REVIEW ARTICLE
RENAL ARTERIOVENOUS
EDWARD
MESSING,
ROBERT
KESSLER,
PATRICK
FISTULiS”
M.D. M.D.
B. KAVANEY,
M.D.
From the Department of Surgery, Division of Urology, Stanford University School of Medicine, Stanford, California
ABSTRACT - A review of the literature reveals that aggressive treatment of symptomatic intrarenal arteriovenousjstulas, whether by surgical or radiologic techniques, is generally indicated. The exception is thosejstulas which result from closed renal biopsy since these usually heal spontaneously. The ultimate goal of any form of therapy is the maximal preservation of renal tissue. Methods of treatment are discussed, and a review of classification, etiology, incidence, symptoms, physiologic consequences, and means of diagnosis is given. A case of post-traumatic intrarenal arteriovenous fistula with ipsilaterallu elevated renal vein renin and hypertension, cured by partial nephrectomy, is presented.
There have been about 200 documented cases of renal arteriovenous fistulas reported in the world literature.‘*2 Most of these have been diagnosed in recent years because of the increasing use of both percutaneous needle biopsy of the kidney and renal arteriography as diagnostic tools. A surprisingly high number of these patients present with classic findings including an abdominal bruit, congestive heart failure, cardiomegaly, hypertension, abdominal pain, and hematuria. Traditionally, these patients have been treated by nephrectomy. In recent years, however, with advances in vascular surgery and angiography, a variety of renal-sparing procedures have been utilized with great success. These include partial nephrectomy, branch ligation of the renal artery, excision of the individual fistulas or feeding vessels, and even angiographic embolization of feeding vessels. We present here a case of posttraumatic renal arteriovenous fistula with subsequent review of the literature and emphasis on modalities of management. Case Report A twenty-nine-year-old black male truck-driver was first seen in the emergency room in April,
*Supported in part by National Institutes Grant 08-TO1 AM05513A.
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1975, complaining of twelve hours of gross hematuria with the passage of clots, right flank and upper right abdominal quadrant pain, nausea, and vomiting. Twenty years before, the patient was hit by a tree limb in the right posterior chest, suffering four fractured ribs, hemopneumothorax, and gross hematuria which subsided spontaneously. His blood pressure in November, 1973, was 120/70 mm. Hg on several determinations. Six months later he was found to be mildly hypertensive but no medical therapy or dietary controls were recommended. In February, 1975, the patient had an episode of painless hematuria which lasted a few hours and did not recur. On his present admission the pertinent physical findings included a blood pressure of 160/110 mm. Hg, an enlarged heart with a point of maximal impulse at the sixth intercostal space on the midclavicular line, moderate right upper quadrant and right costovertebral angle tenderness, and a continuous bruit which was lateral to the right midclavicular line and 1 cm. inferior to the costal margin. The patient denied fever, chills, stone passage, or irritative urinary symptoms. Urinalysis on admission showed many red blood cells, but was otherwise normal. Urine culture, complete blood count, all coagulation studies, sickle-cell preparation, glucose, and
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TABLE
1.
Plasma renin activity
Site
Preoperative*
Postoperativei
Right renal vein Left renal vein Inferior vena cava (below renal veins)
78 38 45
8 7 7
*Preoperative urinary sodium 44 mEq. per twenty-four hours. Normal renin values of a 10 mEq. sodium diet are 13 to 47 ng. per liter per minute of angiotensin I generated; measured by immunoassay. tPostoperative urinary sodium 118 mEq. per twenty-four hours. Normal renin values for a 309 mEq. sodium diet are 3 to 8 ng. per liter per minute.
serum electrolytes were normal. Twenty-fourhour urine collections revealed normal excretion of 17 hydroxy- and 17 ketosteroids, as well as vanilmandelic acid. Corrected creatinine clearance was 107 ml. per minute. Electrocardiogram indicated left ventricular hypertrophy by voltage criteria, and chest x-ray film showed minimal cardiomegaly and slight vascular congestion (Fig. 1A). Excretory urogram failed to show excretion in the right collecting system; the delayed nephrogram effect was substantially more pronounced in the upper pole (Fig. 1B). The contrast material was entirely excreted within twelve hours without passage of a stone. The patient was treated with intravenous hydration while his hematuria and pain subsided; hypertension persisted. Cystoscopy was normal with clear efflux coming from both ureters. Right retrograde urogram revealed minimally dilated upper tracts with small filling defects within the pelvis which were thought to be clots. A renal angiogram demonstrated a large arteriovenous fistula in the inferioventral aspect of the right kidney. A diminished nephrogram phase was again seen in the lower pole (Fig. 1C and D). The right renal vein contained more than twice the plasma renin activity present in the left renal vein (Table I). On the following day hematuria and pain recurred, and the patient underwent transperitoneal right lower pole nephrectomy with prior control of the renal pedicle. His postoperative course was uneventful, and by one week after surgery blood pressure had dropped to 140/80 mm. Hg. Three weeks after surgery blood pressure was 120175 mm. Hg, and repeat excretory urogram revealed good function on the right side with a defect in the right lower pole consistent with the tissue removed at surgery. Several months after surgery the patient was normotensive. Roentgenogram of the chest done
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at that time showed a 2.2-cm. reduction in the transverse diameter of the heart and decreased vascularity in the pulmonary tree (Fig. 1E). Cardiomegaly could not be appreciated on either physical examination or electrocardiogram. Corrected creatinine clearance was I.21 ml. per minute. Repeat angiograms did not show the arteriovenous fistula, and there was good preservation of renal tissue on the right (Fig. 1F). Although he was not on a low-sodium diet, plasma renin activity was similar in both renal veins and the inferior vena cava twelve weeks after surgery (Table I). The surgical specimen showed arteriovenous communications and mild thickening of anterior walls. The patient has returned to work and is well (ten months of follow-up), Classification and Etiology Renal arteriovenous (A-V) fistulas are described as either congenital or acquired, etiologic classifications based on angiographic criteria. Congenital fistulas have a cirsoid configuration with multiple communications between arteries and veins; they are considered congenital because the angiographic appearance is typical of known congenital A-V malformations in other areas of the body.lm4 Despite their (presumed) congenital nature, these malformations generally do not present clinically until the patients are adults. 5*6They have an equal sex incidence6 and account for less than one quarter of all renal A-V fistulas (Table II). lA4 Acquired A-V fistulas are also defined by angiographic criteria; they appear as solitary communications between artery and vein and account for almost three quarters of all renal A-V fistulas. iB2
TABLE
II.
