THE
Vol. 118, October Printed in UXA..
JOURNAL OF UROLOGY
Copyright © 1977 by The Williams & Wilkins Co.
REV ASCULARIZATION OF THE CHRONIC TOTALLY OCCLUDED RENAL ARTERY WITH RESTORATION OF RENAL FUNCTION LEONARD ZINMAN*
AND
JOHN A. LIBERTINO
From the Department of Urology, Lahey Clinic Foundation, Boston, Massachusetts
ABSTRACT
Nine patients with non-functioning kidneys and complete renal artery occlusion discovered on arteriographic investigation for hypertension underwent renal artery revascularization with successful restoration of renal. blood flow. Of these patients 7 experienced recovery of renal function and 2 showed no evidence of improvement. One patient had a creatinine clearance of 38 cc per minute from the revascularized kidney 2 years postoperatively. Predictive determinants of salvageable renal parenchyma were the histologic evidence of intact viable glomernli and the angiographic features of a rich perihilar collateral circulation in the presence of a proximal occlusion with a patent distal renal artery. The duration and degree of renal ischemia compatible with survival of a significant amount of renal parenchyma in patients with complete main renal artery occlusion are not known. Patients with ischemic non-functioning kidneys secondary to renal artery disease traditionally have undergone nephredomy to control hypertension, with the understanding that there is irreparable damage from prolonged ischemia. 1. 2 However, reports of renal artery embolectomy 9 to 56 days after acute total arterial occlusion with satisfactory return of renal function~]() suggest that persistent ischemia with absent excretory renal function can occur without cell death and that pre-existing collateral circulation may offer a variable degree of protection and maintain viable renal tissue at subfiltration arterial pressure perfusion. 11 Since surgical revascularization of renal artery occlusion in high risk patients with altered renal function and associated severe hypertension is a more formidable procedure than nephrectomy, criteria to predict reversible ischemia are essential but largely lacking. In our preliminary report on patients with total renal artery occlusion renal morphology was emphasized as the main method of judging the presence of reversible ischemic parenchyma. 1" Since 1968, 15 patients with total chronic renal artery occlusion, absence of function on excretory urography (IVP) and poorly controlled diastolic hypertension have been seen at our clinic. Of these patients 9 have undergone reconstructive arterial operations with successful restoration of blood flow confirmed by renal angiography 6 months to 3 years postoperatively and have had followup studies for 2 to 7 years with varying degrees of recovery of function" Herein we review these 9 cases and call attention to the reversibility of renal failure secondary to total main renal artery occlusion. MATERIALS AND METHODS
From 1968 to 1973, 9 patients with severe refractory diastolic hypertension were found to have a silent unilateral non-visualized kidney on IVP and total main renal artery occlusion on transfemoral renal angiography. The 4 women and 5 men in age from 21 to 64 years (table 1). Six patients had atherosclerotic thrombotic occlusion of the left main stem and 2 had atherosclerotic occlusion of the right main stem. Traumatic thrombosis of the right renal artery had occurred 6 Accepted for publication December 3, 1976. Read at annual meeting of American Urological Association, Miami Beach, Florida, May 11-15, 1975. * Requests for reprints: Department of Urology, Lahey Clinic Foundation, 605 Commonwealth Ave., Boston, Massachusetts 02215. 517
months before the study in 1 patient, who was fouJ.lid to have complete distal main renal artery occlusion. The duration of the occlusion in 8 patients was not known since there were no lateralizing signs to indicate the date of onset. Two µa,,,,cJu.c0 had IVPs showing a non-visualized collecting system identified during a 6 to 12-month period. Six patients had serum creatinine values ranging from 0.8 to 5.6 mg. per 100 ml. Two of these 6 patients had greater than 80 per cent stenosis of contralateral side and underwent bilateral revascularization procedures. Renal silhouette measurements varied from 8.5 to 11.5 cm. long. Four patients underwent divided renal function studies and urinary excretion was absent from the non-visual,. ized kidney. Significant lateralizing renal vein renin ratios obtained in 6 patients ranged from 1.7 to 6.0. Early and delayed arteriograms were studied carefully for details of collateral circulation. Seven patients underwent an autogenous saphenous vein aortorenal bypass graft, 1 underwent endarterectomy and patient had a left splenorenal bypass graft (table 2). patients had intraoperative renal biopsies, 2 of whom also contralateral renal biopsies. Renal arteriotomy confirmed the presence of complete proximal occlusion with good distal backflow in the entire group. Seven patients had proximal orifice occlusion with a patent soft distal vesseL One patient had occlusion of the main renal artery up to the bifurcation and the 1 patient with a history of traumatic thrombosis had a distal fibrotic occlusion just proximal to the first bifurcation. Successful restoration of renal blood flow with patent was achieved in the entire group and confirmed by renal angiography 6 months to 2 years after the arterial RESULTS
Seven patients have had return of renal function as evidenced by prompt appearance of contrast material, with a well visualized collecting system within 3 months postoperatively. One patient had no return of function and 1 had faint appearance of contrast material with no change in values for serum creatinine (cases 5 and 6). Four patients had a decrease in the levels of serum creatinine and a 1 to 3 cm. increase in the size of the renal silhouette in the first 6 months after restoration of blood flow (cases 1, 4, 7 and 9). One patient had a 38 cc per minute measured creatinine clearance from the revascularized kidney on divided function study 2 years postoperatively and a 2 cm. increase in renal size (case 1). Intraoperative renal biopsies in 5 patients revealed that in 80 per cent of the glomeruli architecture was preserved intact with minimal basement membrane thickening. These 5 pa-
518
ZINMAN AND LIBERTINO TABLE
Case-Age- Sex No. (yrs.)
