THE ANATOMICAL RECORD 242:47-56 (1995) Vascular Anatomy of the Rabbit Ureter GLENN C. DOUGLAS AND FRED E. HOSSLER Department of Anatomy and Cell Biology, James H. Quillen College of Medicine, East Tennessee State University, Johnson City, Tennessee ABSTRACT 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, Pericyte 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). 0 1995 WILEY-LISS, INC 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. 48 G.C. DOUGLAS AND F.E. HOSSLER 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). MATERIALS AND METHODS 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 removed. 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 VASCULAR ANATOMY OF THE URETER 49 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 50 G.C. DOUGLAS AND F.E. HOSSLER 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. VASCULAR ANATOMY OF THE URETER 51 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. RESULTS 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. 52 G.C. DOUGLAS AND F.E. HOSSLER 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 processes. 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 53 VASCULAR ANATOMY OF THE URETER 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 pm. 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). DISCUSSION 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 54 G.C. DOUGLAS AND F.E. HOSSLER 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 VASCULAR ANATOMY OF THE URETER 55 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 pericytes. 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 56 G.C. DOUGLAS AND F.E. HOSSLER 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 radially. 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. ACKNOWLEDGMENTS 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. 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