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MICROSCOPY RESEARCH AND TECHNIQUE 42:226–233 (1998)
Testicular Microvascularization in the Common Tree Shrew
(Tupaia glis) as Revealed by Vascular Corrosion Cast/SEM
and by TEM
W. PRADIDARCHEEP,1 S. KONGSTAPONKIT,1 P. WARAKLANG,1 P. CHUNHABUNDIT,2 AND R. SOMANA1*
1Department
2Department
of Anatomy, Faculty of Science, Mahidol University, Bangkok, Thailand
of Anatomy, Faculty of Dentistry, Mahidol University, Bangkok, Thailand
KEY WORDS
testis; microcirculation; scanning electron microscope; transmission electron
microscope; vascular cast
ABSTRACT
Testicular angioarchitecture in lower primates has not been established and the
route of androgens from Leydig cells entering the systemic circulation is still a matter of controversy.
In the present study, the common tree shrew (Tupaia glis) was used as the model for vascular
corrosion cast/SEM and conventional TEM studies. With vascular corrosion cast/SEM, it was
revealed that while coursing in the spermatic cord, the testicular artery convoluted and gave off
branches to supply the epididymis, the coverings of the spermatic cord and the pampiniform plexus.
Upon approaching the testis, it encircled the organ, then penetrated into the testicular parenchyma
near the rostro-medial pole before further dividing into arterioles that gave rise to capillary plexuses
looping around the seminiferous tubules. These capillaries converged into the intratesticular
venules, then into larger venules on ventral and dorsal surfaces of the testis and finally into the
collecting veins on medial and lateral borders of the testis. In addition, the capillaries in the central
or medullary portion of the gland collected the blood into the medullary venules and central
(medullary) vein, respectively. The collecting veins as well as central vein joined together before
dividing into pampiniform plexus. With transmission electron microscopy, the capillaries in the
testis were shown to be of the thick basement membrane and continuous type. The Leydig cells were
found adjacent to lymphatic vessels among the seminiferous tubules. This structure is compatible
with the idea that most of the androgens drain into the lymphatic vessels rather than into the
capillaries. Microsc. Res. Tech. 42:226–233, 1998. r 1998 Wiley-Liss, Inc.
INTRODUCTION
The testes of most higher mammals descend into the
scrotum. Some exceptions are the elephant (Short et al.,
1967) and rock hyrax (Glover, 1973). The species having
testes permanently lodged in the abdominal cavity
have a straight testicular artery without pampiniform
plexus (Glover, 1973; Short et al., 1967). Those with
scrotal testes have a coiled testicular artery with
pampiniform plexus (Christensen, 1964; Chubb and
Desjardins, 1982; Dhingra, 1979; Ohtsuka, 1984; Osman et al., 1979; Noordhuizen-Stassen et al., 1985;
Sisson, 1969). In most animals with scrotal testis, the
testicular artery encircles the gland on the capsular
surface before arteriolization into the testicular tissue
(Chubb and Desjardins, 1982; Suzuki, 1982) but, in
man, the artery does not surround the gland and it
sends off many branches before or upon reaching the
surface of the testis (Kormano and Suoranta, 1971). In
addition, the intratesticular capillary organization varies in different mammals. In mouse, such capillary
arrangement can be visualized in a rope-ladder-like
pattern (Suzuki, 1982) while in man, the pattern does
not follow any discernible pattern (Kormano and Suoranta, 1971; Suzuki and Nagano, 1986; Takayama and
Tomoyoshi, 1981).
Three-dimensional study of the testicular vascular
pattern with the corrosion cast technique combined
r 1998 WILEY-LISS, INC.
with scanning electron microscopy has previously been
performed in only a restricted number of species,
notably, the mouse (Suzuki, 1982), rat (Ohtsuka, 1984),
and man (Suzuki and Nagano, 1986). Such studies have
not been conducted in the common tree shrew, an
animal regarded as a lower primate (DeVore and Eimerl, 1970; Palley et al., 1984). The present study,
therefore, aimed to carry out three-dimensional analysis of the vascular pattern in this animal. Additional
study with transmission electron microscopy was undertaken to determine the characteristics of the intratesticular capillaries in relation to the Leydig cells and
seminiferous tubules and of the lymphatic vessels in
the tree shrew testis.
