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Vascular anatomy of the rabbit ureter.

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THE ANATOMICAL RECORD 242:47-56 (1995)
Vascular Anatomy of the Rabbit Ureter
Department of Anatomy and Cell Biology, James H. Quillen College of Medicine, East
Tennessee State University, Johnson City, Tennessee
Background: The success of kidney transplant surgery and
ureteral reconstruction requires the preservation of the ureteral blood supply. Because of its potential vulnerability to surgical trauma during transplant and reconstructive surgery, the ureteral vasculature merits a full
anatomical description.
Methods: The microvascular anatomy of the ureter was studied in male
New Zealand white rabbits by light microscopy and transmission electron
microscopy and scanning electron microscopy of vascular corrosion casts
and alkali digested tissue.
Results: The rabbit ureter is supplied predominantly by a branch of the
renal artery proximally (cranial ureteral artery) and by a branch of the
vesicular artery distally (caudal ureteral artery). Minor vascular continuities are also present between the capillary beds of the ureter and those of
the renal pelvis cranially and the bladder wall caudally. There are no external vascular connections to the middle ureter with the exception of a
single, small vein which drains into the inferior vena cava. A single group
of longitudinal arteries and veins runs the full length of the ureter within
the adventitia. Branches of these longitudinal vessels pass tangentially
through the muscularis to supply a vascular complex within the lamina
propria. This complex in turn supports a rich, mucosal capillary plexus
located at the junction between the transitional epithelium and the lamina
propria. In the fixed ureter the capillary plexus lies in grooves formed by
displacement of the basal layers of the overlying transitional epithelium.
The capillaries are continuous or fenestrated, are often invested with pericytes, and are distributed uniformly around the entire circumference of
the ureter.
Conclusions: The ureteral vasculature exhibits several unique features
related to its function in urine conduction and its ability to accommodate
expansion and contraction. The combination of techniques used provides a
clear three-dimensionalview of this vasculature. Our findings also confirm
that, because of its limited blood supply, the ureter may be very susceptible
to injury during renal transplantation or other abdominal surgery.
0 1995 Wiley-Liss, Inc.
Key words: Ureter, Rabbit, Microvasculature, Capillary plexus, Vascular
corrosion cast, Scanning electron microscopy, Urothelium,
The prevention of urological complications in renal
homotransplantation and ureteral reconstruction demands a comprehensive understanding of the anatomy
of the ureter and its vasculature. The importance of
preserving the ureteral blood supply in renal transplant surgery is well documented (Salvatierra et al.,
1977; Beland, 1979; Jordan and Scaljon, 1979; Bergman, 1981). In fact, a majority of urological complications including ureteral necrosis and subsequent extravasation during renal transplant and ureteral
reconstruction surgery have been attributed t o disruption of the ureteral blood supply (Salvatierra et al.,
1977; Bergman, 1981; Benoit et al., 1984).
Although the occurrence of urological complications
in abdominal surgery has declined in the past two decades due to improved surgical techniques and greater
knowledge of the ureteral vasculature, possible trauma
to the ureter remains a major concern to surgeons
(Benoit et al., 1984). Knowledge of the ureteral blood
Received October 3, 1994; accepted November 14, 1994.
Address reprint requests to Fred E. Hossler, Department of Anatomy and Cell Biology, Box 70582, James H. Quillen College of Medicine, East Tennessee State University, Johnson City, TN 37614.
supply has clinical significance in the prevention of
accidental ligation or transection of ureteral vessels in
the performance of ureteral reconstruction and graft
surgery and in the prevention of ischemia and trauma
to the ureter during bladder surgeries, hysterectomies,
prostatectomies, colon surgery, and Cesarean sections
(Jordan and Scaljon, 1979).
The human ureter receives blood mainly from three
vascular territories: the upper ureter is fed by branches
from the renal arteries, the middle ureter by branches
from the common iliac artery, or middle ureteric artery, and the lower ureter by branches from the vesicular or uterine arteries (Daniel and Shackman, 1952).