Etiology of congenital and acquired jistulas
Percentages of All A-V Fistulas*
Etiology
Renal
Congenital “Congenital” Idiopathic Acquired Post needle biopsy Trauma
22 to 25 3 to 5 35 to 40 15 to 20 10 3 to 5 5
Tumor Postsurgery Inflammatory-other *These percentages published
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FIGURE 1. (A) Preoperative chest radiograph. (B) Three-and-one-half-hour delayedfilm on initial intravenous urogram; note increased nephrogram effect, reduced nephrogram phase in lower pole (arrow), and lack of opaci$cation of collecting system on right. (C) Early (one second) preoperative selective right renal arteriogram: reduced nephrogram (arrow) is seen in parenchyma which lies distal to large arteriovenous fistula. (D) Eater (nine seconds) preoperative selective right renal arteriogram: diminished nephrogram in lower pole, and dense opacij%ation of inferior vena cava is observed. (E) Two months postoperative chest x-ray film: note change from (A) in cardiac shape, reduction of transverse cardiac diameter by 2.2 cm., and decrease in upper lobe vascularity. (F) Postoperative selective right renal arteriogram: small arrow demonstrates take off of artery which formerly supplied jistula; note good preservation of renal tissue.
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The term idiopathic is used to describe those fistulas whose angiographic appearance is similar to that of acquired A-V communications, but whose origins are thought to be renal artery or branch renal artery aneurysms which have eroded into veins.2,8*9 A similar mechanism is also postulated for post-traumatic and postsurgical A-V fistulas. lo More than 35 per cent of all A-V fistulas are caused by needle biopsy (Table II). Seventy-five per cent of these patients had diastolic hypertension before the biopsy was performed.’ A-V communications occasionally develop immediately after trauma. These appear on angiograms which are done for initial evaluation of the extent of injury. They can also occur months to years afterward, as happened in our patient. This group accounts for about 15 per cent of all fistulas (Table II).2 Seventy-five per cent of patients in whom A-V fistulas develop after trauma have had penetrating injuries. l1 Those A-V fistulas which occur after surgery are almost exclusively in patients who have had either partial nephrectomies or nephrolithotomies, and account for 3 to 5 per cent of all fistulas (Table II).5,12 In hypernephromas and rarely in other renal neoplasms, hemodynamically significant solitary communications between large arteries and veins result from erosion of tumor into the vessels.4-6 These represent 10 to 15 per cent of all A-V fistulas (Table II).2 Some authors believe that those patients with renal tumors whose angiograms reveal only very small A-V fistulas but who present with congestive heart failure may have an accumulative effect from these fistulas which is hemodynamically the same as a single huge fistula. ‘,12 Other groups of acquired fistulas are those associated with inflammation (granulomas, subacute bacterial endocarditis, or infection stones), polycystic kidney and fibromuscular dysplasia of the renal arteries; together they represent less than 5 per cent of all fistulas (Table II).4,5 Pathophysiology Those A-V fistulas which occur after nephrectomy have been attributed to the use of mass ligation of, and transfixion sutures in, the renal pedicle, packing of the renal bed, infection, and recurrent tumor.‘*13 Less than 20 cases have been recorded in the world literature.‘,5,‘3 As with all acquired A-V fistulas the symptoms in this group may occur many years after the original surgical procedure. However, because no renal paren-
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chyma is found distal to the fistula, they are physiologically distinct from the group with ipsilaterally intact kidneys. lo Like all peripheral A-V fistulas they create a high venous return, an increase in cardiac output, and sometimes, a rise in systolic blood pressure. This leads to a reduction in peripheral resistance and a decrease in diastolic blood pressure. If the heart cannot compensate for this shunt while trying to meet increased tissue demands, high output cardiac failure will naturally result. 1*2,7~10~14 On the other hand if there is any renal tissue distal to the fistula, it will receive diminished perfusion with a narrowed pulse pressure.‘.1°*14 While the hemodynamic changes resulting in increased systolic blood pressure still occur when the fistula exists proximal to the kidney, there may also be an increase in diastolic blood pressure, presumably due to renal ischemia as occurs in the Goldblatt 7,10,15,16 Th ese patients can have high output cardiac failure, increased systolic blood pressure, and increased diastolic blood pressure. Based on functional studies such as renograms, split function tests, and intravenous urograms, as well as histologic analysis of the excised renal tissue, it has been postulated that increased renin secretion from this ischemic tissue is responsible for the diastolic hypertension. ‘,l”,17 However, confirmation of elevated renal vein renin in any of the previous hypertensive patients with A-V fistulas has been rare.lJ2J5J8 It is thought that technical factors dealing with the collection of these samples, specifically that the venous fistula has primarily arterial blood flowing through it, may be responsible for the inability to demonstrate high renal vein renin activity in most of kidney.
TABLE
III. Chical
presentation
Clinical Manifestations
Percentages
Intra-abdominal bruit Cardiomegaly Congestive heart failure (85 per cent obviously symptomatic in Sechas’ series)22 Diastolic hypertension Abdominal or flank pain Hematuria (>75 per per cent is gross hematuria) Intra-abdominal mass (tumor or rupture) Headache, lightheadedness
70 to 75 48 to 57 43
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43 to 50 26 to 34 33 (65 in O’Brien’s series)’
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attempts these patients. 12,16To date experimental to create intrarenal19 or extrarenalzO”l fistulas in animals have not been helpful; it has proved difficult to produce either diastolic hypertension or increased renin secretion. Clinical
Presentation
the kidney will have these close spontaneously within eighteen months. 12,28 Hence, close observation and supportive care is usually sufficient in this group of patients. An undetermined but presumably much smaller number of the fistulas which are documented shortly after trauma will also close spontaneously. l1 While we have found 6 such cases reported in the literature, 11,30one could argue in favor of early surgical repair even in this group; the majority (7 of 13) of these patients treated expectantly eventually required surgery (often nephrectomy). Of those who did not, a protracted hospital course and considerable morbidity occurred. In those patients who have symptomatic fistulas which are not secondary to renal biopsy, surgical intervention is generally indicated. There have been a few cases of frank rupture and exsanguinating hemorrhage in those patients who have refused surgery and who have been treated conservatively.31*32 Of more importance more than 60 per cent of patients with renal A-V fistulas and hypertension (85 per cent of those with hypertension secondary to post-traumatic A-V fistulas) will have the hypertension cured by repair of the fistula. Almost all other patients with hypertension will be easier to manage medically if the fistula is surgically corrected. Similarly, congestive heart failure will almost certainly be controlled once the fistula is removed.
