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Experimental Hydronephrosis: Retro-Aortic Transposition of Left Ureter
THE JOURNAL OF UROLOGY
Vol. 89, No. 5 May 1963 Copyright © 1963 by The Williams & Wilkins Co. Printed in U.S.A..
EXPERIMENTAL HYDRONEPHROSIS: RETRO-AORTIC TRANSPOSITION OF LEFT URETER ABRAHAM T. K. COCKETT
AND
J.B. FITZGERALD*
From the Department of Experimental Surgery, United States Air Force School of Aerospace Medicine, Aerospace Medical Division, Brooks Air Force Base, Texas and the Divisions of Urology, Harbor General Hospital, Torrance, and University of California Medical Center, Los Angeles, Cal.
The etiology of hydronephrosis has aroused interest and, to a lesser degree, controversy for more than a century. Several of the many theories which have been offered to explain the genesis of hydronephrosis remain prominent. It is probably true however, that no single common factor can be implicated in the sequence of events leading to hydronephrosis in all cases. Early studies of hydronephrosis emphasized mechanical obstruction of the upper urinary outflow tract. 1 • 2 More recently Creevy 3 and Jewett4 have listed the most frequent causes of mechanical obstruction at the ureteropelvic junction. Both authors emphasized the importance of fibrosis with stricture formation in many forms of obstruction. Jewett found accessory renal vessels as the probable cause of hydronephrosis in 24 of 71 cases (34 per cent). Hellstrom 5 stated that aberrant vessels may be responsible for hydronephrosis in half of all cases. Quinby 6 indicated that continued pounding of an artery ~gainst the ureter may disturb peristalsis sufficiently to produce hydronephrosis. Accepted for publication October 30, 1962. Supported in part by Grant No. P 131 from the Attending Staff Association, Harbor General Hospital. * Present address: Department of Surgery, Baylor School of Medicine, Houston, Texas. 1 Young, H. H.: Obstruction to the ureter produced by aberrant blood vessels. Surg., Gynec. & Obst., 54: 26-38, 1932. 2 Murnaghan, G. F.: Mechanism of congenital hydronephrosis with reference to factors influencing surgical treatment. Ann. R. Coll. Surgeons England, 23: 25-46, 1958. 3 Creevy, C. D.: The operative treatment of hydronephrosis due to obstruction at the ureteropelvic junction, Surgery, 1: 228-237, 1937. 4 Jewett, H. J.: Stenosis of the ureteropelvic juncture; congenital and acquired. J. Urol., 44: 247-258, 1940. 5 Hellstrom, J.: Contribution to knowledge of relation of abnormally running renal vessels to hydronephrosis and investigation of arterial conditions in 50 kidneys. Acta. chir. Scandinav.,
61: 289-330, 1927. 6 Quinby, W. C.: Factors influencing operative procedure in hydronephrosis. J. A. M. A., 93:
1709-1710, 1929. 656
Spontaneous development of right hydronephrosis in young rats of a highly inbred strain has recently been described by Sellers and associates. 7 Hydronephrosis in these rats was due to partial obstruction of the ureter by an ovarian or internal spermatic artery lying in close apposition to the ureter. Our experiments were designed to develop a method for the production of hydronephrosis. Structural and functional changes in the affected kidney pelvis and ureter which occur when that organ is placed in intimate association with a pulsating artery were evaluated. METHODS
One ureter in each of 24 healthy adult mongrel dogs was brought into close contact with: 1) the external iliac artery, 2) the inferior mesenteric artery, or 3) the aorta and inferior mesenteric artery. All operations were performed aseptically through a midline abdominal incision with the dogs under sodium pentobarbital anesthesia. Excretory urograms with 15 to 20 ml. 50 per cent diatrizoate were made before surgery in each dog. Group 1. Ureter behind external iliac artery (4 dogs). The left ureter was placed between the left external iliac artery and the left posterior iliac vein in each dog. The left external iliac artery was doubly clamped and divided immediately proximal to the origin of its deep femoral branch. Both ureters were freed of their attachments at the junction of their middle and distal thirds. The left ureter was placed between the posterior iliac vein and the external iliac artery, and the right ureter was replaced in its normal bed (fig. 1). The continuity of the left iliac artery was reestablished. The vascular anastomosis in the external iliac artery was lateral and distal to the route of intact left ureter. Excretory urograms were obtained at postoperative intervals of 2, 4, and 6 months in 2 dogs and 2, 4, 6 and 12 months 7 Sellers, A. L., Rosenfeld, S. and Friedman, N. B.: Spontaneous hydronephrosis in the rat. Proc. Soc. Exp. Biol. Med., 104: 512-515, 1960.