However, a review of the literature reveals that considerable variation in ureteral blood supply exists
across mammalian species and among individuals of
the same species (Jordan and Scaljon, 1979). This perhaps should not be surprising considering that, embryologically, the mammalian ureter arises from the
mesonephric duct, and, as it grows caudocranially, receives its blood supply from branches of several segmental aortic sprouts rather than from a single major
trunk as is the case with organs such as the kidney
(Larsen, 1993). As a result, the vascular supply varies
with the length and anatomical orientation of the ureter among the various mammalian species.
In 1972, Shafik obtained crude casts of the human
ureter by injection of silastic followed by tissue digestion, but until recently most knowledge of the ureteral
blood supply has come from dye studies and gross dissection. The microvascular ultrastructure of the rabbit
ureter has not been described previously, even though
the rabbit has been an animal model of choice in studies of the human urinary system. Although considerable information exists on the vascular morphology of
the rodent kidney from vascular corrosion casts, only
recently has the corrosion cast method using polymer
plastics been employed to study the vascular network
of the guinea pig (Aharinejad et al., 1990) and human
ureter (Spaniel-Boroski et al., 1992).
The purpose of our study was to provide a comprehensive characterization of the microvascular morphology of the rabbit ureter using a combination of techniques: vascular corrosion casting, light microscopy,
scanning and transmission electron microscopy, and alkali digestion. A preliminary report of this study has
appeared in abstract form (Douglas and Hossler, 1994).
Vascular Corrosion Casts
Fig. 1. Apparatus for perfusion and corrosion casting. Aorta is cannulated above the renal arteries for perfusion of upper ureter (shown)
and below the renal arteries for perfusion of lower ureter.
femoral arteries and veins, the superior and inferior
mesenteric arteries and veins, and the deep circumflex
iliac arteries and veins were ligated to limit unnecessary perfusion. The severed vena cava served as the
site of blood exit. The vasculature was flushed for approximately 5-10 min at a pressure of 100 ? 20 mm Hg
with 0.5-1 L of warm (37"C), 0.9% NaCl in 0.01 M
phosphate, pH 7.3 (PBS), containing 10 mg/ml procaine. Resin was then infused through the same cannula via a second port on the stopcock at a pressure of
120 & 20 mm Hg until polymerization ensued (5-8
min). Resin was prepared just before use and consisted
of Mercox CL-2B (Ladd Research Industries, Burlington, VT), methyl methacrylate (Polysciences, Inc.,
Warrington, PA), and catalyst (Ladd Research Industries, Inc.) a t a ratio of 4:1:0.3 (v:v:v).
After 30 min the ureter and surrounding tissue were
dissected from the carcass and placed in 50°C tap water
for 1 h to complete resin curing. The tissue was macerated for 48 h in 10% KOH a t room temperature,
washed with hot (50"C),running tap water for 24 h or
longer, and soaked in distilled water for another 24 h.
Vascular casts of the ureter were washed once with 5%
formic acid for 15 min (Lametschwandtner et al., 1990),
twice with distilled water for 30 min, and three times
with 100% ethanol and then critical point dried (Samdri-PVT-3B Critical Point Dryer, Tousimis Research
Corp., Rockville, MD) from liquid COz. In order to view
the vasculature in the interior of the ureter, casts were
frozen in blocks of distilled water and cut with a jeweler's saw, and the resulting sections were lyophilized.
Dried casts were mounted on stubs with silver paste,
sputter-coated with gold-palladium for 120 seconds,
and viewed and photographed in a DSM 940 scanning
electron microscope (Carl Zeiss, Inc., Thornwood, NY)
at an accelerating voltage of 5 KV.
Thirty, male, New Zealand white rabbits weighing
2-2.6 kg were heparinized intraperitoneally (1,000
U/kg), allowed to rest for 30 min, and then given an
overdose of sodium pentobarbital, either intraperitoneally (100 mg/kg) or intravenously (50 mg/kg). The
abdomen was separated from the thorax at the diaphragm, and the stomach, intestines, and liver were
A flared-tip cannula (polyethylene tubing 1.57 mm
i.d. x 2.08 mm 0.d.) connected to a three-way stopcock
was inserted into the abdominal aorta and secured
with a ligature (Fig. 1). For casts of the upper ureter
Light Microscopy and Transmission Electron Microscopy
(n = 15), the cannula was introduced cranial to the
The ureteral vasculature (n = 3) was flushed free of
renal arteries, and for casts of the lower ureter (n =
lo), it was introduced caudal to the renal arteries. The blood with 500 ml of PBS solution and then fixed by
Fig. 2. Cross-section of upper ureter. A, adventitia; LP, lamina propria; M, muscularis; T, transitional epithelium. Arrows, primary longitudinal ureteral vessels. x 80.