of A-V Fistulas
The clinical presentation of this syndrome is very impressive because many patients have symptomatic congestive heart failure, hypertension, and gross hematuria (Table III). Almost three quarters of the patients have a continuous abdominal bruit.1,2,4*22 While no large series has addressed this question, in most of the case reports in which sufficient data are given, the chest x-ray film, cardiogram, venous blood gases, and circulation time have confirmed the presence of hypertension or a high cardiac output.7,23 The intravenous urogram is normal in about one half of the patients. ’ Abnormalities are variable and include nonvisualization of the kidney, intrapelvic defects, calyceal displacement by the fistula,4,24 and, in both acquiredz5 and congenital 26,27 fistulas, cobblestone-like indentations of the intrarenal collecting system by tortuous collateral (and tumor) vessels. Renogram and isotope studies may indicate the area of ischemia in the kidney and can sometimes visualize the abnormalities in flow to that region.7,28 The definitive diagnosis is made by renal arteriogram. This, of course, will distinguish a fistula from arterial stenosis, where a bruit and hypertension are also typical. Significantly, in our patient and in othersz9 a reduced nephrogram was seen in the parenchyma distal to the fistula, supporting the proposed mechanism of ischemia distal to the shuntingofblood (Fig. lB, C, and D). As noted earlier the aggressive use of this technique, both in the management of trauma and in the evaluation of hypertensive and tumor patients, has caused greater recognition of A-V fistulas in recent years.
Modes
Traditionally, nephrectomy is the most common operation, and this is still the suggested method of treatment when the fistula is caused by tumor or congenital malformation.33 If the congenital lesion is small and well localized, partial nephrectomy is a reasonable approach. As with congenital A-V malformations in other areas of the body, attempts at simple branch ligation frequently fail to obliterate the fistula.33 Moreover, since most of these are intrarenal as much renal tissue may be destroyed by an attempted vascular correction as by a partial nephrectomy. Those patients who have the acquired type of A-V fistula generally warrant a renal-sparing procedure. Several authors have tried to ligate the feeding vessels to the intrarenal A-V fistula. Although these procedures usually have been successful, there have been several reported recurrences. 1,33 Experiments on peripheral fistulas indicate that recurrence is likely unless the distal artery and collateral vessels (which may be present in an intrarenal A-V malformationz5)
Management Once the diagnosis of arteriovenous fistula of the kidney has been made, the surgeon is faced with several therapeutic options. The first decision is whether operative or conservative management is indicated. Whatever decision is made, supportive medical therapy to control heart failure, hypertension, and anemia is often required. Approximately 70 per cent of patients who sustain A-V fistulas secondary to needle biopsy of
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are not also ligated. l4 Postoperative angiography often shows that as much tissue has been infarcted as when a partial nephrectomy is perforrned.‘~‘s,~~*~~In one series 2 of the 3 patients treated with branch ligation had persistence of their hypertension postoperatively.34 Many techniques which attempt to locate the specific feeding vessels intraoperatively have been utilized. They all involve the detection of a thrill (either by palpation or by auscultation with sterile stethoscope or Doppler and recognition of its cessation after ligating various arteries. 18,2335 These procedures, as reported, appear tedious and time-consuming, often because of the difficult intrarenal dissection required. We have found, as have others, that partial nephrectomy, particularly with an intrarenal lesion that involves one of the poles, offers a simpler procedure with a surer result and with probably no greater loss of kidney parenchyma than occurs with intrarenal branch artery ligation. 17*36 When the fistula lies extrarenally, particularly in the renal hilum, ligation of the individual vessels and excision of the aneurysmal sac is the best approach, although vascular reconstruction is sometimes required. 33,37This is not unlike the approach used for A-V fistulas in peripheral locations. With the advent of safer bench surgery in the future, less accessible lesions may be ligated individually or excised with a maximal preservation of renal tissue. Several radiologists have attempted embolization or occlusion of the fistula through angiographic techniques. 38-40The most frequently used method is embolization with either autologous clot or other foreign matter (fat, “Gelfoam,” or metallic pellets) injected into specific branch renal arteries visualized by selective renal angiograms.38B3gThis technique is used primarily in patients with postbiopsy fistulas where the arteriovenous connections are usually in small vessels. Since almost three quarters of post needle biopsy fistulas close spontaneously, perhaps many would have closed without such angiographic intervention. After embolization is performed the feeding vessels do not clot off because they have an intact intima which produces fibrinolysin. The fistulas do not have normal intima and, hence, thrombose.3g Invariably, a small area of infarction results, but fortunately there have been no cases of pulmonary emboli or other untoward events secondary to this procedure.38-40 In general, embolization is reserved for those patients who are considered poor surgical candidates.
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A more promising angiographic technique involves inserting a balloon catheter into the fistula and occluding the feeding vessels: a method that has been used with a great deal of success (as has the embolization technique) in various A-V malformations in both the central nervous system and peripheral vascular tree. 41The balloon catheter is a particularly attractive technique in large intrarenal fistulas which occur in the midportion of the kidney where a partial nephrectomy, or elaborate vascular surgery, destroys much renal tissue. Occlusion, as opposed to embolization, offers greater control of the specific vessels to be blocked;38 it also reduces the likelihood of potentially fatal pulmonary emboli. Preventive therapy in the management of A-V fistulas must also be considered. Little can be done to prevent acquired and congenital fistulas, but those which occur postnephrectomy can be avoided by ligating the renal pedicle vessels individually. Similarly, while prospective, retrospective, and experimental studies demonstrate that in at least 15 per cent of patients undergoing closed needle biopsy, fistulas will subsequently develop; 12~28~28 biopsies performed under fluoroscopic guidance with contrast material in the renal collecting system are associated with a lower incidence of complications, including subsequent hemorrhage and A-V fistula formations.42 Moreover, those patients who have severe hypertension or clotting abnormalities should be considered for open biopsy43 since there is an increased risk of these complications developing postbiopsy. In summary the diagnosis of A-V fistulas rests on a high index of clinical suspicion. An abdominal bruit, particularly when present with hypertension, hematuria, heart failure, or a history of trauma or renal surgery, should suggest the diagnosis of a renal arteriovenous fistula. Even if the intravenous urogram is normal, selective renal angiography should be considered. Stanford, California 94305 (DR. KESSLER) References O’BRIEN, D. P., PARROTT, T. S., WALTON, K. N., and LEWIS, E. L.: Renal arteriovenous fistulas, Surg. Gynecol. Obstet. 139: 739 (1974): MCALHANY, J. C., BLACK, H. C., HANBACK, L. D., and YARBROUGH, D. R.: Renal arteriovenous fistula as a cause ofhypertension, Am. J. Surg. 122: 117 (1971). DESAI, S. G., and DESAUTELS, R. E.: Congenital arteriovenous malfortiation of the kidney, J. Ural. 110: 17 (1973).
