Clinical Studies

Renal Arteriovenous Fistula*A Reversible Cause of Hypertension and Heart Failure

JORGE E. MALDONADO, M .D ., SHELDON G. SHEPS, M .D ., PHILIP E . BERNATZ, M .D .,

JAMES H. DEWEERD, M.D . and EDGAR G. HARRISON, JR., M.D .

Rochester, Minnesota

RTERIOVENOUS fistulas of the renal vascula-A ture have been reported with increasedfrequency during the past decade . These fistulasare unique in that the major manifestations arediastolic hypertension and high-output cardiacfailure, both of which may be reversed byobliteration of the arteriovenous connection .Increasing attention to renal causes of hyper-tension and routine auscultation to detect intra-abdominal bruits have contributed to the morefrequent detection of this abnormality since aloud, continuous bruit, audible over the renalregions, commonly occurs . Primary malignantneoplasia of the kidney also may present with asimilar picture .

Alterations in circulatory hemodynamics andin renal function were studied in two patientswith renal arteriovenous fistulas : one with anidiopathic fistula of the major renal vessels, andone with a fistula within a hypernephroma. Inaddition, we have reviewed fifty-three casespreviously reported and present a classificationbased on the clinical-pathologic correlationsnoted .

CASE REPORTS

CASE I . A thirty-four year old woman was firstseen in May 1962 because of hypertension . This hadbeen present since her fourth pregnancy, in 1957, andthe blood pressure had increased progressively .Headaches, congestive heart failure and palpitationsdeveloped and became prominent . Multiple anti-hypertensive medications had been administeredpreviously without successful control of the bloodpressure . The fifth (and last) pregnancy, in 1959, hadbeen complicated by severe postpartum hemorrhageand shock. Vigorous massage of the abdomen hadbeen carried out for an entire day at that time .

The first three pregnancies had been withoutincident. There was no family history of hypertensionor renal disease . Three episodes of rheumatic feverhad occurred during childhood but a heart murmur(due to mitral valvular disease) was first made knownto the patient in 1952 .

Blood pressure in the right arm was 240 mm. Hgsystolic and 130 mm . Hg diastolic ; it was 220/120mm. Hg in the left arm and 280/130 mm. Hg in theright thigh. The pulse was 90 and regular . Jugularvenous pressure was increased slightly . Arterialpulsations in the neck and abdomen were bounding .The heart was overactive, with left ventricular thrust,and there was a systolic regurgitant murmur ofmoderate intensity over the apex and tricuspidregion. In addition, there was an ejection typesystolic murmur of moderate intensity over the pulmo-nary region. The second sound in the pulmonic areawas moderately increased in intensity . There was afaint diastolic murmur over the right parasternal area .The liver was slightly enlarged and the right kidneywas moderately enlarged, presenting as an ovoidmass. There was an easily palpable thrill over thismass, and a very loud, high-pitched bruit was audibleover the entire abdomen, but best heard over theright kidney; this was continuous in nature, withsystolic accentuation . (Fig . 1 .) Examination of theoptic fundus revealed marked generalized and focalnarrowing of the arterioles and moderate hyper-tensive sclerosis . An electrocardiogram revealed asinus rhythm of 100, left axis deviation, and leftventricular hypertrophy .

Results of the following studies were within normallimits: hematocrit, hemoglobin, erythrocyte count,leukocyte total and differential counts, erythrocytesedimentation rate, fasting blood sugar, blood urea,serum potassium, serologic test for syphilis andurinary catecholamines .

Roentgenographic studies of the heart demonstratedmarked generalized enlargement with prominenceof the left ventricle . (Fig. 2A.) No valvular calcifica-

* From the Sections of Medicine, Surgery, Urology and Surgical Pathology, Mayo Clinic and Mayo Foundation,Rochester, Minnesota. Manuscript received November 14, 1963 .

VOL . 37, OCTOBER 1964

499

500

Renal Arteriovenous Fistula-Maldonado et al .

CAROTID ARTERY PULSE

RIGHT UPPER QUADRANTI ~ f ~, j

50 C . /SECOND BAND

"

11 '

RIGHT UPPER QUADRANT'200 C . /SECOND BAND,

PAPER SPEED 100 MM ./SECOND

Fin. 1 . Case I . Phonocardiogram of patient with renal arteriovenous fistula, illustrating the continuous bruitwith accentuation during cardiac systole .

tion was identified on fluoroscopic examination . Anexcretory urogram revealed a large right kidney withsome deformity of the pelvis and calyces . The leftkidney appeared to be normal in size and in excretoryfunction. A percutaneous transfemoral retrogradeaorticorenal arteriogram was made . (Fig. 3A.) Theleft renal artery, its primary and intrarenal branches,and the renal silhouette were normal. The right renalartery was the site of an aneurysm extending from itsorigin to the trifurcation and involving a short portionof the primary branches. The branch of the rightmain renal artery supplying the superior pole segmentoriginated more proximally than usual and the initialportion appeared abnormal . The arrow in the figurepoints to a jet of contrast medium which passed from

FIC . 2 . Case I. Thoracic roentgenograms. A, preoperatively, showing marked cardiomegaly. B, postoperatively, showingreduction in heart size. Patchy pneumonitis in both lungs.

the region of the trifurcation of the right renal arteryinto a large lobulated saccular cavity. The branchesof the renal artery were seen to extend around andbeyond this cavity. An accessory artery arose sepa-rately from the aorta distally and supplied the lowerportion of the right kidney.

A standard radioisotope renogram [1] (Fig. 3B)showed an abnormality which was bilateral but moremarked on the right. The delayed concentration andexcretion of the radioiodinated medium on the rightwas highly suggestive of a renovascular lesion [2] .Renal function studies were carried out utilizingpreviously described technics [3] . The mean data offour consecutive study periods are given in Table I.The reduction in mean volume flow and mean con-

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Renal Arteriovenous Fistula-Maldonado et al .

1 .2

1 .1 -

1 .0-

0.9-

0.8-

0 .7 -

0 .6 -

0 .5 -

centration of sodium on the right are strongly sug-gestive of predominantly right-sided ischemia [3,4] .This is further supported by the greater concentrationsof inulin and para-aminohippurate on the right . Theincreased tubular reabsorption of filtered water andsodium on the right is also indicative of predominantlyright-sided impairment of renal blood flow, althoughthe disparity is not great . The osmolality was a littlegreater from the left kidney . Effective renal plasmaflow was reduced on the left as well as on the right,as compared to normal. These data were consistentwith bilateral impairment of renal function, muchgreater on the right, and are indicative of ischemiaon the right .