Fig. 4. Portion of fenestrated mucosal capillary. E, endothelial cell;
L, capillary lumen. Arrowheads, basal laminae; arrows, fenestrations.
x 22,800.
Fig. 3. Cross-section through ureteral wall. L, lumen; LP, lamina
propria; M, muscularis; T, transitional epithelium. Large arrows, primary longitudinal vessels of the adventitia; small arrows, vascular
plexus of the lamina propria; arrowheads, mucosal capillary plexus.
x 250.
Fig. 5. Mucosal capillary with pericyte (P). T, transitional epithelium. x 5,500.
perfusion with 300 ml of 2% glutaraldehyde in 0.1 M
phosphate buffer (pH 7.3; 37°C) a t a pressure of 100
mm Hg. Ureters were excised, divided into upper, middle, and lower portions, cut into 3 mm segments,
washed in buffer, fixed in 1%osmium (in 0.1 M phos-
phate buffer, pH 7.3; ambient temperature) for 1 h,
dehydrated in graded ethanol solutions, and embedded
in Epon-Araldite. For light microscopy, 0.5-1 pm sections were stained with toluidine blue. For transmission electron microscopy, silver-gold sections were
Fig. 6. Corrosion cast of renal area showing blood supply to upper
ureter. A, aorta; AD, adrenal gland; K, kidney; RA, renal artery; RV,
renal vein; U, ureter; V, vena cava. Arrows, ureteral arteries. x 3.
Figs. 7, 8. Corrosion cast of hilar area of kidney. K, kidney; RA,
renal artery; RV, renal vein; U, ureter. Large arrows, ureteral arteries; small arrows, ureteral veins. Fig. 7: x 12. Fig. 8: x 6.
mounted on copper grids, stained with uranyl acetate
and lead citrate, and viewed in a JEM-100C electron
microscope (JEOL, Inc., Peabody, MA) at an accelerating voltage of 80 KV.
Alkali Digestion
Glutaraldehyde-fixed ureters were excised, cut longitudinally, washed in 0.1 M phosphate buffer (pH 7.31,
and placed in 6 N NaOH for 20-25 min a t 55°C according to the method of Takahashi-Iwanaga and Fujita
(1986). In some cases specimens were sonicated several
minutes to promote separation of tissue layers (Bransonic 220; Branson Cleaning Equipment Co., Shelton,
CT). After washing thoroughly in phosphate buffer, the
tissue was postfixed in 1%OsO, for 1 h, washed in
phosphate buffer, dehydrated in a graded ethanol series, and critical point dried from liquid CO,. Dried
specimens were mounted on stubs with silver paste,
sputter-coated with gold-palladium, and observed by
scanning electron microscopy.
Light Microscopy and Transmission Electron Microscopy
The wall of the rabbit ureter consists of three layers:
an inner mucosa comprised of a typical transitional
epithelium and a lamina propria, a middle tunic consisting of smooth muscle, and an outer adventitia or
serosa (Fig. 2).
The transitional epithelium is characteristically
thicker and more folded, and the capillary plexus underlying the epithelium is typically more dense in the
cranial and middle portions of the ureter than in the
caudal portions. The lamina propria consists of loose
connective tissue and contains numerous arterioles
and venules which supply the mucosal capillary plexus
lying a t the junction between the epithelium and lamina propria (Figs. 2, 3). The mucosal capillary plexus
extends uniformly around the full circumference of the
ureter. This plexus consists of a closely packed network
of capillaries situated within grooves formed by displacement of the basal layers of the transitional epi-
Fig. 9. Blood supply to lower ureter; corrosion cast. B, bladder; CI,
common iliac artery; U, ureter; V, vesicular artery. Arrowhead, ureteral artery and vein. x 3.
thelium. However, a pair of thin basal laminae separates the capillary endothelia from the basal epithelial
cells (Fig. 4). The capillaries are continuous or fenestrated, measure 9.33 k 1.3 km in diameter (from light
micrographs; n = 49), exhibit very few cytoplasmic
Fig. 10. Corrosion cast of lower ureter. PA and PV, primary longitudinal artery and vein; UA, ureteral
artery; UV, ureteral vein; VC, vascular complex of lamina propria. The cranial direction is to the left;
caudal is to the right. X 22.