1. Clinical data in 9 revascularized patients with complete renal artery occlusion Blood Pressure (mm.Hg)
Site and Type of Pathology
Serum Creatinine (mg./100 ml.)
Preop.
Postop.
Preop.
Postop.
1-56-M
Lt. main stem, atherosclerotic occlusion
210/130
140/90
1.9
1.3
2-62-F 3-51-F 4-64-M
Lt. main stem, atherosclerotic occlusion Rt. main stem, atherosclerotic occlusion Rt. main stem, atherosclerotic occlusion
220/140 200/120 230/116
120/80 132/70 150/90
1.4 0.8 4.2
1.4 1.0 2.2
5-21-F 6-59-M 7-54-M 8-55-F 9-60-M
Rt. main stem, trauma Lt. main stem, atherosclerotic occlusion Lt. main stem, atherosclerotic occlusion Lt. main stem, atherosclerotic occlusion Lt. main stem, atherosclerotic occlusion
205/130 170/110 240/120 204/124 196/90
105/70 180/110 150/100 110/64 130/86
0.9 1.8 5.6
0.9 1.8 3.2
TABLE
Case
1.1
1.1
2.0
1.0
Postop. IVP After 6 Mos. Function recovered, 1.5 cm. increase in renal size Function recovered Function recovered Function recovered, 2 cm. increase in renal size No recovery No recovery Function recovered Function recovered Function recovered
2. Correlation of functional recovery with renal biopsy and visualized collateral
Operation
Functional Response*
Extent of Main Artery Involved
Scarred Glomeruli
1
Endarterectomy and patch graft
+++
Proximal
0
2 3 4
Saphenous vein bypass graft Saphenous vein bypass graft Saphenous vein bypass graft
+++ +++ +++
Proximal Proximal Proximal
+ + +
5 6 7 8 9
Saphenous vein bypass graft Bilat. saphenous vein bypass graft Bilat. saphenous vein bypass graft Splenorenal bypass graft Saphenous vein bypass graft
0
+ +++ +++ +++
Distal Total Proximal Proximal Proximal
+++ +++ ++ +
Tubular Atrophy
++ +++ (diffuse) ++ (diffuse) ++ (focal) ++ ++ ++ +++
(diffuse) (diffuse) (diffuse) (diffuse)
Collateral Peripelvic delayed filling of distal artery Hilar and periureteral Poorly visualized Peripelvic delayed filling of distal branches Capsular and adrenal pre-stenotic Not visualized Not visualized Hilar Peripelvic
* Followup period 3 to 8 years. Functional recovery determined by appearance and concentration of contrast material on IVP. Case 1 had a 38 cc per minute serum creatinine clearance from revascularized kidney 2 years postoperatively.
tients had excellent return ofrenal function on IVP with good concentration of contrast material. Two patients with poor functional recovery had extensive fibrous replacement of the glomeruli. One patient had approximately 70 per cent of the glomeruli preserved with good functional return and a decrease in levels of serum creatinine from 5.6 to 3.2 mg. per 100 ml. All biopsy material showed a significant degree of tubular atrophy with an increase in interstitial material, which did not correlate well with the degree offunctional recovery. The variable amount of arteriolosclerosis encountered did not seem to preclude functional return. Of the 7 patients with good functional recovery 4 had a perihilar and peripelvic collateral circulation visualized on the delayed portion of the angiogram. In 2 of these patients (cases 1 and 4) filling of the distal main renal artery was visualized on the late films, which was the result of retrograde filling from the peripelvic communicating collateral circuit into the distal main renal artery and its branches. In this group of patients proximal obstruction with a patent distal main vessel left adequate opportunity for retrograde flow by hilar connecting collateral pathways into the post-occlusive arterial system with successful reversal of renal function. This collateral circuit was demonstrated on delayed angiography as a tortuous collection in the perihilar region coming from the peripelvic and upper ureteral vasculature. One patient (case 5) had an extensive adrenal and capsular collateral circuit anastomosing with the right renal artery proximal to the occlusive lesion, which prevented the collateral blood flow from draining into the distal parenchymal vessels. No functional recovery followed revascularization but the hypertension was cured. There was a significant elaboration of renin from the renal vein in the presence of irreversibly damaged renal parenchyma. The presence of elevated renal vein renin was not predictive of viable renal parenchyma or of significant collateral flow. This patient had experienced an acute arterial occlusion, which may not have allowed sufficient time for the proper collateral pathways to develop. The patients with successful reversal of renal function probably had gradual atherosclerotic main renal arterial narrowing that preceded the final total occlusion. Gradual long-standing renal artery narrowing
stimulated the development of increased blood flow in the renal collateral system and allowed a more effective parenchymal support circulation. The features of age, renal size, tubular atrophy and small vessel disease did not correlate well with the amount of functional restoration. CASE REPORTS