EXPERIMENTAL HYDRONEPHROSIS
Frn. 1. Left ureter coursrng behind external iliac artery. in 2 dogs. The animals were killed and an autopsy was performed: 1 dog, 6 months after operation; 1 dog, 9 months after operation; and 2 dogs, 12 months after surgery. Group 2. Ureter anterior to inferior mesenteric artery (10 dogs). The right ureter in each dog was brought from its normal retroperitoneal position to a new location anterior to the inferior mesenteric artery. The abdominal aorta was doubly clamped and divided both above and below the origin of the inferior mesenteric artery. The right ureter was freed at the junction of its middle and upper thirds, and the segment of aorta with attached inferior mesenteric artery was passed from right to left posterior to~ ureter. The right ureter was now in a position anterior to and in intimate contact with inferior mesenteric artery (fig. 2). The left ureter was freed of its attachments at the junction of middle and upper thirds and was then replaced in its usual position. Postoperative excretory urograms were obtained at 2-month intervals. Group 3. Left retro-aortic ureter (10 dogs). The left ureter in each dog was brought to a new location behind the aorta (fig. 3). Both ureters were freed of their attachments at the junction
657
Frn. 2. Right ureter anterior to inferior mesenteric artery.
1
Frn. 3. Retro-aortic transposition of left ureter of their upper and middle thirds. The aorta was doubly clamped and divided both above and below the origin of inferior mesenteric artery. The segment of aorta with attached inferior
658
COCKETT AND FITZGERALD
mesenteric artery was passed behind left ureter, and aortic continuity was re-established. The left ureter now had a course posterior to the aorta, anterior to the inferior mesenteric artery at its origin on the right, and posterior to the aorta. The freed segment of right ureter was replaced in its usual position. Excretory urograms were made at 2 month intervals after operation. One dog died during surgery. One dog escaped from the outdoor compound 6 months after surgery. Six animals were sacrificed: 1 dog 5 months after operation, 1 dog 6 months after surgery, 1 dog 9 months after surgery, and 3 dogs 12 months after surgery. The remaining 2 dogs are awaiting 12 month sacrifices. The ureters were not divided in any of these experiments. RESULTS
Periodic excretory urograms after intervals as long as 12 months revealed neither functional abnormalities nor hydronephrosis in the 4 dogs of group 1, whose ureter had been placed between the iliac vessels. Similar x-ray studies performed as long as 12 months after operation in 10 dogs of group 2, whose ureters were placed anterior to inferior mesenteric artery, revealed no changes in the renal outflow system. Figure 4 shows a hydration urogram performed 12 months after operation in a dog belonging to group 2. There is no suggestion of ureterectasis or of hydronephrosis. Excretory urograms were performed periodically for 6 to 12 months postoperatively. Six dogs in group 3, whose ureters were placed in a
FIG. 4. Hydration pyelogram on group 2 animal
retroaortic position, showed moderate to moderately severe hydronephrosis (fig. 5,A-C). In a seventh animal, early hydronephrotic changes were already apparent 5 months after operation (fig. 5,D). The opposite, control ureters were normal. DISCUSSION
These findings suggest the importance of 2 factors in the genesis of hydronephrosis: continued arterial pulsation combined with partial ureteral obstruction. While a continued arterial pulse was in apposition to the middle and lowermiddle thirds of the ureter in other groups of animals, this pulsation did not appear to be significant in the formation of hydronephrosis. It is possible that the junction of middle ureter with upper ureter differs structurally from the more distal ureter. Of significance is the absence of hydronephrotic
FIG. 5. A, delayed pyelogram in group 3 animal 1 year after surgery. B, moderately severe left hydronephrosis in another group 3 animal 1 year after surgery. C, moderately severe left hydronephrosis with ureterectasis in a third animal (group 3) 1 year after surgery. D, early ureterectasis and slight pelviectasis in group 3 animal 5 months following surgery.