vesicles, and are often sparsely invested with pericytes
(Fig. 5). However, most of the external surfaces of the
endothelial cells are devoid of pericytes or pericytic
The muscular layers of the cranial and middle portions of the ureter are typically 10-20 smooth muscle
cells in thickness (Fig. 3). Besides an occasional capillary, the muscularis exhibits few blood vessels with the
exception of those connecting the primary adventitial
vessels to the vascular complex of the lamina propria.
The caudal portion of the ureter adjacent t o the urinary
bladder contains a thickened muscle layer (presumably
acting as a ureteral sphincter) and a diminished mucosa.
The major longitudinal arteries and veins of the ureter are located within the collagenous adventitia of the
wall (Figs. 2, 3). This is most readily appreciated on
cross-sections of the upper and lower ureter (and on
corrosion casts; see below).
Vascular Corrosion Casts
Cranially, each ureter is supplied by a branch of the
renal artery and vein (Figs. 6-8) and caudally by a
branch of the vesicular artery and vein (Fig. 9). Hereafter, these vessels are referred to as the cranial ureteral artery and vein and the caudal ureteral artery
and vein, respectively. Upon entering the ureteral
wall, all extrinsic vessels split to form a “T”, sending
one branch cranially and another caudally (Fig. 10).
The only other blood supply to the ureter comes from
continuities with the capillary beds of the renal pelvis
proximally (Fig. 11)and the bladder distally. The entire middle ureter has no direct, extrinsic arterial supply but is usually (78% of rabbits) drained by a small,
single vein emptying into a branch of the vena cava
superior to the deep circumflex vein (Fig. 12). The vein
draining the left middle ureter is typically about 3 cm
caudal to its counterpart on the right. Thus, blood entering the ureteral vasculature at the cranial and caudal ends is distributed the entire length of the ureter
via a single set of vessels located in the adventitia.
These longitudinal arteries are accompanied by a similar set of longitudinal veins. Because of this arrangement of vessels, complete, intact casts of the entire
length of the ureter are not always obtained. However,
by injecting resin into the aorta either cranial or caudal to the renal vessels in separate experiments (see
Materials and Methods), casts of the entire length of
the ureter could be observed.
In 78% of the rabbits examined, the cranial artery
originates from the renal artery near the renal pelvis
(Fig. 7); in the other 22% it originates from the renal
artery near the abdominal aorta (Fig. 8). In all cases its
venous counterpart joins the renal vein adjacent to the
kidney. Distally, the caudal ureteral artery typically
arises from the vesicular artery about 1 or 2 cm from
the latter’s origin from the internal (or occasionally
external) iliac. Similarly, the caudal ureteral vein
empties into the vesicular vein.
The longitudinal vessels in the ureteral adventitia
send oblique branches deep through the muscular tunic
to supply the vascular complex in the lamina propria
(Figs. 10, 13). These penetrating arterioles are commonly flanked on both sides by venules (Figs. 10, 13)
and can be distinguished from the latter by their
Fig. 11. Section through renal pelvis; corrosion cast. RA and RV,
branch of renal artery and vein; U, vasculature of ureter. Arrowheads, continuities between capillary beds of ureter and renal pelvis.
x 16.
Fig. 12. Blood supply to middle ureter; corrosion cast. A, aorta; U,
ureter; V, vena cava. Arrowheads, veins connecting ureters to vena
cava. x6.
smaller, rounder, and more uniform bores and by the
shape of the endothelial nuclear impressions on the
cast surfaces (Fig. 13). In arterioles these impressions
are elongated and are regularly arranged parallel to
Fig. 13.Corrosion cast of lower ureter. a, arteries; v, veins; V, primary longitudinal vein of ureter; VC,
vascular complex of lamina propria. Arrows, tangential branches of primary ureteral vessels. The cranial
direction is to the lower left; caudal is to the upper right. X 80.
the long axis of the vessels. In veins the impressions
are rounded or oval and more randomly oriented with
regard to the vessel’s axis. The ureteral vasculature
shows no evidence of venous valves.