Indicator-dilution studies were performed in themanner described by Fox and Wood [5] . The recircu-lation time on a central indicator-dilution curve was16 seconds . The shape of the curve was within normallimits; there was no evidence of shunt. The cardiacindex, as determined by standard methods, was 5 .4 L .per minute per M2 .

The right kidney was explored through a rightparamedian transperitoneal incision. Exploration ofthe abdominal cavity gave negative results. A largecystic mass was present just medial to the right kidney,which was displaced laterally and superiorly . Thevena cava was at least 6 cm . in diameter but was notpulsating and no thrill was palpable over it . The renalartery was 12 to 15 mm . in diameter throughout itslength, with no evidence of obstruction. The smallinferior accessory artery was located and both renalarteries were divided at their origin. There was asingle renal vein of very short length which enteredthe inferior vena cava posteriorly. Following divisionof this vein, the vena cava immediately became

VOL . 37, OCTOBER 1964

10

Renal Function

Urinary volume (ml ./min.) . . . .Urinary osmolality (mOsm ./L.)Urinary concentrationInulin (mg./ml .)PAH (mg ./ml.)Sodium (mEq ./L .)

Clearances (ml ./min ./1 .73 Mt,)InulinPAH

Reabsorptions,t per centWaterSodium

Minutes

RightKid-ney

0 .65408 .0

19 .95 .3

92 .0

41 .0109 .0

98 .499 .0

I20

FIG . 3 . Case I . A, aorticorenal arteriogram illustrating the arteriovenous connection (arrow), bilobular sac, dilatedmain right renal artery, and the apparently normal accessory right renal artery . B, radioisotope renogram illustratingthe delayed concentration and excretion of the radioiodinated medium on the right .

TABLE I

RENAL FUNCTION BEFORE AND FIVE MONTHS AFTERRIGHT NEPHRECTOMY IN CASE I

Preoperative

LeftKid-ney

1 .36430 .0

14 .24 .1

111 .0

68 .0193 .0

98 .098 .4

Right kidney

Left kidney

Percent

Differ-ence*

-52-5

+40+29-17

-40-44

+0.4+0 .6

RightKid-ney

00

501

I30

Post-operative

LeftKid-ney

94358

*The per cent difference is derived from the formula 100 X

R - L)for each value.

Lt The proportions of filtered water and sodium are derived from the

formulas 100 - 100 X V and 100 - 100 XC!9

respectively, whereCIp

CmCp, is the clearance of sodium, Cto, the clearance of inulin, and V, theurinary volume per minute,

smaller in diameter . The aneurysm and kidney wereremoved without incident .

Postoperatively, the blood pressure remainednormal until the fourth postoperative day when itincreased to 190/100 mm. Hg. The hypertensionpersisted and antihypertensive therapy was instituted ;the final program consisted of bendroflumethiazide,

502 Renal Arteriovenous Fistula-Maldonado et al .

FIG . 4 . Case i . Gross appearance of right kidney. A,anterior view of injected specimen which is opened toshow plastic cast of the thin-walled, bilobular arterio-venous sac. The venous portion of the aneurysm is to theleft and the arterial portion is to the right of the probewhich passes through the arteriovenous fistula. Notedepressed zone of infarction. B, injection materialremoved to display the thin-walled aneurysm and theopening of the fistula on the venous side (arrow) . C,opened renal artery showing moderate dilation and ostiumof the fistula at the primary arterial bifurcation (arrow) .

A.Fic . 5 . Case I. Histologic appearance. A, the wall of therenal artery (right) sectioned at the fistula . Note loss ofinternal elastic membrane and much of the media atjuncture with the aneurysm (left) . Elastic van Giesenstain, original magnification X 40 . B, extreme thinningof the wall of the aneurysm, which here is composed ofadventitia and only a few remnants of smooth muscle .Elastic van Giesen stain, original magnification X 40 .C, incomplete infarction of renal parenchyma showingextensive atrophy of tubules. Hematoxylin and eosinstain, original magnification X 130 .

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5035 mg. twice daily, and hydralazine, 50 mg . four timesdaily. Viral pneumonitis also occurred during thepostoperative course. At dismissal, the heart wasmuch reduced in size (Fig . 2B) and the cardiacmurmurs were less intense . There was no evidenceof congestive heart failure . The blood pressureaveraged 140/100 mm . Hg just prior to dismissal.

The patient was seen again six months later . Thedaily blood pressure (determined by the patient) hadaveraged 150/105 mm. Hg in the sitting position. Shehad continued on the therapeutic program initiatedpostoperatively and had felt very well, with no limita-tion of activities . The optic fundus showed decidedlyless focal and generalized arteriolar narrowing andsclerosis . The heart was still slightly enlarged butmuch less so than previously . A soft precordial systolicmurmur was heard but no other murmurs wereaudible in the chest or abdomen . The thoracicroentgenogram confirmed the reduction in heartsize although there was still some prominence of theleft ventricle . The electrocardiogram also confirmedthe marked reduction in degree of left ventricularhypertrophy .The hemodynamic studies were repeated . The

blood pressure in the radial artery was 148/85 mm .Hg. Normal time components were observed on acentral indicator-dilution curve . The recirculationtime was 18 seconds, and no evidence of a shunt wasseen . The cardiac index was 4 .6 L. per minute perM2 .

The function of the left kidney was evaluated bymeans of bladder clearance ; the mean glomerularfiltration rate was 94 ml . and the mean effectiverenal plasma flow was 358 ml . per minute per 1 .73M2, (the average of two periods) . (Table L.) Thisincrease in function of the solitary left kidney wasindicative of compensatory hypertrophy . The resultsof urinalysis and the concentrations of blood hemo-globin and serum sodium and potassium were normal .Bendroflumethiazide therapy was increased to 15 mg .daily and hydralazine dosage was continued at 200mg. daily .

Pathologic Studies. The resected kidney weighed200 gm. A large depressed zone of incomplete corticalinfarction was present on the anterior surface . Therewas slight hydronephrosis, apparently due to extrinsicureteropelvic compression . The thin-walled, bilobulararteriovenous aneurysm projected from the hilus andmeasured 10 by 5 by 3.5 cm. To demonstrate thefistula and aneurysm, the renal artery was cannulatedand then injected with silicone rubber . * This wasfollowed by overnight fixation in formalin . Both thearterial portion of the aneurysm, which measured 5 .5cm. in maximal dimension, and the venous portion,which measured 4.5 cm., were filled with the injectedmaterial. (Fig. 4A.) The venous portion of the sacinvolved both the primary vein and its hilar branches ;the arterial branches distal to the fistula were not

* Silastic (R.T.V . No. 2), Dow Corning Company,Midland, Michigan .