Case 1. A 56-year-old man had a 6-year history of hypertension and mild right intermittent claudication. The patient was admitted to the hospital with severe occipital headaches and poorly controlled hypertension. Blood pressure taken on hospitalization was 210/130 mm. Hg while the patient was taking 2 antihypertensive drugs. He was experiencing troublesome side effects with postural hypertension, anorexia and vomiting. Pedal pulses were absent and the right femoral pulse was weak. He had an enlarged heart and grade 2 hypertensive retinopathy. An aortic bruit was heard in the right lower quadrant. Serum creatinine measured 1.9 mg. per 100 ml. and a urine sediment was normal. An IVP 3 months before the patient was hospitalized revealed a non-visualized left kidney (9.5 cm.) and a normal right kidney (12 cm.). Findings on repeat IVP in July 1968 were unchanged with no evidence of a left collecting system (fig. 1, A). Retrograde pyelography revealed a small but normal left collecting system and ureter. There was no urine output from the left kidney. Transfemoral aortography revealed severe atheromatous involvement of the aorta and iliac arteries with total occlusion of the right common iliac artery, complete occlusion of the left proximal renal artery and 2 patent right renal arteries. A collection of tortuous collateral vessels was noted in the hilar region of the left kidney (fig. 1, B). Revascularization of the left kidney by renal endarterectomy, and vein patch graft and renal biopsy were done on July 14. The biopsy specimen revealed normal glomeruli with collapsed atrophic tubules and a considerable increase in interstitial material. The small vessels revealed mild arteriolosclerosis. The origin of the renal artery was completely occluded with a soft normal distal wall and a significant amount of back bleeding. Blood pressure in the early postoperative period was 150/90 mm. Hg, and serum creatinine measured 1.3 mg. per 100 ml. and remains at that level. IVP 2
REVASCULARIZATION OF RENAL ARTERY
years postoperatively revealed prompt excretion of the contrast material in 5 minutes with good concentration and a 2 cm. increase in renal length (fig. 2, A). The patient was reassessed at that time with repeat left renal angiography that demonstrated a patent left renal artery and distal vasculature (fig. 2, B). A divided ureteral catheterization study revealed a serum creatinine clearance of 38 cc per minute from the previnon-functioning left kidney. 4. A 64-year-old man had had mild hypertension for 10 years. He was admitted to the hospital in December 1972 with a 3-month history of acceleration of hypertension and severe
519
frontal headaches unresponsive to 4 antihypertensive drugs. The patient had had an uncomplicated myocardial infarction in November 1969. No evidence of peripheral vascular or cere., brovascular disease was found. Blood pressure on hospitalization was 230/116 mm. Hg and a grade 3 retinopathy with a few retinal hemorrhages was noted. Urinalysis revealed signifi .. cant proteinuria. The serum creatinine level was 4.2 mg. 100 ml. and blood urea nitrogen was 40 mg. per 100 ml. revealed a non-functioning right kidney (11.5 cm.) and a left kidney (13 cm.), with decreased concentration of the contrast material up to 20 minutes (fig. 3, A). Renal angiography
Fm. 1. Case 1. A, preoperative IVP reveals non-functioning 9.5 cm. left kidney. B, preoperative transfemoral aortogram demonstrates occluded left renal artery with filling of hilar collaterals.
Fm. 2. Case 1. A, IVP 2 years after left renal endarterectomy shows good visualization ofleft collecting system. B, postoperative selective left renal angiogram reveals patent distal vasculature with resolved left renal parenchymal blood flow.
520
ZINMAN AND LIBERTINO
revealed a normal patent left renal artery but an aortic plaque totally occluded the proximal right renal artery. Delayed angiography revealed a network of vessels in the right hilar region consistent with peripelvic renal collateral circulation filling the post-stenotic main renal artery in a retrograde manner (fig. 3, B). At operation on December 1, 1972 a biopsy of the right kidney revealed crowding of normal glomeruli with an occasional hyalinized tuft, minimal mesangial thickening, focal tubular atrophy with increased interstitial material and a moderate degree of arteriolar sclerosis. An end-toside aortorenal saphenous vein bypass graft to a patent distal
right renal artery beyond the occlusion effectively restored right renal blood flow. When the renal artery was opened a good backflow of blood from the distal branches was observed. Hypertension dramatically improved in the first 3 months and retinopathy was· completely reversed. The patient presently is taking chlorthalidone 4 years postoperatively, with a blood pressure of 150/90 mm. Hg. IVP 3 months after revascularization revealed a functioning, well visualized right collecting system and a serum creatinine level of2.2 mg. per 100 ml. (fig. 4, A). Repeat renal angiography demonstrated a patent vein graft (fig. 4, B). The right renal silhouette increased 1.5 cm. in
Fm. 3. Case 4. A, preoperative IVP reveals absent right excretory function with kidney 11.5 cm. long. B, aortogram shows complete occlusion of orifice of right renal artery with prominent network of hilar collaterals and retrograde filling of distal main artery.
Fm. 4. Case 4. A, IVP shows prompt appearance of contrast material 3 months after right renal revascularization. B, right renal angiogram 6 months after right saphenous vein aortorenal bypass graft.
521.