The three-dimensional anatomy of the mucosal capillary plexus is also well demonstrated by vascular corrosion casting (Figs. 14, 15) and by exposure through
alkali digestion (Figs. 16, 17). The plexus consists of a
closely packed array of capillaries frequently oriented
parallel with the long axis of the ureter and displaying
multiple “Y” and “T” anastomoses (Figs. 14,151. At the
many points of junction with the underlying arterioles
and venules of the lamina propria, the capillaries commonly exhibit acute “kinks” and “bends” (Fig. 15). Connections with the lamina propria are oriented radially.
Intercapillary distances range from 10-80 pm but
would likely vary considerably with distension of the
ureter. Capillary diameters typically vary from 5-15
confirms that the mucosal capillary plexus lies within
grooves in the base of the epithelium (Fig. 16) and is
supported by the dense layer of connective tissue fibers
in the lamina propria (Fig. 17).
As in the human, the rabbit ureter is situated anatomically in a protected area-retroperitoneally and
medially-against the posterior body wall. The blood
supply to the rabbit ureter is dependent almost exclusively on a single set of longitudinal vessels running
the full length of the organ. With the exception of a
small vein draining into the vena cava from the middle
ureter, blood enters and leaves this organ only at the
cranial and caudal ends. Proximally, blood is supplied
to each ureter by single branches of the renal artery
and vein (the names cranial ureteral artery and vein
are suggested), and distally by single branches of the
vesicular artery and vein (the names caudal ureteral
Alkali Digestion
artery and vein are suggested). The only other extrinDigestion with NaOH causes the wall of the ureter to sic vascular connections to the ureter include continuseparate at the junction between the lamina propria ities with the capillary beds of the kidney pelvis craniand the transitional epithelium, thus exposing the mu- ally and the bladder caudally. The consequence of such
cosal capillary plexus (Figs. 16, 17). Digestion clearly an arrangement is that most of the length of the ureter
Fig. 14. Luminal surface of mucosal capillary plexus. C, capillaries. Arrows, vascular complex of
lamina propria; arrowheads, vessels connecting vasculature of lamina propria to capillary plexus. The
cranial direction is up; caudal is down. x 200.
is completely dependent for nutrition on the integrity
of the longitudinal adventitial vessels. The rabbit ureter is similar although not identical to the human ureter in this respect.
Most of the blood to the human ureter is likewise
supplied cranially by branches of the renal artery and
caudally by branches of the vesicular, ovarian or testicular, colic, and rectal arteries (Shafik, 1972; Notley,
1978;Jordan and Scaljon, 1979).As in the rabbit, these
vessels bifurcate upon entering the wall of the ureter,
join with the longitudinal vessels of the adventitia, and
run the full ureteral length (Shafik, 1972). Blood supplied directly to the middle ureter is limited to long
peritoneal branches of the vessels mentioned above.
Again this arrangement puts the ureter at high risk in
renal transplant and other abdominal surgery. Commonly, the only blood supply to the ureter in renal
transplants is the ureteral branch of the renal artery.
This may originate anywhere along the length of the
renal artery from a site adjacent t o the aorta [25% in
human (Benoit et al., 1984); 22% in rabbit (present
study)] to a site within the kidney hilus. Therefore, any
dissection or manipulation of tissue in the area of the
kidney hilus is discouraged during transplantation
surgery (Benoit et al., 1984).
The intrinsic microvasculature of the ureter has received little attention beyond the histological level
(Shafik, 1972). One exception is an excellent study of
the guinea pig ureter using vascular corrosion casting
(Aharinejad et al., 1990). The technique of vascular
corrosion casting used in the latter and present studies
provides a three-dimensional description of the ureteral microvasculature not possible by other means.
The extrinsic blood supply to the rabbit ureter is similar to that of the guinea pig, with several important
exceptions. The proximal segment of the rabbit ureter
is supplied exclusively by branches of the renal artery,
whereas the guinea pig ureter is additionally supplied
by branches of the aorta and testicular or ovarian arteries. The middle segment of the guinea pig ureter
receives blood from the aorta and the internal iliac
artery and is drained by branches of the iliac veins and
vena cava. The middle segment of the rabbit ureter has
no extrinsic blood supply and is drained by a single
vein emptying into the vena cava. Caudally, the rabbit
ureter is supplied by the vesicular artery and vein; but
Fig. 15. Mucosal capillary plexus. Arrowhead, acute connection between capillary plexus and underlying vasculature of lamina propria. X 360.