MATERIALS AND METHODS
Eight adult male common tree shrews (Tupaia glis),
weighing between 120–180 g, were used. The preparation of animals and the injection of Batson’s no. 17
plastic mixture (casting medium) and the preparation
Contract grant sponsor: National Science and Technology Development Agency
(NSTDA).
*Correspondence to: Prof. Reon Somana, M.D., Ph.D., Department of Anatomy,
Faculty of Science, Mahidol University, Rama VI Road, Phayathai, Bangkok
10400, Thailand.
Received 23 January 1998; accepted in revised form 28 May 1998
TESTICULAR MICROVASCULARIZATION IN THE COMMON TREE SHREW TESTIS
of testicular vascular casts were processed according to
the method previously described by Chunhabundit and
Somana (1988, 1991). Each vascular cast of the testis
was air-dried, stuck onto a brass stub with silver paint,
and coated with gold/palladium prior to being examined and photographed under a scanning electron microscope at an accelerating voltage of 30 kV. For transmission electron microscopy, testes from three animals
were fixed by vascular perfusion with 2.5% glutaraldehyde in phosphate buffer, pH 7.4, and left overnight in
the same fixative at 4°C. The samples were postfixed in
1% osmium tetroxide, dehydrated in a graded series of
ethanol, infiltrated and embedded in Araldite 502 resin.
Sections 70–100 nm thick were stained with 1% uranyl
acetate, then lead citrate, and examined under a transmission electron microscope at an accelerating voltage
of 75 kV.
RESULTS
The testis of the common tree shrew is an ellipsoidal
organ with the approximate dimensions of 5 3 10 3 4
mm. The average combined weight of both testes is 1.2
g. Each testis receives arterial blood supply from the
testicular artery, which arises from the abdominal
aorta just caudal to the renal artery. Each testicular
artery runs along the side of vertebral column on the
ventral surface of the psoas major muscle, passes over
the external iliac vessels and then joins the spermatic
cord. The average diameter of the artery is 0.25 mm.
The diameter of the seminiferous tubule in this animal
is 100–200 µm.
The vascular corrosion cast technique in conjunction
with SEM at low magnification revealed the tree shrew
testis to be highly vascularized. The morphology of the
cast conforms to the appearance of the testis (Fig. 1).
The proximal portion of the testicular artery is somewhat straight, accompanied by a single testicular vein.
The artery becomes convoluted upon approaching the
pelvis. The degree of convolution gradually increases as
the artery runs caudally to the testis and is prominent
in the middle and distal portions of the spermatic cord.
The convoluting segments are surrounded by the pampiniform plexus of numerous anastomosing veins (Fig.
2). The convoluted part of the artery also gives off small
branches to supply the epididymis and the coverings of
the spermatic cord (Fig. 3). In addition, some of these
small branches give rise to vasa vasorum, supplying the
LIST OF ABBREVIATIONS
a
CoV
CV
E
EA
L
LY
LS
Pe
PP
S
ST
T
TA
v
VV
arteriole
collecting vein
central vein
epididymis
epididymal artery
lymphocyte
interstitial cell of Leydig
lymphatic space
pericyte
pampiniform plexus
seminiferous epithelium
space for seminiferous tubule
testis
testicular artery
venule
vasa vasorum
227
wall of pampiniform plexus, especially in its distal
portion (Fig. 4).
When the artery emerges from the pampiniform
plexus and approaches the testis at the rostro-medial
pole, it courses caudally along the medial border, then
rostrally along the lateral border, and finally penetrates into the testicular parenchyma near the rostral
pole (Figs. 1,5). While curving on the lateral border of
the gland, it gives off 4–5 parenchymal branches penetrating perpendicularly into the testicular tissue (Fig.
5). When viewing the cut surface of the testicular
vascular cast, it is clearly revealed that each parenchymal branch courses tortuously in parallel to the seminiferous tubule before further dividing into large and then
small arterioles in the interstitial spaces. Each small
arteriole leads into capillaries within the interstitium.