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4. MALDONADO,J. E., and SHEPS, S. G.: Renal arteriovenous fistula, Postgrad. Med. 40: 263 (1966). 5. KELLEY, D. G.: Renal arteriovenous fistula: a report of four cases and review of the literature, Br. J. Urol. 39: 162 (1967). 6. THOMASON, W. B., et al. : Intrarenal arteriovenous fistulas, J. Urol. 108: 526 (1972). 7. MALDONADO,J. E., et al. : Renal arteriovenous fistula: a reversible cause of hypertension and heart failure, Am. J. Med. 37: 499 (1964). 8. THOMAS, R. G., GRIEVE, S., and LJIWIN, B.: Spontaneous renal arteriovenous fistula and contralateral renal artery aneurysms, Br. J. Radiol. 35: 128 (1962). 9. BRON, K. M., and REDMAN, H. : Renal arteriovenous fistula and fibromuscular hyperplasia: a new association, Ann. Intern. Med. 68: 1039 (1968). 10. MILLOY, F., FELL, E. H., DILLON, R. F., and ZAYAS, A. M.: Intrarenal arteriovenous fistula with hypertensive cardiovascular disease, Am. J. Surg. 96: 3 (1958). 11. COSGROVE, M. D., MENDEZ, R., and MORROW, J. . Traumatic renal arteriovenous fistula: report of 12 zses J. Urol. 110: 627 (1973). 12. NELS)ON, B. D., BROSMAN, S. A., and GOODWIN, W. E.: Renal arteriovenous fistulas, ibid. 109: 779 (1973). 13. CHEW, Q. T., and MADAYAG, M. A.: Post-nephrectomy arteriovenous fistula, ibid. 109: 546 (1973). 14. HOLMAN, E., and TAYLOR, G.: Problems in the dynamics of blood flow. II. Pressure relations at the site of an arteriovenous fistula, Angiology 3: 415 (1952). 15. STOCKIGT, J. R., et al.: Renal vein renin in various forms of renal hypertension, Lancet 1: 1194 (1972). 16. JAHNKE, R. W., MESSING, E. M., and SPELLMAN, M. c.: Hypertension and post-traumatic renal arteriovenous fistula; documentation of unilateral renin secretion, J. Urol., in press. 17. RIBA, L. W., and SIMON, M. P.: Intrarenal arteriovenous fistula treated with partial nephrectomy, ibid. 98: 293 (1967). 18. WISE, H. A., WINTER, C. C., MOLNAR, W., and BUSH, C. A.: Management of renal arteriovenous fistula and carcinoma in the opposite kidney: an unusual combination, ibid. 112:433 (1974). Blood pressure and 19. EKELUND, L., and GOTHLIN, J.: intrarenal arteriovenous fistulae: an experimental study in rabbits, Stand. J. Urol. Nephrol. 7: 210 (1973). Effects on kidney and 20. LASHER, E. P., and GLENN, F.: blood pressure of artificial communication between renal artery and veins, Arch. Surg. 38: 886 (1939). 21. SECREST, A. J.: Experimental renal arteriovenous fistula, J. Urol. 102: 552 (1969). 22. SECHAS, M. N., PLESSAS, S. N., and SKALKEAS,G. D.: Post-traumatic renovascular hypertension, Surgery 76: 666 (1974). 23. GIBBONS, R. P., CORREA, R. J., and TREMANN, J. R.: Management of intrarenal vascular malformations, Urology 1: 136 (1973). 24. BOIJSEN, E., and KOHLER, R.: Renal arteriovenous fistulae, Acta Radiol. 57: 433 (1962). 25. KINKHABWALA, M., DZIADIW, R., and PATIL, U.:
Intrarenal arterial< collaterals simulating malignant tumor in traumatic arteriovenous fistula, Urology 4: 715 (1974). 26. MARK, L. K. : Arteriovenous malformations of kidney, ibid. 4: 706 (1974). 27. CLOUSE, M. E., and ADAMS, D. E.: Congenital renal arteriovenous malformation: angiography in its diagnosis, ibid. 5: 282 (1975). 28. EKELUND, L., et al. : Arteriovenous fistulas following renal biopsy with hypertension and hemodynamic changes: report of a case studied by dye-dilution technique, J. Urol. 108: 373 (1972). 29. LANG, E. K., et al. : Renal angiography in the assessment of renal trauma, Radiology 98: 103 (1971). 30. Rous, S. N.: The value of serial selective renal angiography in the delayed management of renal trauma, J. Urol. 107: 345 (1972). 31. SANOUDUS,G. M., BERENBAUM, E., and CLAUSS, R. H.: Ruptured renal arteriovenous fistula, J.A.M.A. 219: 1581(1972). 32. JANTET, G. H., FOOT, E. C., ~~~KENYON, J. R.: Rupture of an intrarenal arteriovenous fistula secondary to carcinoma: a case report, Br. J. Surg. 49: 404 (1962). 33. TYNES, W. V., DEVINE, C. J., DEVINE, P. C., and POUTASSE, E. F. : Surgical treatment of renal arteriovenous fistulas: report of5 cases, J. Urol. 103: 692 (1970). 34. COSGROVE, M. D., MENDY, R., and MORROW, J. W.: Branch artery ligation for renal arteriovenous fistula, ibid. 110: 632 (1973). 35. PALMER, J. M., and CONNOLLY, J. E.: Intrarenal arteriovenous fistula: surgical excision under selective renal hypothermia with kidney survival, ibid. 96: 599 (1966). 36. SCHWEITZER, F. A.: Conservative surgery for renal arteriovenous aneurysms, Guy Hosp. Rep. 121: 205 (1972). 37. MERKEL, F. K., and SAKO, Y.: Surgical treatment for traumatic renal arteriovenous fistulas, Arch. Surg. 101: 438 (1970). 38. RIZK, G. K., ATALLAH, N. K., and BRIDI, G. I.: Renal arteriovenous fistula treated by catheter embolization, Br. J. Radiol. 46: 222 (1973). 39. SILBER, S. J.. and CLARK, R. E.: Treatment of massive hemorrhage after renal biopsy with angiographic injection of clot, N. Engl. J. Med. 292: 1387 (1975). 40. BOOKSTEIN, J. J., and GOLDSTEIN, H. M.: Successful management of post biopsy arteriovenous fistula with selective arterial embolization, Radiology 109: 535 (1973). 41. BENTSON, J. R., and CRANDALL, P. H.: Use of the Fogarty catheter in arteriovenous malformations of the spinal cord, ibid. 105: 65 (1972). 42. MCCANSE, L. R., CROSSE, D., WHITTIER, F., and MEBUST, W. K.: Percutaneous renal biopsy with localization by retrograde pyelogram, Proc. Kimbrough Urological Sem. 8: 94 (1974). 43. PATIL, J., BAILEY, G. L., and MAHONEY, E. F.: Open-renal biopsy in uremic patient, Urology 3: 293 (1974).
