 514.
42. Hees H, Koenig HE, Hees I. Recherches sur la
structure vasculaire du systme de vaisseaux
sanguins des structures labores au cours du cycle
ovarien chez la j ument. Une recherche au
microscope optique et au microscope balayage
lectronique. Contracept Fertil Sex 1988; 16: 521526.
43. Knig HE, Amselgruber W, Russe I. La
microcirculation dans les follicles et les corps jaunes
d'ovaires de bovins. Une etude anatomique par
corrosion. Contracept. Fertil Sex 1989; 17: 179186.
44. Yamada O, Abe M, Takehana K, Hiraga T, Iwasa
K, Hiratsuka T. Microvascular changes during the
development of follicles in bovine ovaries: A study
of corrosion casts by scanning electron microscopy.
Arch Histol Cytol 1995; 58: 567574.
45. Cavender JL, Murdoch WJ. Morphological studies
of the microcirculatory system of periovulatory
ovine follicles. Biol Reprod 1988; 39: 989997.
46. Murdoch WJ, Cavender JL. Effect of indomethacin
on the vascular architecture of preovulatory ovine
follicles: possible implication in the luteinized
unruptured follicle syndrome. Fertil Steril 1989; 51:
153155.
47. Kikuta A, Macchiarelli G, Murakami T.
Microvasculature of the ovary. In: Familiari G,
Makabe S, Motta PM (eds.), Ultrastructure of the
Ovary. Boston, Dordrecht: Kluwer Academic
Publishers, 1991, pp. 239254.
48. Macchiarelli G, Nottola SA, Kikuta A, Ohtani O,
Murakami T, Motta PM. The ovary: Three-
dimensional morphodynamics of the luteo-
follicular complex by SEM of vascular corrosion
casts and other EM techniques. In: Motta PM,
Murakami T, Fujita T (eds.), Scanning Electron
Microscopy of Vascular Casts: Methods and
Applications. Kluwer Academic Publishers, Boston,
1992, pp 245259.
49. Macchiarelli G, Vizza E, Nottola SA, Familiari G,
Motta PM. Cellular and microvascular changes of
the ovarian follicle during folliculogenesis: A
scanning electron microscopic study. Arch Histol
Cytol 1992; 55 (suppl): 191204.
50. Takada S, Shimada T, Nakamura M, Mori H,
Kigawa T. Vascular pattern of the mammalian
ovary with special reference to the three-
dimensional architecture of the spiral artery. Arch
Histol Jpn 1987; 50: 407418.
51. Nottola SA, Macchiarelli G, Vizza E, Familiari
G, Napoli M, Motta PM. Hilar vessels of the ovary
as seen by scanning electron microscopy of
vascular corrosion casts. Proceedings of the XVIII
Congress of Societ Italiana di Microscopia
Elettronica. Padova, Sept. 2428, 1991. Microscopia
Elettronica 1991; 2 (suppl.): 7778.
52. Harper MJK. Ovulation in the rabbit: the time of
follicular rupture and expulsion of the eggs, in
relation to injection of luteinizing hormone. J
Endocrin 1963; 26: 307316.
53. Murakami T. Application of the scanning electron
microscope to the study of fine distribution of the
blood vessels. Arch Histol Jpn 1971; 32: 445454.
54. Macchiarelli G, Nottola SA, Motta PM. On the
presence of extensive arterio-venous contacts in the
rabbit ovarian hilus and medulla. Ultrastructural
225 THE MICROVASCULATURE OF THE OVARY
observations by scanning electron microscopy of
vascular corrosion casts. In: Motta PM (ed.), Recent
Advances in Microscopy of Cells, Tissues and
Organs, A. Delfino Editore, Rome, Italy, 1997, pp.
519525.
55. Reynolds SRM. Morphological determinants of the
flow characteristics between an artery and its
branch, with special reference to the ovarian spiral
artery in the rabbit. Acta Anat 1948; 5: 116.
56. Greenwald GS, Terranova PF. Follicular selection
and its control. In: Knobil E, Neill G (eds.), The
Physiology of Reproduction. Raven Press Ltd, New
York, 1988, pp 387445.
57. Janson PO, Williams D, Petrucco OM, Amato F,
Seamark RF, Findlay JK. Blood flow in the ovary
and adjacent structures of the not pregnant sheep.
Acta Endocr 1983; 103: 259265.
58. Krzymowski T, Kotwica J, Stefanczyk-
Kr zymowska S. Ut er i ne and ovar i an
countercorrent pathways in the control of ovarian
function in the pig. J Reprod Fert (suppl) 1990; 40:
179191.
59. Jones RE, Summers CH, Austin HB, Smith HM,
Gleeson TT. Ovarian, oviductal and adrenal
vascular connections in female lizards. Anat Rec
1983; 206: 247255.
60. Del Campo CH, Ginther OJ. Vascular anatomy of
the uterus and ovaries and the unilateral luteolytic
effect of the uterus: histologic structure of
uteroovarian vein and ovarian artery in sheep. Am
J Vet Res 1974; 35: 397399.
61. Lee CS, OShea JD. The extrinsic blood vessels of
the ovary of the sheep. J Morphol 1976; 148: 287
304.
62. Hunter RHF, Bogh IB, Einer-Jensen N, Muller S,
Greve T. Preovulatory Graafian follicles are cooler
than neighbouring stroma in pig ovaries. Human
Reprod 2000; 15: 273283.
63. Byskov, AG. Follicular atresia. In: Jones RE (ed.),
The Vertebrate Ovary. New York, London: Plenum
Press, 1978, pp. 533562.
64. Guraya SS, Greenwald GS. Histochemical studies
on the interstitial gland in the rabbit ovary. Am J
Anat 1964a; 114: 495520.
65. Guraya SS, Greenwald GS. A Comparative
histochemical study of interstitial tissue and
follicular atresia in the mammalian ovary. Anat Rec
1964b; 149: 411434.
66. Hubbard CJ, Oxberry B. Follicular atresia. In:
Familiari G, Makabe S, Motta PM (eds.), Motta
Ultrastructure of the Ovary. Boston: Kluwer Acad.
Publishers, 1991, pp. 273285.
67. Farookhi R. Atresia, an hypothesis. In: Schwartz
NB, Hunzcken Dumm M (eds.), Dynamics of
Ovarian Function. New York: Raven Press, 1981,
pp. 1323.
68. Abdul-Karim RW, Bruce N. Blood flow to the
ovary and corpus luteum at different stages of
gestation in the rabbit. Fertil Steril 1973; 24: 4447.
69. Wiltbank MC, Gallagher KP, Christensen AK,
Brabec RK, Keyes PL. Physiological and
immunocytochemical evidence for a new concept
of blood flow regulation in the corpus luteum. Biol
Reprod 1990; 42: 139149.

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