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dilated . On opening the renal artery the lumen wasnoted to be somewhat dilated and measured 0 .8 cm.in diameter . The ostium of the arteriovenous fistulawas found at the primary bifurcation of the artery,involving the branch to the upper pole and enteringthe major renal vein . (Fig . 4B and 4C .) Neither grossatheroma nor mural thrombus formation was noted .No communication could be demonstrated betweenthe aneurysm and the accessory renal artery whichmeasured 0.3 cm. in diameter and was patentthroughout .

Histologic examination of the main renal arteryrevealed marked patchy fragmentation of the internalelastic membrane, a decrease in elastic fibers in themedia, and an increase in loose fibrous tissue in alllayers. These changes were less pronounced in theaccessory artery . Sections taken at the orifice betweenthe primary branching of the renal artery and theaneurysm showed an interruption of the internalelastic membrane and a marked decrease, progressingto almost complete absence, of smooth muscle of themedia. (Fig. 5A.) Only remnants of smooth musclefibers could be found in either the venous or thearterial portion of the aneurysm, and, in large areas,only the fibrous tissue of the adventitia remained .(Fig . 5B.) There was no evidence of vasculitis andonly a few small intimal atheromas were seen in therenal artery and in the aneurysm .

Sections of renal parenchyma showed an area ofincomplete infarction bordered by zones of essentiallynormal appearance. In sections* taken from theinfarcted region, the glomeruli were essentially intactbut there was extensive atrophy of tubules . (Fig. 5C .)The tubular atrophy particularly involved the proxi-mal convoluted tubules which had a more cuboidalepithelium with clear cytoplasm. Minimal lympho-cytic infiltration was seen in the area of the atrophictubules . Parenchymal arteries and veins were notunusual .

This case documents for the first time in man,renal ischemia distal to a renal arteriovenousfistula . Radioisotope renography and renalfunction studies gave results which were stronglysuggestive of ischemia of the renal parenchyma ;this was confirmed by the pathologic findings ofincomplete infarction in the absence of arterialstenosis or thromboembolism . The high cardiacoutput, congestive heart failure and cardio-megaly were relieved by nephrectomy andaneurysmectomy but diastolic hypertension,although much ameliorated, persisted. As hasbeen demonstrated by Thal and associates [6],

* Dr. Sheldon Sommers kindly performed juxta-glomerular cell counts on sections of the kidney . Inatrophic zones, the cell counts of 25 bodies totaled 247(high), while in nonatrophic zones it totaled 155 (low) .He interpreted these findings as consistent with hyper-tension of the Goldblatt type arising from partialatrophy of the kidney .

504 Renal Arteriovenous Fistula-Maldonado et al .

FIG. 6 . Case n. Thoracic roentgenograms. A, two years prior to fistula operation showing normal cardiac silhouette(heart 13 .5 cm . in diameter) . B, one year later the cardiac silhouette had increased to 15 .5 cm . in diameter.

this may have been due to the long-standingsevere hypertension which had produced somenephrosclerosis in the contralateral kidney .

Certain features of this relatively large, soli-tary, arteriovenous communication suggest thatit began as a renal arterial aneurysm whichbecame adherent and then ruptured into therenal vein. Almost complete loss of elastic tissueand of much of the smooth muscle of the mediawas seen at the ostium of the fistula . These find-ings, and the location of the fistula near thebifurcation of the artery, would be in keepingwith an antecedent aneurysm .

Of interest was the finding of fragmentationof the internal elastic membrane and of someof the elastic fibers in the walls of the main andaccessory arteries . Although this was somewhatreminiscent of renal arteries with fibromusculardysplasia, there were no multiple mural aneu-rysms, no other focal defects in the media and nostenosing fibromuscular segments which arecommonly seen in fibromuscular dysplasia [7] .Perhaps a localized basic defect or degenerationof elastic tissue of the arterial wall underlies theproduction of the vascular abnormalities in bothconditions. In addition, some of these elastictissue changes may be partially due to the hemo-dynamic stresses of the fistula since they werenoted to a lesser degree in our second case .

CASE It . The patient, a sixty-seven year oldwoman, was first seen in 1960 . Left radical mastec-tomy had been performed for grade 4 adenocarci-noma. The axillary lymph nodes were not involvedand local roentgen therapy had been administered.At that time the blood pressure was 120/75 mm . Hg

and the thoracic roentgenogram appeared normal(heart, 13 .5 cm. in transverse diameter) . (Fig. 6A .)She had returned about one year later because ofsome distress in the region of the left twelfth rib . Theblood pressure then was 135/70 mm. Hg and athoracic roentgenogram revealed cardiac enlarge-ment (15 .5 cm.) . (Fig . 6B .)

The next visit, in July 1962, was occasioned bypersistence of the distress on the left side . The bloodpressure was 140/70 mm . Hg and pulse was 92 andregular. A thrill was palpable in the left upperquadrant and a continuous bruit with systolicaccentuation was audible in the same region (similarto that heard in Case I) over a pulsating mass that wasabout 8 cm . in diameter. A 2 mm. nodule was notedin the mastectomy scar. The results of the remainderof the examination were noncontributory. A thoracicroentgenogram did not reveal any increase in thecardiac enlargement (15 .5 cm.) . An electrocardio-gram indicated left ventricular hypertrophy andincomplete right bundle branch block . The erythro-cyte sedimentation rate was 45 mm. in 1 hour(Westergren) . Excisional biopsy of the skin nodulerevealed scirrhous adenocarcinoma . Results of thefollowing studies were within normal limits : erythro-cyte count, hemoglobin, leukocyte total and differen-tial counts, cervical smear, protein-bound iodine,alkaline phosphatase and urinalysis .

A roentgenogram of the abdomen revealed mottledcalcification in an apparently enlarged lower poleof the left kidney. On excretory urography, themedium was in normal concentration on the left butthe lower calyx and lower border of the pelvis weremarkedly deformed . There was an irregular collectionof medium over the lower pole of that kidney.Visualization on the right was normal . On a per-cutaneous transfemoral retrograde aorticorenal ar-teriogram (Fig. 7) the right renal artery and kidneyappeared to be normal. The left renal artery was

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Renal Arteriovenous Fistula-Maldonado et al .

FIG . 7 . Case n. Aorticorenal arteriograms . A, early phase showing the diffuse enlargement of the left renal artery and alarge neoplasm in the lower pole of the left kidney . B, later phase showing the large cavernous vascular lakes and hugerenal vein . C, late phase showing the greatly dilated left ovarian vein and left renal vein .