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107
RENAL ARTERIOVENOUS
EDWARD
MESSING,
ROBERT
KESSLER,
PATRICK
FISTULiS”
M.D. M.D.
B. KAVANEY,
M.D.
From the Department of Surgery, Division of Urology, Stanford University School of Medicine, Stanford, California
ABSTRACT - A review of the literature reveals that aggressive treatment of symptomatic intrarenal arteriovenousjstulas, whether by surgical or radiologic techniques, is generally indicated. The exception is thosejstulas which result from closed renal biopsy since these usually heal spontaneously. The ultimate goal of any form of therapy is the maximal preservation of renal tissue. Methods of treatment are discussed, and a review of classification, etiology, incidence, symptoms, physiologic consequences, and means of diagnosis is given. A case of post-traumatic intrarenal arteriovenous fistula with ipsilaterallu elevated renal vein renin and hypertension, cured by partial nephrectomy, is presented.
There have been about 200 documented cases of renal arteriovenous fistulas reported in the world literature.‘*2 Most of these have been diagnosed in recent years because of the increasing use of both percutaneous needle biopsy of the kidney and renal arteriography as diagnostic tools. A surprisingly high number of these patients present with classic findings including an abdominal bruit, congestive heart failure, cardiomegaly, hypertension, abdominal pain, and hematuria. Traditionally, these patients have been treated by nephrectomy. In recent years, however, with advances in vascular surgery and angiography, a variety of renal-sparing procedures have been utilized with great success. These include partial nephrectomy, branch ligation of the renal artery, excision of the individual fistulas or feeding vessels, and even angiographic embolization of feeding vessels. We present here a case of posttraumatic renal arteriovenous fistula with subsequent review of the literature and emphasis on modalities of management. Case Report A twenty-nine-year-old black male truck-driver was first seen in the emergency room in April,
*Supported in part by National Institutes Grant 08-TO1 AM05513A.
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1975, complaining of twelve hours of gross hematuria with the passage of clots, right flank and upper right abdominal quadrant pain, nausea, and vomiting. Twenty years before, the patient was hit by a tree limb in the right posterior chest, suffering four fractured ribs, hemopneumothorax, and gross hematuria which subsided spontaneously. His blood pressure in November, 1973, was 120/70 mm. Hg on several determinations. Six months later he was found to be mildly hypertensive but no medical therapy or dietary controls were recommended. In February, 1975, the patient had an episode of painless hematuria which lasted a few hours and did not recur. On his present admission the pertinent physical findings included a blood pressure of 160/110 mm. Hg, an enlarged heart with a point of maximal impulse at the sixth intercostal space on the midclavicular line, moderate right upper quadrant and right costovertebral angle tenderness, and a continuous bruit which was lateral to the right midclavicular line and 1 cm. inferior to the costal margin. The patient denied fever, chills, stone passage, or irritative urinary symptoms. Urinalysis on admission showed many red blood cells, but was otherwise normal. Urine culture, complete blood count, all coagulation studies, sickle-cell preparation, glucose, and
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TABLE
1.
Plasma renin activity
Site
Preoperative*
Postoperativei
Right renal vein Left renal vein Inferior vena cava (below renal veins)
78 38 45
8 7 7
*Preoperative urinary sodium 44 mEq. per twenty-four hours. Normal renin values of a 10 mEq. sodium diet are 13 to 47 ng. per liter per minute of angiotensin I generated; measured by immunoassay. tPostoperative urinary sodium 118 mEq. per twenty-four hours. Normal renin values for a 309 mEq. sodium diet are 3 to 8 ng. per liter per minute.
serum electrolytes were normal. Twenty-fourhour urine collections revealed normal excretion of 17 hydroxy- and 17 ketosteroids, as well as vanilmandelic acid. Corrected creatinine clearance was 107 ml. per minute. Electrocardiogram indicated left ventricular hypertrophy by voltage criteria, and chest x-ray film showed minimal cardiomegaly and slight vascular congestion (Fig. 1A). Excretory urogram failed to show excretion in the right collecting system; the delayed nephrogram effect was substantially more pronounced in the upper pole (Fig. 1B). The contrast material was entirely excreted within twelve hours without passage of a stone. The patient was treated with intravenous hydration while his hematuria and pain subsided; hypertension persisted. Cystoscopy was normal with clear efflux coming from both ureters. Right retrograde urogram revealed minimally dilated upper tracts with small filling defects within the pelvis which were thought to be clots. A renal angiogram demonstrated a large arteriovenous fistula in the inferioventral aspect of the right kidney. A diminished nephrogram phase was again seen in the lower pole (Fig. 1C and D). The right renal vein contained more than twice the plasma renin activity present in the left renal vein (Table I). On the following day hematuria and pain recurred, and the patient underwent transperitoneal right lower pole nephrectomy with prior control of the renal pedicle. His postoperative course was uneventful, and by one week after surgery blood pressure had dropped to 140/80 mm. Hg. Three weeks after surgery blood pressure was 120175 mm. Hg, and repeat excretory urogram revealed good function on the right side with a defect in the right lower pole consistent with the tissue removed at surgery. Several months after surgery the patient was normotensive. Roentgenogram of the chest done
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at that time showed a 2.2-cm. reduction in the transverse diameter of the heart and decreased vascularity in the pulmonary tree (Fig. 1E). Cardiomegaly could not be appreciated on either physical examination or electrocardiogram. Corrected creatinine clearance was I.21 ml. per minute. Repeat angiograms did not show the arteriovenous fistula, and there was good preservation of renal tissue on the right (Fig. 1F). Although he was not on a low-sodium diet, plasma renin activity was similar in both renal veins and the inferior vena cava twelve weeks after surgery (Table I). The surgical specimen showed arteriovenous communications and mild thickening of anterior walls. The patient has returned to work and is well (ten months of follow-up), Classification and Etiology Renal arteriovenous (A-V) fistulas are described as either congenital or acquired, etiologic classifications based on angiographic criteria. Congenital fistulas have a cirsoid configuration with multiple communications between arteries and veins; they are considered congenital because the angiographic appearance is typical of known congenital A-V malformations in other areas of the body.lm4 Despite their (presumed) congenital nature, these malformations generally do not present clinically until the patients are adults. 5*6They have an equal sex incidence6 and account for less than one quarter of all renal A-V fistulas (Table II). lA4 Acquired A-V fistulas are also defined by angiographic criteria; they appear as solitary communications between artery and vein and account for almost three quarters of all renal A-V fistulas. iB2
TABLE
II.