REV ASCULARIZATION OF RENAL ARTERY
length and the patient remains well with stable renal function. COMMENT
It is well established that renal artery stenosis may produce a reversible pressor response with little or no change in excretory function. However, it is not widely appreciated that small but critical amounts of blood flow also may maintain the viability of the filtering portion of the nephron without demonstrable urinary output. In the event of total main renal artery occlusion the extrarenal collateral circulation is decisive in determining the severity of the renal injury that will develop. The quality of these collateral pathways is dependent on the speed and location of this arterial occlusion and has been demonstrated by some investigators to widen and obtain the size of the gonadal or renal artery branches. 13 This collateral circulation is subject to great variations but the most noteworthy channels available to the severely ischemic kidney are the periureteral, peripelvic and adrenal vessels that may originate in the distal or proximal portion of the main renal artery and its branches, and form an effective circuit with the lumbar arteries coming from uninvolved portions of the aorta. 14 These channels may drain into the post-occlusive portion of the renal artery in retrograde manner and be seen on delayed renal angiography as a rich network of tortuous vessels in the renal hilus. 15 This blood flow may produce sufficient contrast material on the delayed angiograms to produce a renal nephrogram or the delayed appearance of a visualized distal main renal artery. These angiographic features were major predictive determinants in helping to decide which totally obstructed kidneys should be considered for revascularizationo The presence of a patent distal main artery was encountered in all patients with successful restoration of renal function and was an important prerequisite for the developed collateral blood flow to gain access to the renal parenchyma. Preoperative biopsy evidence of preserved glomerular morphology was the most significant predictive criterion in determining whether vascular repair would reverse renal function. Histologically, viable glomeruli in a well selected, representative specimen of renal tissue were consistently present in the group that had satisfactory restoration of renal function. 6 • 8 • 9 · 16 Widespread tubular atrophy with interstitial fibrosis and arteriolar thickening did not have any prognostic significance and merely reflected the histologic changes of chronic reversible renal ischemia. This latter histologic finding, exemplified in our series, may be a signal to the presence of pre-existing chronic renal artery stenosis, which permitted a well developed post-occlusive collateral circulation to be present when complete arterial obstruction developed. If complete renal artery occlusion occurs slowly collateral circulation has been reported to be sufficient to maintain normal renal size and normal renal function. 130 17 However, the absence of visualized collateral channels did not exclude their presence in 2 patients with normal preoperative glomerular histology who were successfully revascularized with good functional return. Patients with sudden acceleration of the pre-existing mild hypertension and a non-functioning silent kidney with complete renal artery occlusion are likely to have recovery of renal
function if angiography demonstrates a rich network of hilar collateral vessels with delayed filling of the main renal artery or a parenchymal nephrogram, surgical exploration establishes the presence of a patent distal vessel with proximal occlusion and the renal biopsy reveals intact glomerular morphology with focal widespread tubular atrophy. This last finding reflects the effect of chronic renal artery stenosis and ischemia and may be substantial evidence for the likelihood of a prior well developed extrarenal collateral circulation, which can maintain potentially viable renal parenchyma in the event of main renal artery occlusion. REFERENCES
1. Schoenbaurn, S., Goldman, M. A. and Siegelman, S. S.: R,ena!
artery embolization. Angiology, 22: 332, 1971. 2. Possati, L., Pierangeli, A., Del Gaudio, A. and Gozzeti, G.: Traitement chirurgical de l'hypertension arterielle par obstruction complete de l'artere renale. Lyon Chir., 66: 13, 1970. 3. Brest, A. N., Bower, R. and Heider, C.: Renal functional recovery following anuria secondary to renal artery embolism. J.A.M.A., 187: 540, 1964. 4. Perkins, R. P., Jacobsen, D.S., Feder, F. P., Lipchik, E. 0. and Fine, P. H.: Return of renal function after late embolectomy. Report of a case. New Engl. J. Med., 276: 1194, 1967. 5. Thomas, T. V., Faulconer, H. T. and Lansing, A. M.: Management of embolic occlusion of renal arteries. Surgery, 65: 576, 1969.
6. Mundth, E. D., Shine, K. and Austen, W. G.: Correction of malignant hypertension and return ofrenal function following late renal artery embolectomy. Amer. J. Med., 46: 985, 1969. 7. Sullivan, M. J., Cronin, R., Lackner, L. H. and Edwards, W. S.: Embolization of a solitary kidney. Successful embolectomy after nine days. J.A.M.A., 222: 82, 1972. 8. Sheil, A.G. R., Stokes, G. S., Tiller, D. J., May, J., Johnson, J. R. and Stewart, J. H.: Reversal of renal failure by revascu-· larisation of kidneys with thrombosed renal arteries. Lancet, 2: 865, 1973. 9. Morgan, T., Wilson, M., Johnston, W., Clunie, G. J. and Gordon, R.: Restoration of renal function by arterial surgery. Lancet, l: 653, 1974. 10. Quantock, 0. P. and Thatcher, G. N.: Reversible renal failure with renal artery occlusion. Brit. Med. J., 2: 27, 1972. 11. Morris, G. C., Jr., Heider, C. F. and Moyer, J. H.: The protective effect of subfiltration arterial pressure of the kidney. Su:rg. Forum, 6: 623, 1956. 12. Zinman, L. and Libertino, J. A.: Revascularization of the totally occluded renal artery (abstract). Circulation, vol. 48, suppl. 4, p. 31, 1973. 13. Brohn, L and Stener, I.: Collaterals in obstruction of the rens.l artery. Acta Radiol. (diagn.), 4: 449, 1966. 14. Abrams, H. L. and Cornell, S. H.: Patterns of collateral flow in renal ischemia. Radiology, 84: 1001, 19650 15. Boijsen, E.: Angiographic studies of the anatomy of single and multiple renal arteries. Acta Radiol., suppl. 183, 1959. 16. Besarab, A., Brown, R. S., Rubin, N. T., Salzman, E., Wirthlin, L., Steinman, T., Atha, R.R. and Skillman, J. J.: Reversible renal failure following bilateral renal artery occlusive diseaseo Clinical features, pathology, and the role of surgical revascularization. J.A.M.A., 235: 2838, 1976. 17. Dobrzinsky, S. J., Voegeli, E., Grant, H. A., Christlieb, Ao R.., Abrams, H. L. and Hickler, R. B.: Spontaneous reestablishment of renal function after complete occlusion of a renal artery. Arch. Intern. Med., 128: 266, 1971.