Fin . 8 . Case ii. Gross appearance of injected kidney. A, the midportion of the kidney is infiltrated by a grade 2 adeno-carcinoma (hypernephroma) . Vein is cannulated by the upper of the two glass tubes and the artery by the lower . B,large vascular spaces within the tumor are filled by injected material . C, hypernephroma grossly invades the openedrenal vein.

diffusely enlarged . There was a large, highly vas-cularized neoplasm in the lower pole of the leftkidney with rapid return of medium into a huge renalvein. The left ovarian vein was greatly dilated andcontrast medium passed through the left ovarianplexus across the uterine plexus to the right ovarianplexus and then superiorly to the right ovarian veininto the proximal inferior vena cava . In addition,contrast medium returned to the inferior vena cavathrough the greatly dilated left renal vein .

Central indicator-dilution curves were obtained .There was a recirculation time of 13 seconds . Therecirculation curve revealed an early hump suggestiveof early recirculating indicator dye [5] . The cardiacindex was 5.4 L. per minute per M 2 .The left kidney was explored through a primary

VOL . 37, OCTOBER 1964

505

incision in the left flank . The renal vein was greatlydilated and appeared pinker than usual . There wasno evidence of venous obstruction. The left renalartery also was dilated and was approximately 8 mm .in diameter. When this was occluded the thrill whichhad been palpable along the lower pole of the kidneydisappeared and the renal vein collapsed somewhatand regained its usual blue color . The left ovarianvein was approximately 1 .5 cm . in diameter . It wasdissected free and interrupted . The main renal veinwas approximately 3 cm. in diameter and it also wasdissected free and occluded proximally to its juncturewith the ovarian vein . The kidney was then removed .Abdominal exploration was carried out and there wasno evidence of disease or metastasis .

The postoperative course was uneventful and the

506 Renal Arteriovenous Fistula-Maldonado et al .

patient remained normotensive . Roentgen therapywas administered to the left side of the chest in theregion from which the metastatic skin lesion (fromthe cancer of the breast) had been removed pre-viously. Ten days postoperatively, hemodynamicstudies revealed a cardiac index of 2 .9 L . per minuteper M 2. The contour of a central indicator-dilutioncurve was normal and the recirculation time was18.6 seconds .

Three months later, in October 1962, the patientreturned because of recurrence of cancer in the skinon the left side of the chest . In addition, a mass wasnow present in the upper outer quadrant of the rightbreast . A thoracic roentgenogram revealed onemetastatic nodule in the right lung above the dia-phragm and one in the left lung near the apex. Therewas fluid above the left diaphragm obscuring thecardiac border . Palliation was begun with estrogentherapy .

Pathologic Studies . The midportion of the leftkidney was replaced by a grade 2 adenocarcinoma ofclear cell type (hypernephroma), 7 by 6 by 6 cm .It did not perforate the capsule but the major veinwas invaded in the hilus . There was no gross externalarteriovenous aneurysm, although the renal vein wasmarkedly dilated and the renal artery was moderatelydilated . By probing through the lumen of the arteryand the vein, a fistula could be detected in the sub-stance of the tumor .

The artery and the vein were cannulated andsilicone rubber was injected into the major arteryand vein to demonstrate their connections . (Fig . 8A .)The specimen was fixed in 10 per cent formalinovernight and these vessels were then opened longi-

FIG . 9. Case II . Histologic appearance . A, section of renal vein with lumen almostcompletely filled by invading hypernephroma . Hematoxylin and eosin stain,original magnification X 90 . B, section of medium-sized artery (traversingfrom top) which has been invaded and communicates with vascular spaceswithin the tumor . Elastic van Giesen stain, original magnification X 30 .

tudinally . Branches of both of these vessels connectedwith cavernous vascular pools which were filled withthe injected plastic and were located within thepartially necrotic tumor, indicating multiple arterio-venous connections. (Fig . 8B.) Large parenchymalbranches of the artery and vein extended into otherhemorrhagic zones of the tumor and a gross extensionof tumor, 1 .0 cm. in length, partially occluded therenal vein . (Fig . 8C .)

Microscopically, alveolar clusters and columns oflarge polygonal cells with clear cytoplasm replacedrenal parenchyma and invaded the renal vein . (Fig .9A.) These cells had vesicular nuclei with largenucleoli and occasional mitotic figures . The tumorwas richly supplied by capillaries and small veinsthroughout . Sections of large vascular lakes showedpartial linings of tumor cells and communicationswith invaded and fragmented medium-sized arteriesand veins. (Fig. 9B.) Sections of the renal arteryshowed slight focal fragmentation of the internalelastic membrane and some loss of elastic fibersof the media .

Aorticorenal arteriography demonstrated thearteriovenous connections as large vascularpools within the hypernephroma, and theextreme dilation of veins proximal to the shunt .This dilation was due to the great increase inblood flow alone, as no obstruction to venousreturn was found at exploration . Due considera-tion was given to the presence of metastaticbreast cancer, but nephrectomy was thoughtto be indicated because of the cardiomegaly,

AMERICAN JOURNAL OF MEDICINE

TABLE IIETIOLOGIC CLASSIFICATION IN THIRTY-FIVE CASES OFRENAL ARTERIOVENOUS FISTULA ASSOCIATED WITH

FUNCTIONING KIDNEY

* Includes Case ii of present report .t Includes Case I of present report.

increased cardiac output and presence of painin the flank .The propensity of renal adenocarcinoma

(hypernephroma) to invade the renal vein waswell demonstrated in this case, as in many of thesimilar cases in the literature . This feature, inaddition to compression and infiltration ofvessels by tumor and resultant hemorrhagicnecrosis, probably brought about the arterio-venous fistulas. Vascular invasion, necrosis andhemorrhage are not infrequent features ofhypernephroma as well as of many othermalignant tumors and it is surprising thatarteriovenous fistulas are not more common .

REVIEW OF THE LITERATURE

From 1928, when Varela [8] reported the firstcase, until 1963, fifty-three cases of renalarteriovenous fistula have been recorded . Fis-tulas occurring between the main renal arteryand vein after nephrectomy have differentclinical manifestations than do fistulas in asso-ciation with an intact kidney and therefore willbe considered separately . The two cases reportedin this paper are included in the review .

Renal Arteriovenous Fistula in Association with a

Functioning Kidney . Thirty-nine recorded caseswere reviewed, but in six insufficient informationwas given [9-14] . With the addition of the twopatients reported herein, thirty-five cases wereavailable for detailed analysis . (Tables ii andVOL . 37, OCTOBER 1964

Renal Arteriovenous Fistula-Maldonado et al .

507

III .) * In all instances the diagnosis was con-firmed by pathologic study . The cases in thisgroup were subdivided, according to etiology,into three groups : congenital, acquired andidiopathic . (Table II .)