Etiology of congenital and acquired jistulas
Percentages of All A-V Fistulas*
Etiology
Renal
Congenital “Congenital” Idiopathic Acquired Post needle biopsy Trauma
22 to 25 3 to 5 35 to 40 15 to 20 10 3 to 5 5
Tumor Postsurgery Inflammatory-other *These percentages published
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FIGURE 1. (A) Preoperative chest radiograph. (B) Three-and-one-half-hour delayedfilm on initial intravenous urogram; note increased nephrogram effect, reduced nephrogram phase in lower pole (arrow), and lack of opaci$cation of collecting system on right. (C) Early (one second) preoperative selective right renal arteriogram: reduced nephrogram (arrow) is seen in parenchyma which lies distal to large arteriovenous fistula. (D) Eater (nine seconds) preoperative selective right renal arteriogram: diminished nephrogram in lower pole, and dense opacij%ation of inferior vena cava is observed. (E) Two months postoperative chest x-ray film: note change from (A) in cardiac shape, reduction of transverse cardiac diameter by 2.2 cm., and decrease in upper lobe vascularity. (F) Postoperative selective right renal arteriogram: small arrow demonstrates take off of artery which formerly supplied jistula; note good preservation of renal tissue.
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The term idiopathic is used to describe those fistulas whose angiographic appearance is similar to that of acquired A-V communications, but whose origins are thought to be renal artery or branch renal artery aneurysms which have eroded into veins.2,8*9 A similar mechanism is also postulated for post-traumatic and postsurgical A-V fistulas. lo More than 35 per cent of all A-V fistulas are caused by needle biopsy (Table II). Seventy-five per cent of these patients had diastolic hypertension before the biopsy was performed.’ A-V communications occasionally develop immediately after trauma. These appear on angiograms which are done for initial evaluation of the extent of injury. They can also occur months to years afterward, as happened in our patient. This group accounts for about 15 per cent of all fistulas (Table II).2 Seventy-five per cent of patients in whom A-V fistulas develop after trauma have had penetrating injuries. l1 Those A-V fistulas which occur after surgery are almost exclusively in patients who have had either partial nephrectomies or nephrolithotomies, and account for 3 to 5 per cent of all fistulas (Table II).5,12 In hypernephromas and rarely in other renal neoplasms, hemodynamically significant solitary communications between large arteries and veins result from erosion of tumor into the vessels.4-6 These represent 10 to 15 per cent of all A-V fistulas (Table II).2 Some authors believe that those patients with renal tumors whose angiograms reveal only very small A-V fistulas but who present with congestive heart failure may have an accumulative effect from these fistulas which is hemodynamically the same as a single huge fistula. ‘,12 Other groups of acquired fistulas are those associated with inflammation (granulomas, subacute bacterial endocarditis, or infection stones), polycystic kidney and fibromuscular dysplasia of the renal arteries; together they represent less than 5 per cent of all fistulas (Table II).4,5 Pathophysiology Those A-V fistulas which occur after nephrectomy have been attributed to the use of mass ligation of, and transfixion sutures in, the renal pedicle, packing of the renal bed, infection, and recurrent tumor.‘*13 Less than 20 cases have been recorded in the world literature.‘,5,‘3 As with all acquired A-V fistulas the symptoms in this group may occur many years after the original surgical procedure. However, because no renal paren-
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chyma is found distal to the fistula, they are physiologically distinct from the group with ipsilaterally intact kidneys. lo Like all peripheral A-V fistulas they create a high venous return, an increase in cardiac output, and sometimes, a rise in systolic blood pressure. This leads to a reduction in peripheral resistance and a decrease in diastolic blood pressure. If the heart cannot compensate for this shunt while trying to meet increased tissue demands, high output cardiac failure will naturally result. 1*2,7~10~14 On the other hand if there is any renal tissue distal to the fistula, it will receive diminished perfusion with a narrowed pulse pressure.‘.1°*14 While the hemodynamic changes resulting in increased systolic blood pressure still occur when the fistula exists proximal to the kidney, there may also be an increase in diastolic blood pressure, presumably due to renal ischemia as occurs in the Goldblatt 7,10,15,16 Th ese patients can have high output cardiac failure, increased systolic blood pressure, and increased diastolic blood pressure. Based on functional studies such as renograms, split function tests, and intravenous urograms, as well as histologic analysis of the excised renal tissue, it has been postulated that increased renin secretion from this ischemic tissue is responsible for the diastolic hypertension. ‘,l”,17 However, confirmation of elevated renal vein renin in any of the previous hypertensive patients with A-V fistulas has been rare.lJ2J5J8 It is thought that technical factors dealing with the collection of these samples, specifically that the venous fistula has primarily arterial blood flowing through it, may be responsible for the inability to demonstrate high renal vein renin activity in most of kidney.
TABLE
III. Chical
presentation
Clinical Manifestations
Percentages
Intra-abdominal bruit Cardiomegaly Congestive heart failure (85 per cent obviously symptomatic in Sechas’ series)22 Diastolic hypertension Abdominal or flank pain Hematuria (>75 per per cent is gross hematuria) Intra-abdominal mass (tumor or rupture) Headache, lightheadedness
70 to 75 48 to 57 43
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attempts these patients. 12,16To date experimental to create intrarenal19 or extrarenalzO”l fistulas in animals have not been helpful; it has proved difficult to produce either diastolic hypertension or increased renin secretion. Clinical
Presentation
the kidney will have these close spontaneously within eighteen months. 12,28 Hence, close observation and supportive care is usually sufficient in this group of patients. An undetermined but presumably much smaller number of the fistulas which are documented shortly after trauma will also close spontaneously. l1 While we have found 6 such cases reported in the literature, 11,30one could argue in favor of early surgical repair even in this group; the majority (7 of 13) of these patients treated expectantly eventually required surgery (often nephrectomy). Of those who did not, a protracted hospital course and considerable morbidity occurred. In those patients who have symptomatic fistulas which are not secondary to renal biopsy, surgical intervention is generally indicated. There have been a few cases of frank rupture and exsanguinating hemorrhage in those patients who have refused surgery and who have been treated conservatively.31*32 Of more importance more than 60 per cent of patients with renal A-V fistulas and hypertension (85 per cent of those with hypertension secondary to post-traumatic A-V fistulas) will have the hypertension cured by repair of the fistula. Almost all other patients with hypertension will be easier to manage medically if the fistula is surgically corrected. Similarly, congestive heart failure will almost certainly be controlled once the fistula is removed.