The capillary then runs either semi- or total circumferentially around the seminiferous tubules (Fig. 6). The
distal ends of these capillaries converge into intratesticular small venules (Fig. 7), which tend to run at right
angles to the testicular surfaces (Fig. 8). These small
venules drain the blood into cortical large venules on
both ventral and dorsal surfaces of the testis (Fig. 8).
The cortical venules on the ventral and dorsal surfaces
empty the blood into the collecting veins on the lateral
and medial borders of the testis, respectively (Fig. 9). In
addition, the capillaries from the medullary region of
the testis drain the blood into the intratesticular venules and finally into the medullary vein or central vein
that courses rostro-medailly (Fig. 9). The two collecting
veins as well as the central vein join together to become
the pampiniform plexus just before leaving the rostral
testicular pole (Fig. 9). Occasionally, the cortical large
venules at the upper rostral pole of ventral and dorsal
surfaces of the testis drain the blood directly into the
pampiniform plexus (Fig. 10). With TEM, it is shown
that the capillaries in the testicular tissue are without
fenestrations and have a thick basement membrane
(Fig. 11). The capillaries are not in close proximity to
the Leydig cell clusters or to the wall of seminiferous
tubules. Moreover, the lymphatic vessels are frequently
observed adjacent to the clusters of Leydig cells and to
the walls of the seminiferous tubules (Fig. 12).
DISCUSSION
The testicular arterial blood supply in the tree shrew
is similar to that in man (Kormano and Suoranta,
1971), rat (Chubb and Desjardins, 1982), and most
mammals in that it derives from a direct branch of the
abdominal aorta. However, the testicular artery of the
tree shrew almost completely encircles the testis and
sends off parenchymal branches while curving along
the lateral border of the gland. This differs from what
has been reported in rabbit (Chubb and Desjardins,
1982) and man (Kormano and Suoranta, 1971). In
rabbit, the artery encircles the testis more than once
before giving off branches into testicular tissue, while
in man, the artery does not surround the gland and it
gives off many branches immediately either before
reaching or when it is on the surface of the testis. It
seems that the rabbit testis rotates more than one turn
during the process of descending while in the tree
shrew and man testes make only one turn and less than
one turn, respectively.
Fig. 1. SEM micrograph at low magnification of testicular vascular
cast and of related organs in the tree shrew. Arrowhead, collecting
vein; E, epididymis; PP, pampinifotm plexus; T, testis; arrow, testicular artery. Bar 5 250 µm.
Fig. 2. SEM micrograph, at low magnification, of the testicular
artery in the spermatic cord. Note the coiled artery (TA) is surrounded
by pampiniform plexus (PP). Bar 5 250 µm.
Fig. 3. SEM micrograph, at low magnification, of the coiling
testicular artery (TA) in spermatic cord. Note the TA gives off branches
to supply various components of the cord. EA, epididymal artery.
Bar 5 250 µm.
Fig. 4. SEM micrograph of the spermatic cord vascular cast
showing the vasa vasorum (VV) deriving from branches of testicular
artery to supply the wall of pampiniform plexus (PP). Note the small
venule (arrow) draining the blood from VV into the vein of the
pampiniform plexus. Bar 5 100 µm.
TESTICULAR MICROVASCULARIZATION IN THE COMMON TREE SHREW TESTIS
Fig. 5. SEM micrograph of the casts of major blood vessels
supplying the tree shrew testis. Note the testicular artery (TA)
encircling the testis after emerging from the pampiniform plexus (PP).
The TA gives off branches (arrowheads) while curving along the lateral
border of the gonad. Bar 5 500 µm.
Fig. 6. SEM micrograph, at high magnification, of the testis
vascular cast illustrating a small arteriole (a) branching to form
229
capillary loops supplying each seminiferous tubule. ST, space for
seminiferous tubule. Bar 5 50 µm.
Fig. 7. SEM micrograph at high magnification of the testicular
vascular cast, intraglandular view, showing the capillaries (*) joining
each other to form small venules (v) that surround the seminiferous
tubule. Note the ovoid endothelial nuclear imprints (arrows) of the
venule. ST, space for seminiferous tubule. Bar 5 50 µm.