Etiology : Cases considered congenital werethose in which there was an angiomatous orcirsoid appearance of the renal vessels, withmultiple arteriovenous connections .

The causes of acquired fistula include hyper-nephroma, trauma, inflammation and athero-sclerosis. The diagnosis of hypernephroma wasmade by histologic examination in six cases .

In eleven patients trauma was considered toplay a significant role in the formation of thefistula. Bullet wounds had been incurred infour, percutaneous renal biopsy and pyelo-lithotomy had been performed in two each, andthe following injuries occurred in one each :knife wound, glass wound and run over by awagon wheel. The injury took place three weeksto twenty-six years before the diagnosis wasmade. All these fistulas were single .

Inflammatory changes were noted about thefistula in three patients . One of these was asso-ciated with subacute bacterial endocarditis[31] . In the remainder, granulomatous lesionswere present about the vessels, but the systemicnature of the process was not clear [30,32] .

In four patients calcification was noted in thewall of the fistulous aneurysm . In one of these[33] the extent of this calcification justifiedinclusion under the acquired group as being

* Two cases have been reported twice [30 and 41, and24 and 42] .

TABLE IIICLINICAL MANIFESTATIONS OF RENAL ARTERIOVENOUS

FISTULA ASSOCIATED WITH FUNCTIONING KIDNEYIN THIRTY-FIVE PATIENTS

Manifestation No. Per cent

Intra-abdominal bruit 24 69Cardiomegaly 20 57Congestive heart failure 17 49Tachycardia 13 37Diastolic hypertension 15 43Systolic cardiac murmur 11 31Hematuria 12 34Pain 12 34Intra-abdominal mass 5 14Headache 4 11Azotemia 3 9

Cases

Classification

No . Per cent

References

Congenital 5 14 15-18

AcquiredHypernephroma * 6 17 19-23Trauma 11 31 18, 22, 24-29

Inflammation 3 9 30-32Atherosclerosis 1 3 33

Idiopathic t 9 26 8, 34-40

508 Renal Arteriovenous Fistula-Maldonado et al.atherosclerotic in origin. The remainder wereclassified as idiopathic [34-36] . The exactetiology of the fistula could not be determinedin another six patients who comprised theremainder of the idiopathic group .

Clinical features: The mean age of this groupwas thirty-nine years (range, three to sixty-nineyears) . Two thirds of the patients with hyper-nephroma were fifty-five years old or older .Twenty-one (60 per cent) patients were femaleand fourteen (40 per cent) male . It is of interestthat five of the six patients with hypernephromawere female, in contrast with the usual malepreponderance of this tumor (2 :1) .

The chief clinical manifestations in this groupincluded intra-abdominal bruit, congestive heartfailure, diastolic hypertension and hematuria .(Table III .) One, or a combination, of thesefindings was noted in nearly all cases . The moststriking finding was the presence of a loudbruit, characteristically high-pitched and con-tinuous but with systolic accentuation, locatedover the renal region . In most instances a thrillwas palpable as well . Cardiomegaly was notedfrequently and was confirmed by electrocar-diography. Although tachycardia and hyper-tension were noted frequently, in only twoinstances was there a comment about increasedpulse pressure . There was no relationshipbetween the age of the patient and the presenceof congestive heart failure . Diastolic hyperten-sion (diastolic pressure greater than 90 mm . Hg)was recorded in fifteen instances . The durationof the hypertension was from six months to sixyears, as recorded in eight cases . Hematuria intwo cases (one with hemophilia) and azotemiain one case were associated with the hypertension .

It is of interest that gross hematuria wasreported in eleven cases and microhematuria inone. In contrast to what might be expected, inonly two patients with hypernephroma [19] andin only one of the patients who had been subjectto trauma [29] (nephrolithotomy in both) washematuria noted. In two of the five congenitalcases, gross hematuria was painless [16,17] andin two was associated with ipsilateral flank pain[Cases 1 and 2 in 18] . One patient in the inflamma-tory group was noted to have gross hematuria,and, on aortography, contrast medium wasdetected entering the renal pelvis from the majorvessels [32] . Gross, painless hematuria was notedin three patients in the idiopathic group[34,37,40] and microhematuria was found in theone patient in the atherosclerotic group [33] .

A mass was palpable in four patients withhypernephroma and in one idiopathic case .Pain was located in the upper part of theabdomen or in the costovertebral angle . It wasgenerally of a chronic nature but renal colic waspresent in two patients . Mild azotemia in threecases was the only abnormality found in theusual hematologic studies .

Roentgenographic studies : Excretory urographyor retrograde pyelography was carried out intwenty-nine patients. In four of these in whomhypernephroma was present, a highly suggestiveabnormality was noted ; in twenty-three, somenonspecific ipsilateral dysfunction was apparent .The remaining two patients were reported tohave a normal result on the ipsilateral side .

Aorticorenal arteriography was performed intwenty-three cases and was diagnostic or highlysuggestive of a renal arteriovenous fistula in allinstances. Reduced accumulation of contrastmedium in the portion of the kidney occupiedby the fistula and local contraction of the renalparenchyma have been interpreted to indicateischemia distal to the shunt [18,37] .

Hemodynamic studies: Four of the five patientsexamined at the Mayo Clinic (Cases 1 and 2 ofScheifley and co-workers [22] and the two casesdescribed in this paper) have had indicator-dilution studies . One was normal and the othersrevealed a rapid recirculation time, indicativeof an arteriovenous shunt . Catheterization of theipsilateral renal vein was accomplished in onecase and studies indicated that 69 per cent of theinferior vena cava blood was from the shunt(Case 2 of Scheifley and co-workers) . All fourpatients had increased cardiac output at rest .

Milloy and associates [28] described a patientwith hypertension, congestive heart failure andincreased cardiac output . The ipsilateral renalvessels were catheterized and a shunt of 29 .5 percent of the cardiac output was calculated . In acase studied by Myhre [19] the cardiac outputwas increased, the pressure was normal in theipsilateral renal vein and inferior vena cava, andthe oxygen saturation of the blood in the rightrenal vein was slightly increased (90, 94 and 94per cent on three determinations) . Jouve andassociates [31] reported increased pressure in thepulmonary capillaries, pulmonary artery, rightventricle and right atrium in a case with asso-ciated subacute bacterial endocarditis and con-gestive heart failure. However, the oxygencontent of the blood entering the right atriumwas not indicative of a large shunt caudad to the

AMERICAN JOURNAL OF MEDICINE

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heart . The studies gave normal results fourmonths following nephrectomy. The explanationfor the initial high pressures is not clear .