of A-V Fistulas
The clinical presentation of this syndrome is very impressive because many patients have symptomatic congestive heart failure, hypertension, and gross hematuria (Table III). Almost three quarters of the patients have a continuous abdominal bruit.1,2,4*22 While no large series has addressed this question, in most of the case reports in which sufficient data are given, the chest x-ray film, cardiogram, venous blood gases, and circulation time have confirmed the presence of hypertension or a high cardiac output.7,23 The intravenous urogram is normal in about one half of the patients. ’ Abnormalities are variable and include nonvisualization of the kidney, intrapelvic defects, calyceal displacement by the fistula,4,24 and, in both acquiredz5 and congenital 26,27 fistulas, cobblestone-like indentations of the intrarenal collecting system by tortuous collateral (and tumor) vessels. Renogram and isotope studies may indicate the area of ischemia in the kidney and can sometimes visualize the abnormalities in flow to that region.7,28 The definitive diagnosis is made by renal arteriogram. This, of course, will distinguish a fistula from arterial stenosis, where a bruit and hypertension are also typical. Significantly, in our patient and in othersz9 a reduced nephrogram was seen in the parenchyma distal to the fistula, supporting the proposed mechanism of ischemia distal to the shuntingofblood (Fig. lB, C, and D). As noted earlier the aggressive use of this technique, both in the management of trauma and in the evaluation of hypertensive and tumor patients, has caused greater recognition of A-V fistulas in recent years.
Modes
Traditionally, nephrectomy is the most common operation, and this is still the suggested method of treatment when the fistula is caused by tumor or congenital malformation.33 If the congenital lesion is small and well localized, partial nephrectomy is a reasonable approach. As with congenital A-V malformations in other areas of the body, attempts at simple branch ligation frequently fail to obliterate the fistula.33 Moreover, since most of these are intrarenal as much renal tissue may be destroyed by an attempted vascular correction as by a partial nephrectomy. Those patients who have the acquired type of A-V fistula generally warrant a renal-sparing procedure. Several authors have tried to ligate the feeding vessels to the intrarenal A-V fistula. Although these procedures usually have been successful, there have been several reported recurrences. 1,33 Experiments on peripheral fistulas indicate that recurrence is likely unless the distal artery and collateral vessels (which may be present in an intrarenal A-V malformationz5)
Management Once the diagnosis of arteriovenous fistula of the kidney has been made, the surgeon is faced with several therapeutic options. The first decision is whether operative or conservative management is indicated. Whatever decision is made, supportive medical therapy to control heart failure, hypertension, and anemia is often required. Approximately 70 per cent of patients who sustain A-V fistulas secondary to needle biopsy of
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are not also ligated. l4 Postoperative angiography often shows that as much tissue has been infarcted as when a partial nephrectomy is perforrned.‘~‘s,~~*~~In one series 2 of the 3 patients treated with branch ligation had persistence of their hypertension postoperatively.34 Many techniques which attempt to locate the specific feeding vessels intraoperatively have been utilized. They all involve the detection of a thrill (either by palpation or by auscultation with sterile stethoscope or Doppler and recognition of its cessation after ligating various arteries. 18,2335 These procedures, as reported, appear tedious and time-consuming, often because of the difficult intrarenal dissection required. We have found, as have others, that partial nephrectomy, particularly with an intrarenal lesion that involves one of the poles, offers a simpler procedure with a surer result and with probably no greater loss of kidney parenchyma than occurs with intrarenal branch artery ligation. 17*36 When the fistula lies extrarenally, particularly in the renal hilum, ligation of the individual vessels and excision of the aneurysmal sac is the best approach, although vascular reconstruction is sometimes required. 33,37This is not unlike the approach used for A-V fistulas in peripheral locations. With the advent of safer bench surgery in the future, less accessible lesions may be ligated individually or excised with a maximal preservation of renal tissue. Several radiologists have attempted embolization or occlusion of the fistula through angiographic techniques. 38-40The most frequently used method is embolization with either autologous clot or other foreign matter (fat, “Gelfoam,” or metallic pellets) injected into specific branch renal arteries visualized by selective renal angiograms.38B3gThis technique is used primarily in patients with postbiopsy fistulas where the arteriovenous connections are usually in small vessels. Since almost three quarters of post needle biopsy fistulas close spontaneously, perhaps many would have closed without such angiographic intervention. After embolization is performed the feeding vessels do not clot off because they have an intact intima which produces fibrinolysin. The fistulas do not have normal intima and, hence, thrombose.3g Invariably, a small area of infarction results, but fortunately there have been no cases of pulmonary emboli or other untoward events secondary to this procedure.38-40 In general, embolization is reserved for those patients who are considered poor surgical candidates.
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A more promising angiographic technique involves inserting a balloon catheter into the fistula and occluding the feeding vessels: a method that has been used with a great deal of success (as has the embolization technique) in various A-V malformations in both the central nervous system and peripheral vascular tree. 41The balloon catheter is a particularly attractive technique in large intrarenal fistulas which occur in the midportion of the kidney where a partial nephrectomy, or elaborate vascular surgery, destroys much renal tissue. Occlusion, as opposed to embolization, offers greater control of the specific vessels to be blocked;38 it also reduces the likelihood of potentially fatal pulmonary emboli. Preventive therapy in the management of A-V fistulas must also be considered. Little can be done to prevent acquired and congenital fistulas, but those which occur postnephrectomy can be avoided by ligating the renal pedicle vessels individually. Similarly, while prospective, retrospective, and experimental studies demonstrate that in at least 15 per cent of patients undergoing closed needle biopsy, fistulas will subsequently develop; 12~28~28 biopsies performed under fluoroscopic guidance with contrast material in the renal collecting system are associated with a lower incidence of complications, including subsequent hemorrhage and A-V fistula formations.42 Moreover, those patients who have severe hypertension or clotting abnormalities should be considered for open biopsy43 since there is an increased risk of these complications developing postbiopsy. In summary the diagnosis of A-V fistulas rests on a high index of clinical suspicion. An abdominal bruit, particularly when present with hypertension, hematuria, heart failure, or a history of trauma or renal surgery, should suggest the diagnosis of a renal arteriovenous fistula. Even if the intravenous urogram is normal, selective renal angiography should be considered. Stanford, California 94305 (DR. KESSLER) References O’BRIEN, D. P., PARROTT, T. S., WALTON, K. N., and LEWIS, E. L.: Renal arteriovenous fistulas, Surg. Gynecol. Obstet. 139: 739 (1974): MCALHANY, J. C., BLACK, H. C., HANBACK, L. D., and YARBROUGH, D. R.: Renal arteriovenous fistula as a cause ofhypertension, Am. J. Surg. 122: 117 (1971). DESAI, S. G., and DESAUTELS, R. E.: Congenital arteriovenous malfortiation of the kidney, J. Ural. 110: 17 (1973).