230
W. PRADIDARCHEEP ET AL.
Fig. 8. SEM micrograph of the upper portion of the testicular
vascular cast, dorsal view, demonstrating the intratesticular small
venules (arrowheads) draining the blood into larger venules (v) on the
testicular surface. Bar 5 500 µm.
Fig. 9. SEM micrograph, at low magnification, dorsal view, of the
testicular vascular cast showing the venules on the testicular surface
(arrowheads) joining each other to form the collecting veins (CoV) near
the borders of the gland. Note the central vein (CV) emptying the blood
from the medullary part of the testis. TA, testicular artery; PP,
pampiniform plexus; **, vascular cast of caput epididymis. Bar 5
250 µm.
Fig. 10. SEM micrograph, dorsal view, of upper medial portion of
testis vascular cast demonstrating medial collecting vein (arrow),
lateral collecting vein (arrowhead), and central vein (CV) joining to
form pampiniform plexus (PP). Note some venules (v) drain the blood
directly into the pampiniform plexus. Bar 5 250 µm.
TESTICULAR MICROVASCULARIZATION IN THE COMMON TREE SHREW TESTIS
Fig. 11. TEM micrograph of the common tree shrew testis illustrating the continuous type of capillary with thick basement membrane in
the interstitial space. Pe, pericyte. Bar 5 1 µm.
231
Fig. 12. TEM micrograph of the interstitial space of the tree
shrew testis containing blood vessels, Leydig cell (LY), and lymphatic
vessel. S, seminiferous epithelium. Note the lymphocyte (L) in the
lymphatic space (LS). Bar 5 5 µm.
232
W. PRADIDARCHEEP ET AL.
With the corrosion cast technique combined with
SEM, we clearly demonstrate that the tree shrew
testicular artery becomes coiled and is surrounded by a
pampiniform plexus while it is in the spermatic cord.
Similar findings have been reported in the camel
(Osman et al., 1979), the buffalo (Dhingra, 1979), the
mouse and rabbit (Chubb and Desjardins, 1982), as
well as in the rat (Ohtsuka, 1984). This special organization of the artery and the veins in the spermatic cord
is generally considered to be related to thermoregulation, yielding the suitable environment for spermatogenesis (Dahl et al., 1959; Fawcett, 1986; Young, 1957).
Furthermore, it may also contribute to the mechanism
for maintaining high concentrations of testosterone
intratesticularly, for the hormone is transferred from
the pampiniform plexus to the testicular artery (Amann
and Ganjam, 1976; Bayard et al., 1975; Dierschke et al.,
1975; Free and Jaffe, 1975, 1978; Free et al., 1973;
Ginther et al., 1974; Jacks and Setchell, 1973) by
diffusion (Free et al., 1973; Free, 1977) or by passing
through the arteriovenous connection (A-V shunt) in
the cord (Godinho and Setchell, 1975; NoorhuizenStassen et al., 1985). On the basis of heat exchange and
hormone transportation, the particular organization
between the testicular artery and the pampiniform
plexus is sometimes referred to as a ‘‘functional portal
system’’ (Henderson and Daneil, 1978; Ohtani, 1981). It
should be emphasized that this study is the first to
elucidate that the coiling part of the testicular artery
gives off small branches that divide into vasa vasorum
supplying the wall of the pampiniform plexus. This
finding is of interest because the vasa vasorum are
usually found to supply the thick wall of the large
vessels (Brook, 1977) whereas the wall of the pampiniform plexus in this species is somewhat thin. It is
possible that these vasa vasorum play a role in controlling the blood flow rate and consequently the blood
volume to the testis. Alternatively, they may be involved with another mechanism other than the known
countercurrent mechanism in order to increase the
blood temperature in the pampiniform plexus before it
is drained back into the body. On the other hand, the
pampiniform plexus could reduce the blood temperature before reaching the testis by absorbing the radiating heat from their encompassed artery to increase
blood temperature, especially, in the distal portion of
the pampiniform plexus. Temperature exchange may
not only be by direct heat transfer between the testicular artery and the pampiniform plexus, but also between the vasa vasorum and the pampiniform plexus,
given the abundance of the vasa vasorum in the distal
portion of the pampiniform plexus.