Renal function studies : Radioisotope renographywas reported by Winter and co-workers [25] tobe normal in one case. In Case i of this paperrenography revealed abnormal function of theipsilateral kidney of a type which we havefrequently observed in patients with renalischemia [2] . Slominski-Laws and co-workers[75] reported reduced urinary concentrationsof sodium and potassium and delayed excretionof phenolsulfonphthalein on the side of a con-genital fistula . Myhre [79] recorded a glomer-ular filtration rate of 79 ml . per minute per1 .73 M2 . and an effective renal plasma flow of363 ml. per minute per 1 .73 M 2 . in anothercase. Renal clearance studies have not beenreported previously ; the changes noted in ourCase i indicated significant ipsilateral functionalimpairment due to ischemia .

Surgical treatment: All but one of the thirty-fivepatients underwent surgical treatment . Nephrec-tomy was performed in thirty and partialnephrectomy in three . In one instance onlyligation of the arterial supply was performed[Case 4 in 18] . The remaining case was diagnosedat necropsy [8] .

Pathologic studies : The fistulas were unilateralin each instance, on the right side in twenty-fourcases and on the left in eleven . The fistula wassingle in thirty cases, seventeen of which wereextrarenal, twelve intrarenal, and one was bothintrarenal and extrarenal in location . In fourinstances multiple fistulas were found : threeintrarenal and one extrarenal . In the remainingcase of the entire group of thirty-five, it was notpossible to determine the location of the fistula .The arterial supply to the aneurysmal sac wasmultiple in one case, the venous return wasmultiple in one case . In only one instance wasthe connection between the renal artery (right)and the inferior vena cava [25] .

The fistulous connection ranged from 0 .4 to1 .0 cm . in diameter among the six cases inwhich this was mentioned . The aneurysmal sacwas variously described as arterial, venous, botharterial and venous, and, not infrequently, it wascommented that the vessel structure was suchthat it was impossible to distinguish artery fromvein. Calcium was noted in the wall of theaneurysm in four cases [14,33-36] . Dilation ofproximal veins, such as the inferior vena cavaand gonadal veins (Fig. 7C), was conspicuousVOL . 37, OCTOBER 1964

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and must be recognized and controlled atoperation. The findings in the hypertensivepatients were similar .

The congenital lesions were angiomatous orcirsoid in nature with multiple vascular shunts .Histologic findings were noted in two cases ; inone [15] there was intimal proliferation, withareas lacking elastic membrane formation, sothat vessel typing was difficult, and in the other[Case 1 in 18] chronic pyelonephritis and nephro-sclerosis was reported .

The cases with hypernephroma were asso-ciated with invasion of the renal vein by thetumor in most instances, as in our second case .In three, tumor was seen eroding arterial walls .The communications may therefore be multipleand are located within the substance of thetumor .The fistula was single in all the traumatic

cases. Histologic studies were available in fourof these . In two cases examination of the kidneyrevealed discrete focal changes : focal glo-merulosclerosis in one [26] and focal chronicpyelonephritis in the other [27] . Histologic studyin the third patient [24] revealed marked narrow-ing of the renal artery distal to the fistula due tointimal proliferation and fibrosis . The renalparenchyma was normal . In the remaining case[Case 3 in 18], nephrosclerosis was marked .

Histologic studies in the inflammatory grouprevealed little similarity among the cases . Inone instance [30] granulomas replaced the mediaand adventitia of the aneurysm. Gelatinouschanges were noted in the artery and vein . Inone case [32] there was a granulomatous arteritisof small intrarenal and perirenal vessels,fibrinoid necrosis of arterioles and multiplearteriovenous connections both within thekidney and in peripelvic fat. The third patient[31] had subacute bacterial endocarditis . Histo-logic examination of the surgical specimenshowed a subacute inflammatory lesion sur-rounding the aneurysm as well as abnormalarteriovenous communications of small vesselsand hyperplasia of the muscular fibers of thesmall arteries .

In the group with idiopathic fistula, histologicstudy of the kidney was made in four cases . Inour Case i the infarction was incomplete .Thomas and co-workers [36] recorded markedpyelonephritis . Rossi and associates [39] de-scribed a small kidney with abundant scartissue. Hutch and Chisholm [38] noted mucoiddegeneration of the media of both the renal

510

Renal Arteriovenous Fistula-Maldonado et al .

artery and vein . Loss of much of the elastictissue and smooth muscle in the renal artery atthe ostium of the fistula and in the aneurysmalsacs were features of our first case . This suggeststhat an aneurysm may have preceded thedevelopment of the fistula .

Results of surgical treatment: Specific commentsregarding the postoperative condition of thepatient were made in twenty-three cases . In allof them the patients had improved . Congestiveheart failure was relieved when present . Noinformation is available with regard to altera-tions in the degree of azotemia postoperatively .

Cardiomegaly and cardiac murmurs promptlydisappeared or became much less prominentafter operation . Hemodynamic alterations, whenmeasured, promptly returned to normal (casesdescribed by Jouve and co-workers [31] andby Scheifley and co-workers [22], and bothcases in this paper) .

Eight of the fifteen hypertensive patientsbecame normotensive (53 per cent) . One ofthese patients was also azotemic prior to opera-tion. In six patients, the diastolic blood pressurewas slightly reduced and in one case (Case i ofthis paper) the degree of diastolic hypertensiondiminished markedly and moderate doses ofantihypertensive agents were sufficient to con-trol the hypertension . Of three cases of hyper-nephroma in which hypertension was noted, theblood pressure in one returned to normal [21],while the blood pressure in the remaining twocases was reduced slightly after operation[20,22] . In the single case in the inflammatorygroup in which it occurred, the hypertensionwas slightly lowered following surgical treat-ment [30] . In the one case in the congenitalgroup in which hypertension was recorded,operation resulted in complete relief of thehypertension [17] . In seven of the traumaticcases the patients were noted to be hypertensive .The trauma had occurred from seventeenmonths to twenty-two years earlier . Operationcompletely relieved the hypertension in four .In two of these, histologic examination revealedfocal scarring [26,27], and in one there wascompression of the parenchyma [28] . In the twocases which occurred following renal biopsy andin the one following pyelolithotomy pre-existinghypertension, present in all, persisted [Cases 3,4 and 5 in 18] . In the idiopathic group, hyper-tension was noted in three cases . Markedscarring of the kidney was present in two[36,39] and incomplete infarction, in the other

TABLE IVCLINICAL MANIFESTATIONS OF POSTNEPHRECTOMY RENAL

ARTERIOVENOUS FISTULA IN FOURTEEN CASES

(Case i of this report) . Following operation, thehypertension was completely relieved in thefirst two, and much ameliorated in the other .