Vol. 118, October Printed in UXA..
JOURNAL OF UROLOGY
Copyright © 1977 by The Williams & Wilkins Co.
REV ASCULARIZATION OF THE CHRONIC TOTALLY OCCLUDED RENAL ARTERY WITH RESTORATION OF RENAL FUNCTION LEONARD ZINMAN*
AND
JOHN A. LIBERTINO
From the Department of Urology, Lahey Clinic Foundation, Boston, Massachusetts
ABSTRACT
Nine patients with non-functioning kidneys and complete renal artery occlusion discovered on arteriographic investigation for hypertension underwent renal artery revascularization with successful restoration of renal. blood flow. Of these patients 7 experienced recovery of renal function and 2 showed no evidence of improvement. One patient had a creatinine clearance of 38 cc per minute from the revascularized kidney 2 years postoperatively. Predictive determinants of salvageable renal parenchyma were the histologic evidence of intact viable glomernli and the angiographic features of a rich perihilar collateral circulation in the presence of a proximal occlusion with a patent distal renal artery. The duration and degree of renal ischemia compatible with survival of a significant amount of renal parenchyma in patients with complete main renal artery occlusion are not known. Patients with ischemic non-functioning kidneys secondary to renal artery disease traditionally have undergone nephredomy to control hypertension, with the understanding that there is irreparable damage from prolonged ischemia. 1. 2 However, reports of renal artery embolectomy 9 to 56 days after acute total arterial occlusion with satisfactory return of renal function~]() suggest that persistent ischemia with absent excretory renal function can occur without cell death and that pre-existing collateral circulation may offer a variable degree of protection and maintain viable renal tissue at subfiltration arterial pressure perfusion. 11 Since surgical revascularization of renal artery occlusion in high risk patients with altered renal function and associated severe hypertension is a more formidable procedure than nephrectomy, criteria to predict reversible ischemia are essential but largely lacking. In our preliminary report on patients with total renal artery occlusion renal morphology was emphasized as the main method of judging the presence of reversible ischemic parenchyma. 1" Since 1968, 15 patients with total chronic renal artery occlusion, absence of function on excretory urography (IVP) and poorly controlled diastolic hypertension have been seen at our clinic. Of these patients 9 have undergone reconstructive arterial operations with successful restoration of blood flow confirmed by renal angiography 6 months to 3 years postoperatively and have had followup studies for 2 to 7 years with varying degrees of recovery of function" Herein we review these 9 cases and call attention to the reversibility of renal failure secondary to total main renal artery occlusion. MATERIALS AND METHODS
From 1968 to 1973, 9 patients with severe refractory diastolic hypertension were found to have a silent unilateral non-visualized kidney on IVP and total main renal artery occlusion on transfemoral renal angiography. The 4 women and 5 men in age from 21 to 64 years (table 1). Six patients had atherosclerotic thrombotic occlusion of the left main stem and 2 had atherosclerotic occlusion of the right main stem. Traumatic thrombosis of the right renal artery had occurred 6 Accepted for publication December 3, 1976. Read at annual meeting of American Urological Association, Miami Beach, Florida, May 11-15, 1975. * Requests for reprints: Department of Urology, Lahey Clinic Foundation, 605 Commonwealth Ave., Boston, Massachusetts 02215. 517
months before the study in 1 patient, who was fouJ.lid to have complete distal main renal artery occlusion. The duration of the occlusion in 8 patients was not known since there were no lateralizing signs to indicate the date of onset. Two µa,,,,cJu.c0 had IVPs showing a non-visualized collecting system identified during a 6 to 12-month period. Six patients had serum creatinine values ranging from 0.8 to 5.6 mg. per 100 ml. Two of these 6 patients had greater than 80 per cent stenosis of contralateral side and underwent bilateral revascularization procedures. Renal silhouette measurements varied from 8.5 to 11.5 cm. long. Four patients underwent divided renal function studies and urinary excretion was absent from the non-visual,. ized kidney. Significant lateralizing renal vein renin ratios obtained in 6 patients ranged from 1.7 to 6.0. Early and delayed arteriograms were studied carefully for details of collateral circulation. Seven patients underwent an autogenous saphenous vein aortorenal bypass graft, 1 underwent endarterectomy and patient had a left splenorenal bypass graft (table 2). patients had intraoperative renal biopsies, 2 of whom also contralateral renal biopsies. Renal arteriotomy confirmed the presence of complete proximal occlusion with good distal backflow in the entire group. Seven patients had proximal orifice occlusion with a patent soft distal vesseL One patient had occlusion of the main renal artery up to the bifurcation and the 1 patient with a history of traumatic thrombosis had a distal fibrotic occlusion just proximal to the first bifurcation. Successful restoration of renal blood flow with patent was achieved in the entire group and confirmed by renal angiography 6 months to 2 years after the arterial RESULTS
Seven patients have had return of renal function as evidenced by prompt appearance of contrast material, with a well visualized collecting system within 3 months postoperatively. One patient had no return of function and 1 had faint appearance of contrast material with no change in values for serum creatinine (cases 5 and 6). Four patients had a decrease in the levels of serum creatinine and a 1 to 3 cm. increase in the size of the renal silhouette in the first 6 months after restoration of blood flow (cases 1, 4, 7 and 9). One patient had a 38 cc per minute measured creatinine clearance from the revascularized kidney on divided function study 2 years postoperatively and a 2 cm. increase in renal size (case 1). Intraoperative renal biopsies in 5 patients revealed that in 80 per cent of the glomeruli architecture was preserved intact with minimal basement membrane thickening. These 5 pa-
518
ZINMAN AND LIBERTINO TABLE
Case-Age- Sex No. (yrs.)