Fig. 16. Underside of urothelium exposed by alkali digestion. Arrowheads, grooves in basal layers of
urothelium. x 600.
Fig. 17. Inner surface of lamina propria exposed by alkali digestion. C, capillaries of mucosal plexus;
LP, lamina propria. x 460.
the guinea pig ureter is supplied not only by vesicular
vessels, but also by uterine or prostatic vessels.
The intrinsic vasculature of the rabbit is very similar
to that of the guinea pig (Aharinejad et al., 1990): primary longitudinal vessels extend the full length of the
ureter within the adventitia, branches of these primary
vessels traverse the muscular layer tangentially to
supply a plexus of secondary vessels within the lamina
propria, and an unusually rich mucosal capillary
plexus occurs at the boundary between the transitional
epithelium and the lamina propria.
In the rabbit, separation of the epithelium from the
lamina propria with alkali digestion reveals that the
capillary plexus lies within a series of interconnecting
grooves in the basal layer of the overlying transitional
epithelium. While the grooves could be a consequence
of mucosal folding due to fixation or muscular contrac-
tion, this procedure does demonstrate the close association between the capillaries and the overlying epithelium. A very similar ultrastructural arrangement has
been described in the mucosa of the rat ureter (Hicks,
1966) and rat (Tatematsu et al., 1978; Inoue and Gabella, 1991) and rabbit (Hossler and Monson, 1993)
bladder. In the present study we also observed that a
pair of thin basal laminae separates the capillary endothelium from the basal layers of the transitional epithelium. The endothelial cells did not exhibit obvious
cytoplasmic vesicles, but at least some of them were
fenestrated, and many were partially enveloped with
Some of these ultrastructural features (e.g., capillary
fenestrations, proximity of capillaries to the mucosal
surface, and richness of the capillary bed) could be compatible with a fluid or electrolyte transport function of
the mucosa. Although transitional epithelia with their
mucous coatings are generally considered excellent
barriers to water and electrolyte exchange (Hicks,
1966; Parsons et al., 1990), isotope studies have provided evidence of some permeability in the bladder
(Kerr et al., 1963; Fellows and Marshall, 1972). In the
bladder, permeability of the transitional epithelium is
increased by overdistention (Levin et al., 1990; Monson
et al., 1991). A recent study has demonstrated that the
transitional epithelium of the human ureter is capable
of the uptake and metabolism of large molecular
weight substances including peroxidase (Holstein et
al., 1994). The dense capillary bed adjacent to the epithelium could thus support a transport function of the
urothelium. However, it may simply be needed to
maintain the transitional epithelium in its role as a
critical barrier between the urine and the interstitial
space. It is known, for example, that blood flow to the
bladder wall, especially the mucosa, is compromised
during distension (Dunn, 1974; Nemeth et al., 1977).
The extensive capillary supply to the epithelium
may, therefore, represent a necessary reserve during
distension. Longitudinal folds in the ureteral mucosa
permit cross-sectional expansion of the ureter during
the passage of urine, and the arrangement of the ureteral vasculature would also accommodate that expansion. Primary and secondary vessels are arranged longitudinally or tangentially, never circularly, and
although connections between the vasculature of the
lamina propria and the mucosal capillary plexus involve acute angles, the connecting vessels are oriented
Pericytes have been shown to be contractile in many
tissues and have been implicated in blood flow regulation, receptor activity, vessel structure, and permeability in capillaries (Tilton, 1991). The sparse pericyte
investment observed here would not appear sufficient
to greatly affect capillary permeability, but structural
or regulatory functions of these cells could be important, especially in relation to contraction and dilation
of the ureter.
The authors thank Dr. Steven Armstrong for his contributions to animal preparation, Ms. Judy Whitimore
for her assistance with transmission electron microscopy, and Mr. Michael McKamey for printing the figures for this manuscript.
This research was supported by a grant from the Research Development Committee at East Tennessee
State University and, in part, by NDDK grant DK
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anatomy, ureter, vascular, rabbits
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