Arterioaenous Fistula After Nephrectomy . Thir-teen cases of postnephrectomy arteriovenousfistula have been reported [42-54] . * An addi-tional case (the first) was strongly suspected onthe basis of clinical data, but in contrast to theothers was not explored [55] .

Nephrectomy had been carried out as treat-ment for renal tuberculosis in three cases, forpyonephrosis or hydronephrosis in three cases,and for renal stones in three cases . No indicationswere noted in the five remaining cases .

Nephrectomy preceded the finding of a fistulaby five months to thirty-five years . It is likelythat in all, or at least in the majority of the cases,ligation en masse of the renal artery and veinhad been performed .

Clinical features : t The mean age in this groupwas fifty years (range, twenty-seven to sixty-eight years) . Eight patients were women andfive were men . As in the group of patients withfistulas occurring with a functioning kidney, theclinical features were those associated with highcardiac output, but diastolic hypertension wasnoted only twice . (Table iv.) Flank painoccurred with greater frequency in this groupand often served to draw attention to thenephrectomy site . The characteristic bruitdescribed in the preceding section was noted inall but one case . The only special investigationcarried out was aorticorenal arteriography andthe results were diagnostic or highly suggestiveof a fistula in the nine patients in whom thisstudy was performed .

* Elliot [45] reported two cases .t The patient described by Poutasse [54] had only a

bruit. The aortogram was diagnostic.AMERICAN JOURNAL OF MEDICINE

Manifestation No . Per cent

Intra-abdominal bruit 13 93Cardiomegaly11 79Congestive heart failure 7 50Pain 5 36Azotemia 3 21Diastolic hypertension 2 14Hematuria 1 7Syncope 1 7

Renal Arteriovenous Fistula-Maldonado et al .

Surgical treatment and results : The fistula andaneurysmal sac were located at the stump ofthe renal pedicle in all cases . All fistulas involvedthe renal artery and vein ; in one case the inferiorvena cava may have been involved rather thanthe renal vein [50] . The renal vein and inferiorvena cava were dilated greatly . In five cases boththe renal artery and vein were ligated ; in four,the sac was resected ; in two, the renal artery onlywas ligated ; and in one, the renal artery wasligated and sectioned .

One patient died of coronary thrombosis onthe second postoperative day . The remainingeleven underwent prompt and marked clinicalimprovement in the degree of heart failure andother manifestations of high cardiac output . Thediastolic hypertension was unchanged in the twopatients in whom this existed preoperatively .

COMMENTS

Arteriovenous fistulas of the renal vessels, incommon with fistulas between other vessels ofsimilar size, result in an increased cardiac outputaccompanied by decreased peripheral resistanceso that the systolic blood pressure increases anddiastolic blood pressure decreases . Cardio-megaly, and eventually congestive heart failure,often ensues [56-59] . This is true when thefistula develops following nephrectomy ; how-ever, when a functioning kidney is still presentthis picture frequently is modified by thepresence of diastolic hypertension. Lasher andGlenn [60] produced renal arteriovenous fistulasin dogs and noted the development of mildhypertension with severe renal damage . Incom-plete infarction of the kidney was noted in ourCase i in the absence of stenosis of the renalartery or thromboembolism . Four other patientswith functioning kidneys, in whom the hyper-tension was completely relieved, had ipsilateralparenchymal scarring [26,27,36,39] .

The renal function studies in our Case i con-firm the reduction in functioning renal paren-chyma and also demonstrate an ischemicpattern on the side of the fistula in man . Thefrequent relief of the diastolic hypertension bynephrectomy is additional evidence that thehypertension may result from the alterations inrenal hemodynamics . The persistence of hyper-tension after operation in our Case i and in thesix cases in the literature [20,22,30 and Cases 3, 4and 5 in 18] may be related to the severity andduration of the hypertension and the degree ofcontralateral damage, or to pre-existing hyper-VOL . 37, OCTOBER 1964

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tension on some other basis . Nephrosclerosis of acontralateral kidney was illustrated to be amechanism for persistent hypertension by Thaland co-workers [6], following repair of uni-lateral renal artery stenosis in man .

The cases reviewed in this paper were dividedinto two large groups, depending on whether ornot a functioning kidney was present on thesame side as the fistula. When it was, a furtheretiologic subdivision was made . Such a classifi-cation is of importance, even though thesymptom complexes are not distinguishable,since the prognosis in cases of hypernephroma,for example, differ from that in cases of trauma .In the past, cases lacking specific pathologic datafrequently have been designated as congenitalin origin . We suggest that this term be reservedfor the angiomatous malformations but untiltheir exact nature is known the cases that cannotbe otherwise classified are best grouped pro-visionally as idiopathic in origin .

The mechanism of fistula formation was clearin some of the cases . Those which developedfollowing nephrectomy were likely due to liga-tion en masse of the renal vessels, with subse-quent necrosis of the wall and perforation .Similar changes occurred after direct trauma .In congenital lesions, the large vessels made upthe fistula . Among the cases of hypernephromathere frequently existed both a connection oflarge artery to vein due to tumor invasion andlarge communicating vascular spaces within thepartially necrotic tumor . In the remaining casesthe initial lesion probably was an arterialaneurysm which eventually eroded the wall ofthe vein to form the connection .An arteriovenous connection should be

suspected in all instances of high cardiac output .The presence of a continuous, high-frequencybruit over the kidney supports suspicion of arenal arteriovenous fistula, especially if asso-ciated with diastolic hypertension or hematuria .Excretory urography, radioisotope renographyand other tests of renal function are usefuladjunctive studies, but the greatest diagnosticaid is obtained by determination of cardiacoutput, central and regional studies of bloodflow, and aorticorenal arteriography .

Although surgical management has necessi-tated total nephrectomy in cases of hyper-nephroma, extensive vascular lesions and severerenal damage, it is presumed that preservationof renal function might be accomplished in thespecial situation in which arterial and venous

512 Renal Arteriovenous Fistula-Maldonado et at .reconstruction is possible . However, the localpathologic anatomy and the general conditionof the patient usually encourage the surgeon tobe content with total or partial nephrectomy.

SUMMARY

A case of renal arteriovenous fistula ispresented in which radioisotope renography anddifferential studies of renal function stronglysuggested the presence of ipsilateral renalischemia, subsequently confirmed . Another case,due to hypernephroma, is described in whichaorticorenal arteriography revealed vascularlakes within the tumor, together with markedextrarenal venous dilation . Fifty-three pre-viously reported cases of renal arteriovenousfistula are reviewed in detail, with specialattention to the relationship of diastolic hyper-tension to the renal and vascular pathology .