1. Clinical data in 9 revascularized patients with complete renal artery occlusion Blood Pressure (mm.Hg)
Site and Type of Pathology
Serum Creatinine (mg./100 ml.)
Preop.
Postop.
Preop.
Postop.
1-56-M
Lt. main stem, atherosclerotic occlusion
210/130
140/90
1.9
1.3
2-62-F 3-51-F 4-64-M
Lt. main stem, atherosclerotic occlusion Rt. main stem, atherosclerotic occlusion Rt. main stem, atherosclerotic occlusion
220/140 200/120 230/116
120/80 132/70 150/90
1.4 0.8 4.2
1.4 1.0 2.2
5-21-F 6-59-M 7-54-M 8-55-F 9-60-M
Rt. main stem, trauma Lt. main stem, atherosclerotic occlusion Lt. main stem, atherosclerotic occlusion Lt. main stem, atherosclerotic occlusion Lt. main stem, atherosclerotic occlusion
205/130 170/110 240/120 204/124 196/90
105/70 180/110 150/100 110/64 130/86
0.9 1.8 5.6
0.9 1.8 3.2
TABLE
Case
1.1
1.1
2.0
1.0
Postop. IVP After 6 Mos. Function recovered, 1.5 cm. increase in renal size Function recovered Function recovered Function recovered, 2 cm. increase in renal size No recovery No recovery Function recovered Function recovered Function recovered
2. Correlation of functional recovery with renal biopsy and visualized collateral
Operation
Functional Response*
Extent of Main Artery Involved
Scarred Glomeruli
1
Endarterectomy and patch graft
+++
Proximal
0
2 3 4
Saphenous vein bypass graft Saphenous vein bypass graft Saphenous vein bypass graft
+++ +++ +++
Proximal Proximal Proximal
+ + +
5 6 7 8 9
Saphenous vein bypass graft Bilat. saphenous vein bypass graft Bilat. saphenous vein bypass graft Splenorenal bypass graft Saphenous vein bypass graft
0
+ +++ +++ +++
Distal Total Proximal Proximal Proximal
+++ +++ ++ +
Tubular Atrophy
++ +++ (diffuse) ++ (diffuse) ++ (focal) ++ ++ ++ +++
(diffuse) (diffuse) (diffuse) (diffuse)
Collateral Peripelvic delayed filling of distal artery Hilar and periureteral Poorly visualized Peripelvic delayed filling of distal branches Capsular and adrenal pre-stenotic Not visualized Not visualized Hilar Peripelvic
* Followup period 3 to 8 years. Functional recovery determined by appearance and concentration of contrast material on IVP. Case 1 had a 38 cc per minute serum creatinine clearance from revascularized kidney 2 years postoperatively.
tients had excellent return ofrenal function on IVP with good concentration of contrast material. Two patients with poor functional recovery had extensive fibrous replacement of the glomeruli. One patient had approximately 70 per cent of the glomeruli preserved with good functional return and a decrease in levels of serum creatinine from 5.6 to 3.2 mg. per 100 ml. All biopsy material showed a significant degree of tubular atrophy with an increase in interstitial material, which did not correlate well with the degree offunctional recovery. The variable amount of arteriolosclerosis encountered did not seem to preclude functional return. Of the 7 patients with good functional recovery 4 had a perihilar and peripelvic collateral circulation visualized on the delayed portion of the angiogram. In 2 of these patients (cases 1 and 4) filling of the distal main renal artery was visualized on the late films, which was the result of retrograde filling from the peripelvic communicating collateral circuit into the distal main renal artery and its branches. In this group of patients proximal obstruction with a patent distal main vessel left adequate opportunity for retrograde flow by hilar connecting collateral pathways into the post-occlusive arterial system with successful reversal of renal function. This collateral circuit was demonstrated on delayed angiography as a tortuous collection in the perihilar region coming from the peripelvic and upper ureteral vasculature. One patient (case 5) had an extensive adrenal and capsular collateral circuit anastomosing with the right renal artery proximal to the occlusive lesion, which prevented the collateral blood flow from draining into the distal parenchymal vessels. No functional recovery followed revascularization but the hypertension was cured. There was a significant elaboration of renin from the renal vein in the presence of irreversibly damaged renal parenchyma. The presence of elevated renal vein renin was not predictive of viable renal parenchyma or of significant collateral flow. This patient had experienced an acute arterial occlusion, which may not have allowed sufficient time for the proper collateral pathways to develop. The patients with successful reversal of renal function probably had gradual atherosclerotic main renal arterial narrowing that preceded the final total occlusion. Gradual long-standing renal artery narrowing
stimulated the development of increased blood flow in the renal collateral system and allowed a more effective parenchymal support circulation. The features of age, renal size, tubular atrophy and small vessel disease did not correlate well with the amount of functional restoration. CASE REPORTS