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4. MALDONADO,J. E., and SHEPS, S. G.: Renal arteriovenous fistula, Postgrad. Med. 40: 263 (1966). 5. KELLEY, D. G.: Renal arteriovenous fistula: a report of four cases and review of the literature, Br. J. Urol. 39: 162 (1967). 6. THOMASON, W. B., et al. : Intrarenal arteriovenous fistulas, J. Urol. 108: 526 (1972). 7. MALDONADO,J. E., et al. : Renal arteriovenous fistula: a reversible cause of hypertension and heart failure, Am. J. Med. 37: 499 (1964). 8. THOMAS, R. G., GRIEVE, S., and LJIWIN, B.: Spontaneous renal arteriovenous fistula and contralateral renal artery aneurysms, Br. J. Radiol. 35: 128 (1962). 9. BRON, K. M., and REDMAN, H. : Renal arteriovenous fistula and fibromuscular hyperplasia: a new association, Ann. Intern. Med. 68: 1039 (1968). 10. MILLOY, F., FELL, E. H., DILLON, R. F., and ZAYAS, A. M.: Intrarenal arteriovenous fistula with hypertensive cardiovascular disease, Am. J. Surg. 96: 3 (1958). 11. COSGROVE, M. D., MENDEZ, R., and MORROW, J. . Traumatic renal arteriovenous fistula: report of 12 zses J. Urol. 110: 627 (1973). 12. NELS)ON, B. D., BROSMAN, S. A., and GOODWIN, W. E.: Renal arteriovenous fistulas, ibid. 109: 779 (1973). 13. CHEW, Q. T., and MADAYAG, M. A.: Post-nephrectomy arteriovenous fistula, ibid. 109: 546 (1973). 14. HOLMAN, E., and TAYLOR, G.: Problems in the dynamics of blood flow. II. Pressure relations at the site of an arteriovenous fistula, Angiology 3: 415 (1952). 15. STOCKIGT, J. R., et al.: Renal vein renin in various forms of renal hypertension, Lancet 1: 1194 (1972). 16. JAHNKE, R. W., MESSING, E. M., and SPELLMAN, M. c.: Hypertension and post-traumatic renal arteriovenous fistula; documentation of unilateral renin secretion, J. Urol., in press. 17. RIBA, L. W., and SIMON, M. P.: Intrarenal arteriovenous fistula treated with partial nephrectomy, ibid. 98: 293 (1967). 18. WISE, H. A., WINTER, C. C., MOLNAR, W., and BUSH, C. A.: Management of renal arteriovenous fistula and carcinoma in the opposite kidney: an unusual combination, ibid. 112:433 (1974). Blood pressure and 19. EKELUND, L., and GOTHLIN, J.: intrarenal arteriovenous fistulae: an experimental study in rabbits, Stand. J. Urol. Nephrol. 7: 210 (1973). Effects on kidney and 20. LASHER, E. P., and GLENN, F.: blood pressure of artificial communication between renal artery and veins, Arch. Surg. 38: 886 (1939). 21. SECREST, A. J.: Experimental renal arteriovenous fistula, J. Urol. 102: 552 (1969). 22. SECHAS, M. N., PLESSAS, S. N., and SKALKEAS,G. D.: Post-traumatic renovascular hypertension, Surgery 76: 666 (1974). 23. GIBBONS, R. P., CORREA, R. J., and TREMANN, J. R.: Management of intrarenal vascular malformations, Urology 1: 136 (1973). 24. BOIJSEN, E., and KOHLER, R.: Renal arteriovenous fistulae, Acta Radiol. 57: 433 (1962). 25. KINKHABWALA, M., DZIADIW, R., and PATIL, U.:
Intrarenal arterial< collaterals simulating malignant tumor in traumatic arteriovenous fistula, Urology 4: 715 (1974). 26. MARK, L. K. : Arteriovenous malformations of kidney, ibid. 4: 706 (1974). 27. CLOUSE, M. E., and ADAMS, D. E.: Congenital renal arteriovenous malformation: angiography in its diagnosis, ibid. 5: 282 (1975). 28. EKELUND, L., et al. : Arteriovenous fistulas following renal biopsy with hypertension and hemodynamic changes: report of a case studied by dye-dilution technique, J. Urol. 108: 373 (1972). 29. LANG, E. K., et al. : Renal angiography in the assessment of renal trauma, Radiology 98: 103 (1971). 30. Rous, S. N.: The value of serial selective renal angiography in the delayed management of renal trauma, J. Urol. 107: 345 (1972). 31. SANOUDUS,G. M., BERENBAUM, E., and CLAUSS, R. H.: Ruptured renal arteriovenous fistula, J.A.M.A. 219: 1581(1972). 32. JANTET, G. H., FOOT, E. C., ~~~KENYON, J. R.: Rupture of an intrarenal arteriovenous fistula secondary to carcinoma: a case report, Br. J. Surg. 49: 404 (1962). 33. TYNES, W. V., DEVINE, C. J., DEVINE, P. C., and POUTASSE, E. F. : Surgical treatment of renal arteriovenous fistulas: report of5 cases, J. Urol. 103: 692 (1970). 34. COSGROVE, M. D., MENDY, R., and MORROW, J. W.: Branch artery ligation for renal arteriovenous fistula, ibid. 110: 632 (1973). 35. PALMER, J. M., and CONNOLLY, J. E.: Intrarenal arteriovenous fistula: surgical excision under selective renal hypothermia with kidney survival, ibid. 96: 599 (1966). 36. SCHWEITZER, F. A.: Conservative surgery for renal arteriovenous aneurysms, Guy Hosp. Rep. 121: 205 (1972). 37. MERKEL, F. K., and SAKO, Y.: Surgical treatment for traumatic renal arteriovenous fistulas, Arch. Surg. 101: 438 (1970). 38. RIZK, G. K., ATALLAH, N. K., and BRIDI, G. I.: Renal arteriovenous fistula treated by catheter embolization, Br. J. Radiol. 46: 222 (1973). 39. SILBER, S. J.. and CLARK, R. E.: Treatment of massive hemorrhage after renal biopsy with angiographic injection of clot, N. Engl. J. Med. 292: 1387 (1975). 40. BOOKSTEIN, J. J., and GOLDSTEIN, H. M.: Successful management of post biopsy arteriovenous fistula with selective arterial embolization, Radiology 109: 535 (1973). 41. BENTSON, J. R., and CRANDALL, P. H.: Use of the Fogarty catheter in arteriovenous malformations of the spinal cord, ibid. 105: 65 (1972). 42. MCCANSE, L. R., CROSSE, D., WHITTIER, F., and MEBUST, W. K.: Percutaneous renal biopsy with localization by retrograde pyelogram, Proc. Kimbrough Urological Sem. 8: 94 (1974). 43. PATIL, J., BAILEY, G. L., and MAHONEY, E. F.: Open-renal biopsy in uremic patient, Urology 3: 293 (1974).
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