EXPERIMENTAL HYDRONEPHROSIS
changes in the opposite control ureters. By careful dissection, the exact extent of ureter lying opposite the surgically displaced ureter was freed from its normal bed before allowing it to be replaced in its usual position. In several recent experiments in which a left retro-aortic ureter was surgically created, intraluminal pressure tracings of both ureters revealed a significant elevation in pressure proximal to the site of partial ureteral obstruction. A pressure of 155 mm. water was noted on the left compared to a control of 30 to 43 mm. water. Pressures were obtained by cannulating each ureter in the lower third through a ureterotomy. Catheters were passed proximally into the renal pelvis and a pressure transducer system connected to a recorder was used. Care ,Yas taken to prevent total ureteral obstruction by utilizing small polyethylene catheters. Positive radiographic findings were evident by excretory urography within 5 months after operation in animals from group 3 (retro-aortic left ureter). In several animals accentuation of hydronephrosis with ureterectasis and pelviectasis was obtained by hydrating the animals before urography. Dilatation of the upper ureters and pelvis extended from the site of obstruction in proximal fashion. In a subsequent paper detailed histologic changes in group 3 animals extending from the site of partial ureteral obstruction and diminish-
659
ing proximally will be reported. Structural changes within the intima and media of the ureters will be emphasized and will be compared to control ureters on the opposite side. SUMMARY AND CONCLUSIONS
A method for the experimental production of hydronephrosis is presented. Ureterectasis and pelviectasis were created in seven of 9 dogs by displacing an intact ureter to a position behind the aorta. The role of continued arterial pulsation with and without partial ureteral obstruction is discussed in the genesis of hydronephrosis. Radiographic changes indicated moderately severe hydronephrosis in dogs (group 3). These changes extended from the site of obstruction proximally. Intraluminal uretcral pressures are discussed. No abnormalities of the ureter or of the renal pelvis were observed in dogs (groups 1 and 2) after displacement of intact ureter to intimate contact with external iliac or inferior mesenteric arteries. The authors gratefully acknmdedge the support and encouragen1ent of Dr. \Villard E. Goodwin, Department of Surgery, l'niversity of California Medical Center, Los )1.ngeles; and Major E. V. Dahl, formerly chief of the Department of Pathology, School of Aerospace l\fedicine, Brooks )cFB, Texas.
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Vol. 89, No. 5 May 1963 Copyright © 1963 by The Williams & Wilkins Co. Printed in U.S.A..
EXPERIMENTAL HYDRONEPHROSIS: RETRO-AORTIC TRANSPOSITION OF LEFT URETER ABRAHAM T. K. COCKETT
AND
J.B. FITZGERALD*
From the Department of Experimental Surgery, United States Air Force School of Aerospace Medicine, Aerospace Medical Division, Brooks Air Force Base, Texas and the Divisions of Urology, Harbor General Hospital, Torrance, and University of California Medical Center, Los Angeles, Cal.
The etiology of hydronephrosis has aroused interest and, to a lesser degree, controversy for more than a century. Several of the many theories which have been offered to explain the genesis of hydronephrosis remain prominent. It is probably true however, that no single common factor can be implicated in the sequence of events leading to hydronephrosis in all cases. Early studies of hydronephrosis emphasized mechanical obstruction of the upper urinary outflow tract. 1 • 2 More recently Creevy 3 and Jewett4 have listed the most frequent causes of mechanical obstruction at the ureteropelvic junction. Both authors emphasized the importance of fibrosis with stricture formation in many forms of obstruction. Jewett found accessory renal vessels as the probable cause of hydronephrosis in 24 of 71 cases (34 per cent). Hellstrom 5 stated that aberrant vessels may be responsible for hydronephrosis in half of all cases. Quinby 6 indicated that continued pounding of an artery ~gainst the ureter may disturb peristalsis sufficiently to produce hydronephrosis. Accepted for publication October 30, 1962. Supported in part by Grant No. P 131 from the Attending Staff Association, Harbor General Hospital. * Present address: Department of Surgery, Baylor School of Medicine, Houston, Texas. 