Case 1. A 56-year-old man had a 6-year history of hypertension and mild right intermittent claudication. The patient was admitted to the hospital with severe occipital headaches and poorly controlled hypertension. Blood pressure taken on hospitalization was 210/130 mm. Hg while the patient was taking 2 antihypertensive drugs. He was experiencing troublesome side effects with postural hypertension, anorexia and vomiting. Pedal pulses were absent and the right femoral pulse was weak. He had an enlarged heart and grade 2 hypertensive retinopathy. An aortic bruit was heard in the right lower quadrant. Serum creatinine measured 1.9 mg. per 100 ml. and a urine sediment was normal. An IVP 3 months before the patient was hospitalized revealed a non-visualized left kidney (9.5 cm.) and a normal right kidney (12 cm.). Findings on repeat IVP in July 1968 were unchanged with no evidence of a left collecting system (fig. 1, A). Retrograde pyelography revealed a small but normal left collecting system and ureter. There was no urine output from the left kidney. Transfemoral aortography revealed severe atheromatous involvement of the aorta and iliac arteries with total occlusion of the right common iliac artery, complete occlusion of the left proximal renal artery and 2 patent right renal arteries. A collection of tortuous collateral vessels was noted in the hilar region of the left kidney (fig. 1, B). Revascularization of the left kidney by renal endarterectomy, and vein patch graft and renal biopsy were done on July 14. The biopsy specimen revealed normal glomeruli with collapsed atrophic tubules and a considerable increase in interstitial material. The small vessels revealed mild arteriolosclerosis. The origin of the renal artery was completely occluded with a soft normal distal wall and a significant amount of back bleeding. Blood pressure in the early postoperative period was 150/90 mm. Hg, and serum creatinine measured 1.3 mg. per 100 ml. and remains at that level. IVP 2
REVASCULARIZATION OF RENAL ARTERY
years postoperatively revealed prompt excretion of the contrast material in 5 minutes with good concentration and a 2 cm. increase in renal length (fig. 2, A). The patient was reassessed at that time with repeat left renal angiography that demonstrated a patent left renal artery and distal vasculature (fig. 2, B). A divided ureteral catheterization study revealed a serum creatinine clearance of 38 cc per minute from the previnon-functioning left kidney. 4. A 64-year-old man had had mild hypertension for 10 years. He was admitted to the hospital in December 1972 with a 3-month history of acceleration of hypertension and severe
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frontal headaches unresponsive to 4 antihypertensive drugs. The patient had had an uncomplicated myocardial infarction in November 1969. No evidence of peripheral vascular or cere., brovascular disease was found. Blood pressure on hospitalization was 230/116 mm. Hg and a grade 3 retinopathy with a few retinal hemorrhages was noted. Urinalysis revealed signifi .. cant proteinuria. The serum creatinine level was 4.2 mg. 100 ml. and blood urea nitrogen was 40 mg. per 100 ml. revealed a non-functioning right kidney (11.5 cm.) and a left kidney (13 cm.), with decreased concentration of the contrast material up to 20 minutes (fig. 3, A). Renal angiography
Fm. 1. Case 1. A, preoperative IVP reveals non-functioning 9.5 cm. left kidney. B, preoperative transfemoral aortogram demonstrates occluded left renal artery with filling of hilar collaterals.
Fm. 2. Case 1. A, IVP 2 years after left renal endarterectomy shows good visualization ofleft collecting system. B, postoperative selective left renal angiogram reveals patent distal vasculature with resolved left renal parenchymal blood flow.
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revealed a normal patent left renal artery but an aortic plaque totally occluded the proximal right renal artery. Delayed angiography revealed a network of vessels in the right hilar region consistent with peripelvic renal collateral circulation filling the post-stenotic main renal artery in a retrograde manner (fig. 3, B). At operation on December 1, 1972 a biopsy of the right kidney revealed crowding of normal glomeruli with an occasional hyalinized tuft, minimal mesangial thickening, focal tubular atrophy with increased interstitial material and a moderate degree of arteriolar sclerosis. An end-toside aortorenal saphenous vein bypass graft to a patent distal
right renal artery beyond the occlusion effectively restored right renal blood flow. When the renal artery was opened a good backflow of blood from the distal branches was observed. Hypertension dramatically improved in the first 3 months and retinopathy was· completely reversed. The patient presently is taking chlorthalidone 4 years postoperatively, with a blood pressure of 150/90 mm. Hg. IVP 3 months after revascularization revealed a functioning, well visualized right collecting system and a serum creatinine level of2.2 mg. per 100 ml. (fig. 4, A). Repeat renal angiography demonstrated a patent vein graft (fig. 4, B). The right renal silhouette increased 1.5 cm. in
Fm. 3. Case 4. A, preoperative IVP reveals absent right excretory function with kidney 11.5 cm. long. B, aortogram shows complete occlusion of orifice of right renal artery with prominent network of hilar collaterals and retrograde filling of distal main artery.
Fm. 4. Case 4. A, IVP shows prompt appearance of contrast material 3 months after right renal revascularization. B, right renal angiogram 6 months after right saphenous vein aortorenal bypass graft.
521.