The organization of the capillaries in the testis has
been described as a ‘‘rope-ladder-like’’ system by Muller
(1957) and this kind of organization has been reported
for the testes of several other species (Kormano, 1967;
Setchell and Brooks, 1988; Suzuki, 1982; Weerasooiya
and Yamamoto, 1985). The present study shows that
the capillary architecture in the tree shrew testicular
parenchyma is rather similar to that in man (Suzuki
and Nagano, 1986; Takayama and Tomoyoshi, 1981) in
that there is no rope-ladder-like organization enclosing
the seminiferous tubule.
Ultrastructurally, testicular capillaries are of the
continuous nonfenestrated type. This finding is quite
unique since the capillaries in other endocrine glands of
the same animals including pineal (Chunhabundit and
Somana, 1991), thyroid (Rattanachaikunsopon et al.,
1991), pituitary (Sudwan et al., 1991), endocrine pancreas (Bamroongwong et al., 1992), and adrenal (Thongpila et al., 1997) are with fenestrations. The presence of
continuous capillaries in this endocrine gland leads to
the speculation that the androgens produced by the
Leydig cells may pass directly through the capillary
wall since the steroid hormones could easily propagate
through the cell membrane (Daryl, 1993).
By means of electron microscopy, Davidoff et al.
(1990) and Ergun et al. (1994) have shown that the
capillaries in the human testis are also found within
the lamina propria of the seminiferous tubules. Such
capillaries, called intramural capillaries, are not present in the tree shrew testis, as in rat and mouse. The
seminiferous tubules in tree shrews themselves seem to
be avascular structures. As in humans, the intramural
capillaries make close contact to cells of the seminiferous tubules, and they have been assumed to associate
with the paracrine regulation for spermatogenesis. In
tree shrew testis, the lymphatic vessels are frequently
observed in close relation to the walls of the seminiferous tubules and the clusters of the Leydig cells as has
been reported in the guinea pig and chinchilla (Fawcett
et al., 1969). Such lymphatics might play a role in the
distribution of androgens within the testis as, although
the lymph flow rate is very slow (Fawcett et al., 1969),
the wall of the lymph vessels is very thin. The route of
androgens from Leydig cells entering the systemic
circulation has been reported as being via blood (Amann
and Ganjam, 1976; Bayard et al., 1975; Free and Jaffe,
1975; Ginther et al., 1974).
The concept of blood testis barrier (BTB) is as old as
that of the blood brain barrier (BBB) and had been
derived by the scientists who observed that when dyes
were injected into animals, most tissues were stained
but not the brain or testis (Bouffard, 1906; Goldmann,
1909). The BTB is believed to be constituted by tight
junctions between Sertoli cells in the seminiferous
tubules and possibly by myoid cells that encircle these
tubules. Recently, Holash et al. (1993) using immunocytochemical and histochemical techniques, showed that
the endothelium of testicular microvessels also contributes to the BTB. The present study also demonstrates
that capillaries in the interstitium of the tree shrew
testis are with a quite thick basement membrane and
without fenestrations. Such a finding could lead to the
speculation that the thick basement membrane might
be another component of the BTB. In conclusion, the
endothelium, the thick basement membrane of the
capillaries, and the epithelial (Sertoli) components of
BTB are ‘‘in series’’ and complement each other in
achieving a stable milieu for spermatogenesis in this
animal.
SEM of microvascular corrosion casts has enabled us
to study novel aspects of arterial and venous patterns of
the tree shrew testis. It demonstrates that the main
route of the testicular artery in this animal is similar to
that of nonprimates (rat, mouse, rabbit), as it surrounds the gland before arteriolization, yet the architecture of intratesticular capillaries is similar to those of
primates (man), as the rope-ladder-like pattern is not
clearly apparent. This implies that the vascular organi-
TESTICULAR MICROVASCULARIZATION IN THE COMMON TREE SHREW TESTIS
zation of the tree shrew testis shares some characters of
both nonprimates and primates.
ACKNOWLEDGMENTS
This study was supported by Senior Fellowships,
National Science and Technology Development Agency
(NSTDA) of Thailand.
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