1 Young, H. H.: Obstruction to the ureter produced by aberrant blood vessels. Surg., Gynec. & Obst., 54: 26-38, 1932. 2 Murnaghan, G. F.: Mechanism of congenital hydronephrosis with reference to factors influencing surgical treatment. Ann. R. Coll. Surgeons England, 23: 25-46, 1958. 3 Creevy, C. D.: The operative treatment of hydronephrosis due to obstruction at the ureteropelvic junction, Surgery, 1: 228-237, 1937. 4 Jewett, H. J.: Stenosis of the ureteropelvic juncture; congenital and acquired. J. Urol., 44: 247-258, 1940. 5 Hellstrom, J.: Contribution to knowledge of relation of abnormally running renal vessels to hydronephrosis and investigation of arterial conditions in 50 kidneys. Acta. chir. Scandinav.,
61: 289-330, 1927. 6 Quinby, W. C.: Factors influencing operative procedure in hydronephrosis. J. A. M. A., 93:
1709-1710, 1929. 656
Spontaneous development of right hydronephrosis in young rats of a highly inbred strain has recently been described by Sellers and associates. 7 Hydronephrosis in these rats was due to partial obstruction of the ureter by an ovarian or internal spermatic artery lying in close apposition to the ureter. Our experiments were designed to develop a method for the production of hydronephrosis. Structural and functional changes in the affected kidney pelvis and ureter which occur when that organ is placed in intimate association with a pulsating artery were evaluated. METHODS
One ureter in each of 24 healthy adult mongrel dogs was brought into close contact with: 1) the external iliac artery, 2) the inferior mesenteric artery, or 3) the aorta and inferior mesenteric artery. All operations were performed aseptically through a midline abdominal incision with the dogs under sodium pentobarbital anesthesia. Excretory urograms with 15 to 20 ml. 50 per cent diatrizoate were made before surgery in each dog. Group 1. Ureter behind external iliac artery (4 dogs). The left ureter was placed between the left external iliac artery and the left posterior iliac vein in each dog. The left external iliac artery was doubly clamped and divided immediately proximal to the origin of its deep femoral branch. Both ureters were freed of their attachments at the junction of their middle and distal thirds. The left ureter was placed between the posterior iliac vein and the external iliac artery, and the right ureter was replaced in its normal bed (fig. 1). The continuity of the left iliac artery was reestablished. The vascular anastomosis in the external iliac artery was lateral and distal to the route of intact left ureter. Excretory urograms were obtained at postoperative intervals of 2, 4, and 6 months in 2 dogs and 2, 4, 6 and 12 months 7 Sellers, A. L., Rosenfeld, S. and Friedman, N. B.: Spontaneous hydronephrosis in the rat. Proc. Soc. Exp. Biol. Med., 104: 512-515, 1960.
EXPERIMENTAL HYDRONEPHROSIS
Frn. 1. Left ureter coursrng behind external iliac artery. in 2 dogs. The animals were killed and an autopsy was performed: 1 dog, 6 months after operation; 1 dog, 9 months after operation; and 2 dogs, 12 months after surgery. Group 2. Ureter anterior to inferior mesenteric artery (10 dogs). The right ureter in each dog was brought from its normal retroperitoneal position to a new location anterior to the inferior mesenteric artery. The abdominal aorta was doubly clamped and divided both above and below the origin of the inferior mesenteric artery. The right ureter was freed at the junction of its middle and upper thirds, and the segment of aorta with attached inferior mesenteric artery was passed from right to left posterior to~ ureter. The right ureter was now in a position anterior to and in intimate contact with inferior mesenteric artery (fig. 2). The left ureter was freed of its attachments at the junction of middle and upper thirds and was then replaced in its usual position. Postoperative excretory urograms were obtained at 2-month intervals. Group 3. Left retro-aortic ureter (10 dogs). The left ureter in each dog was brought to a new location behind the aorta (fig. 3). Both ureters were freed of their attachments at the junction
657
Frn. 2. Right ureter anterior to inferior mesenteric artery.