REV ASCULARIZATION OF RENAL ARTERY
length and the patient remains well with stable renal function. COMMENT
It is well established that renal artery stenosis may produce a reversible pressor response with little or no change in excretory function. However, it is not widely appreciated that small but critical amounts of blood flow also may maintain the viability of the filtering portion of the nephron without demonstrable urinary output. In the event of total main renal artery occlusion the extrarenal collateral circulation is decisive in determining the severity of the renal injury that will develop. The quality of these collateral pathways is dependent on the speed and location of this arterial occlusion and has been demonstrated by some investigators to widen and obtain the size of the gonadal or renal artery branches. 13 This collateral circulation is subject to great variations but the most noteworthy channels available to the severely ischemic kidney are the periureteral, peripelvic and adrenal vessels that may originate in the distal or proximal portion of the main renal artery and its branches, and form an effective circuit with the lumbar arteries coming from uninvolved portions of the aorta. 14 These channels may drain into the post-occlusive portion of the renal artery in retrograde manner and be seen on delayed renal angiography as a rich network of tortuous vessels in the renal hilus. 15 This blood flow may produce sufficient contrast material on the delayed angiograms to produce a renal nephrogram or the delayed appearance of a visualized distal main renal artery. These angiographic features were major predictive determinants in helping to decide which totally obstructed kidneys should be considered for revascularizationo The presence of a patent distal main artery was encountered in all patients with successful restoration of renal function and was an important prerequisite for the developed collateral blood flow to gain access to the renal parenchyma. Preoperative biopsy evidence of preserved glomerular morphology was the most significant predictive criterion in determining whether vascular repair would reverse renal function. Histologically, viable glomeruli in a well selected, representative specimen of renal tissue were consistently present in the group that had satisfactory restoration of renal function. 6 • 8 • 9 · 16 Widespread tubular atrophy with interstitial fibrosis and arteriolar thickening did not have any prognostic significance and merely reflected the histologic changes of chronic reversible renal ischemia. This latter histologic finding, exemplified in our series, may be a signal to the presence of pre-existing chronic renal artery stenosis, which permitted a well developed post-occlusive collateral circulation to be present when complete arterial obstruction developed. If complete renal artery occlusion occurs slowly collateral circulation has been reported to be sufficient to maintain normal renal size and normal renal function. 130 17 However, the absence of visualized collateral channels did not exclude their presence in 2 patients with normal preoperative glomerular histology who were successfully revascularized with good functional return. Patients with sudden acceleration of the pre-existing mild hypertension and a non-functioning silent kidney with complete renal artery occlusion are likely to have recovery of renal
function if angiography demonstrates a rich network of hilar collateral vessels with delayed filling of the main renal artery or a parenchymal nephrogram, surgical exploration establishes the presence of a patent distal vessel with proximal occlusion and the renal biopsy reveals intact glomerular morphology with focal widespread tubular atrophy. This last finding reflects the effect of chronic renal artery stenosis and ischemia and may be substantial evidence for the likelihood of a prior well developed extrarenal collateral circulation, which can maintain potentially viable renal parenchyma in the event of main renal artery occlusion. REFERENCES
1. Schoenbaurn, S., Goldman, M. A. and Siegelman, S. S.: R,ena!
artery embolization. Angiology, 22: 332, 1971. 2. Possati, L., Pierangeli, A., Del Gaudio, A. and Gozzeti, G.: Traitement chirurgical de l'hypertension arterielle par obstruction complete de l'artere renale. Lyon Chir., 66: 13, 1970. 3. Brest, A. N., Bower, R. and Heider, C.: Renal functional recovery following anuria secondary to renal artery embolism. J.A.M.A., 187: 540, 1964. 4. Perkins, R. P., Jacobsen, D.S., Feder, F. P., Lipchik, E. 0. and Fine, P. H.: Return of renal function after late embolectomy. Report of a case. New Engl. J. Med., 276: 1194, 1967. 5. Thomas, T. V., Faulconer, H. T. and Lansing, A. M.: Management of embolic occlusion of renal arteries. Surgery, 65: 576, 1969.
6. Mundth, E. D., Shine, K. and Austen, W. G.: Correction of malignant hypertension and return ofrenal function following late renal artery embolectomy. Amer. J. Med., 46: 985, 1969. 7. Sullivan, M. J., Cronin, R., Lackner, L. H. and Edwards, W. S.: Embolization of a solitary kidney. Successful embolectomy after nine days. J.A.M.A., 222: 82, 1972. 8. Sheil, A.G. R., Stokes, G. S., Tiller, D. J., May, J., Johnson, J. R. and Stewart, J. H.: Reversal of renal failure by revascu-· larisation of kidneys with thrombosed renal arteries. Lancet, 2: 865, 1973. 9. Morgan, T., Wilson, M., Johnston, W., Clunie, G. J. and Gordon, R.: Restoration of renal function by arterial surgery. Lancet, l: 653, 1974. 10. Quantock, 0. P. and Thatcher, G. N.: Reversible renal failure with renal artery occlusion. Brit. Med. J., 2: 27, 1972. 11. Morris, G. C., Jr., Heider, C. F. and Moyer, J. H.: The protective effect of subfiltration arterial pressure of the kidney. Su:rg. Forum, 6: 623, 1956. 12. Zinman, L. and Libertino, J. A.: Revascularization of the totally occluded renal artery (abstract). Circulation, vol. 48, suppl. 4, p. 31, 1973. 13. Brohn, L and Stener, I.: Collaterals in obstruction of the rens.l artery. Acta Radiol. (diagn.), 4: 449, 1966. 14. Abrams, H. L. and Cornell, S. H.: Patterns of collateral flow in renal ischemia. Radiology, 84: 1001, 19650 15. Boijsen, E.: Angiographic studies of the anatomy of single and multiple renal arteries. Acta Radiol., suppl. 183, 1959. 16. Besarab, A., Brown, R. S., Rubin, N. T., Salzman, E., Wirthlin, L., Steinman, T., Atha, R.R. and Skillman, J. J.: Reversible renal failure following bilateral renal artery occlusive diseaseo Clinical features, pathology, and the role of surgical revascularization. J.A.M.A., 235: 2838, 1976. 17. Dobrzinsky, S. J., Voegeli, E., Grant, H. A., Christlieb, Ao R.., Abrams, H. L. and Hickler, R. B.: Spontaneous reestablishment of renal function after complete occlusion of a renal artery. Arch. Intern. Med., 128: 266, 1971.