1
Frn. 3. Retro-aortic transposition of left ureter of their upper and middle thirds. The aorta was doubly clamped and divided both above and below the origin of inferior mesenteric artery. The segment of aorta with attached inferior
658
COCKETT AND FITZGERALD
mesenteric artery was passed behind left ureter, and aortic continuity was re-established. The left ureter now had a course posterior to the aorta, anterior to the inferior mesenteric artery at its origin on the right, and posterior to the aorta. The freed segment of right ureter was replaced in its usual position. Excretory urograms were made at 2 month intervals after operation. One dog died during surgery. One dog escaped from the outdoor compound 6 months after surgery. Six animals were sacrificed: 1 dog 5 months after operation, 1 dog 6 months after surgery, 1 dog 9 months after surgery, and 3 dogs 12 months after surgery. The remaining 2 dogs are awaiting 12 month sacrifices. The ureters were not divided in any of these experiments. RESULTS
Periodic excretory urograms after intervals as long as 12 months revealed neither functional abnormalities nor hydronephrosis in the 4 dogs of group 1, whose ureter had been placed between the iliac vessels. Similar x-ray studies performed as long as 12 months after operation in 10 dogs of group 2, whose ureters were placed anterior to inferior mesenteric artery, revealed no changes in the renal outflow system. Figure 4 shows a hydration urogram performed 12 months after operation in a dog belonging to group 2. There is no suggestion of ureterectasis or of hydronephrosis. Excretory urograms were performed periodically for 6 to 12 months postoperatively. Six dogs in group 3, whose ureters were placed in a
FIG. 4. Hydration pyelogram on group 2 animal
retroaortic position, showed moderate to moderately severe hydronephrosis (fig. 5,A-C). In a seventh animal, early hydronephrotic changes were already apparent 5 months after operation (fig. 5,D). The opposite, control ureters were normal. DISCUSSION
These findings suggest the importance of 2 factors in the genesis of hydronephrosis: continued arterial pulsation combined with partial ureteral obstruction. While a continued arterial pulse was in apposition to the middle and lowermiddle thirds of the ureter in other groups of animals, this pulsation did not appear to be significant in the formation of hydronephrosis. It is possible that the junction of middle ureter with upper ureter differs structurally from the more distal ureter. Of significance is the absence of hydronephrotic
FIG. 5. A, delayed pyelogram in group 3 animal 1 year after surgery. B, moderately severe left hydronephrosis in another group 3 animal 1 year after surgery. C, moderately severe left hydronephrosis with ureterectasis in a third animal (group 3) 1 year after surgery. D, early ureterectasis and slight pelviectasis in group 3 animal 5 months following surgery.
EXPERIMENTAL HYDRONEPHROSIS
changes in the opposite control ureters. By careful dissection, the exact extent of ureter lying opposite the surgically displaced ureter was freed from its normal bed before allowing it to be replaced in its usual position. In several recent experiments in which a left retro-aortic ureter was surgically created, intraluminal pressure tracings of both ureters revealed a significant elevation in pressure proximal to the site of partial ureteral obstruction. A pressure of 155 mm. water was noted on the left compared to a control of 30 to 43 mm. water. Pressures were obtained by cannulating each ureter in the lower third through a ureterotomy. Catheters were passed proximally into the renal pelvis and a pressure transducer system connected to a recorder was used. Care ,Yas taken to prevent total ureteral obstruction by utilizing small polyethylene catheters. Positive radiographic findings were evident by excretory urography within 5 months after operation in animals from group 3 (retro-aortic left ureter). In several animals accentuation of hydronephrosis with ureterectasis and pelviectasis was obtained by hydrating the animals before urography. Dilatation of the upper ureters and pelvis extended from the site of obstruction in proximal fashion. In a subsequent paper detailed histologic changes in group 3 animals extending from the site of partial ureteral obstruction and diminish-
659
ing proximally will be reported. Structural changes within the intima and media of the ureters will be emphasized and will be compared to control ureters on the opposite side. SUMMARY AND CONCLUSIONS
A method for the experimental production of hydronephrosis is presented. Ureterectasis and pelviectasis were created in seven of 9 dogs by displacing an intact ureter to a position behind the aorta. The role of continued arterial pulsation with and without partial ureteral obstruction is discussed in the genesis of hydronephrosis. Radiographic changes indicated moderately severe hydronephrosis in dogs (group 3). These changes extended from the site of obstruction proximally. Intraluminal uretcral pressures are discussed. No abnormalities of the ureter or of the renal pelvis were observed in dogs (groups 1 and 2) after displacement of intact ureter to intimate contact with external iliac or inferior mesenteric arteries. The authors gratefully acknmdedge the support and encouragen1ent of Dr. \Villard E. Goodwin, Department of Surgery, l'niversity of California Medical Center, Los )1.ngeles; and Major E. V. Dahl, formerly chief of the Department of Pathology, School of Aerospace l\fedicine, Brooks )cFB, Texas.
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