ADDENDUM

Since this review was completed, three addi-tional cases of renal arteriovenous fistula withfunctioning kidney [61,62] and one case ofpostnephrectomy fistula [63] have been reported .Two of the three fistulas with functioning kidneyappeared after percutaneous renal biopsy [61] .Another postnephrectomy fistula was seenrecently in a patient at the Mayo Clinic .

Acknowledgment : Drs. R. F. Haff and J. P .Grier in Omaha, Nebraska, were very helpful inobtaining early data in our Case i. We wouldalso like to express our appreciation to ourcolleagues, Drs . J. C. Hunt, F. T. Maher, A .Schirger and H . J . C. Swan, for their advice andsuggestions .

REFERENCES

1 . TAUxE, W. N., HUNT, J. C . and BURBANK, M. K.The radioisotope renogram (ortho-iodohippurate-I's') . Standardization of technic and expressionof data. Am. J. Clin . Path ., 37 : 567, 1962 .

2 . BURBANK, M. K., HUNT, J. C., TAUXE, W. N. andMAHER, F. T. Radioisotopic renography . Diag-nosis of renal arterial disease in hypertensivepatients. Circulation, 27: 328, 1963 .

3. MAHER, F. T . Separated renal function studies .Proc. Staff Meet., Mayo Clin ., 36 : 701, 1961 .

4. HOWARD, J. E. and CONNOR, T. B. Hypertensionproduced by unilateral renal disease . Arch . Int .Med., 109 : 8, 1962 .

5 . Fox, I . J. and WOOD, E . H. Applications of dilutioncurves recorded from the right side of the heart orvenous circulation with the aid ofa new indicatordye. Proc. Staff Meet., Mayo Clin., 32 : 541, 1957 .

6 . THAL, A . P ., GRACE, T . B. and VERNIER, R. L .Function of the contralateral kidney in renalhypertension due to renal artery stenosis . Circula-tion, 27 : 36, 1963 .

7. HUNT, J. C., HARRISON, E . G., JR ., KINCAID, O. W .,BERNATZ, P. E . and DAvis, G. D. Idiopathicfibrous and fibromuscular stenoses of the renalarteries associated with hypertension . Proc . StaffMeet., Mayo Clin ., 37 : 181, 1962 .

8 . VARELA, M. E . Aneurisma arteriovenoso de losvasos renales y asistolia consecutiva . Rev. med.Latino-Am., 14: 3244, 1928 .

9 . ADAMS, H. D. Congenital arteriovenous and cirsoidaneurysms . Surg ., Gynec . & Obst ., 92 : 693, 1951 .

10. GOLLMANN, G. Hypertonus bei einseitiger Nieren-arterienstenose mit arteriovenoser Fistel . Fortschr .Geb . Rontgenstrahlen, 88: 684, 1958 .

11 . BRINK, A. J . Vascular fistulae (with a report on casesof pulmonary, renal and peripheral arteriovenousfistulae) . South African J. Lab . & Clin. Med., 6 :158, 1960.

12 . CAMPS, F . B. Quoted by Lasher, E. P., Jr. andGlenn, F. [60].

13 . Huu-HY-HUNG. Quoted by Nguyen-Huu, Ngo-Gia-Hy and Bui-Mong-Hung [16] .

14 . CHEVERAU, R. Quoted by Nguyen-Huu, Ngo-Gia-Hy and Bui-Mong-Hung [16] .

15 . SLOMINSKI-LAWS, M . D., KIEFER, J . H. and VER-MEULEN, C. W . Arteriovenous aneurysm of thekidney . Case report . J. Urol., 75 : 586, 1956 .

16. NGUYEN-Huu, NGO-GIA-HY and BuI-MONG-HUNG .Anevrysmes arterio-veineux des vaisseaux renaux .Rein en place; leur role dans l'hypertensionarthrielle d'origine renale . Presse mid., 67 : 1680,1959.

17 . GRACE, J. T., STAUBITZ, W., LESSMANN, F . andEGAN, R . Intrarenal arteriovenous fistula . Arch .Surg ., 81 : 718, 1960 .

18 . BOIJSEN, E . and KdHI.ER, R . Renal arteriovenousfistulae . Acta radiol., 57 : 433, 1962 .

19 . MYHRE, J. R. Arteriovenous fistula of the renalvessels. A case report . Circulation, 14 : 185, 1956 .

20. ABBOTT, C. E . and POUTASSE, E. F. Renal arterio-venous fistula. Occurrence in renal-cell carci-noma. Report of a case . Cleveland Clin. Quart ., 28 :283, 1961 .

21 . HAMILTON, G. R., GETZ, R. J. and JEROME, S.Arteriovenous fistula of the renal vessels. Casereport and review of the literature . J. Urol., 69 :203, 1953 .

22 . SCHEIFLEY, C. H., DAUGHERTY, G. W., GREENE,L. F. and PRIESTLEY, J. T . Arteriovenous fistulaof the kidney. New observations and report of threecases. Circulation, 19: 662, 1959 .

23 . JANTET, G. H., FOOT, E. C . and KENYON, J . R.Rupture of an intrarenal arteriovenous fistulasecondary to carcinoma. A case report . Brit . J.Surg., 49 : 404, 1962 .

24 . KIRBY, C. K ., NICHOLS, W. G., GARRITANO, A . P.,WOHL, G. T. and PIETROLUONGO, A. L . Arterio-venous fistula of the renal vessels. A case report .Surgery, 37 : 267, 1955 .

25 . WINTER, B ., KAUFMAN, J. J., ALLENSTEIN, B . J . andBECK, W. A., SR . Arteriovenous fistula betweenright renal artery and inferior vena cava . Cali-fornia Med_, 91 : 285, 1959 .

AMERICAN JOURNAL OF MEDICINE

26 . PELOT, G., PESSEREAU, G . and DAFTARI, B. Hyper-tensions malignes et nephropathies unilat6rales .A propos de 4 observations. J . urol ., Paris, 60 :245, 1954 .

27 . BARON, G. J. and KOENEMANN, R. H . Arteriovenousfistula of the renal vessels. A case report. Radiology,64: 85, 1955 .

28 . MILLOY, F ., JR., FELL, E. H., DILLON, R . F . andZAYAS, A . M. Intrarenal arteriovenous fistula withhypertensive cardiovascular disease. Review of theliterature . Am. J. Surg ., 96 : 3, 1958 .

29 . VEST, S . A. Renal arteriovenous fistula . UrologistCorrespondence Club. December 6, 1954.

30 . RIEDER, W. Sonderstellung arterio-venoser Aneu-rysmen der Nierengefasse im Rahmen operativerBehandlung schwerer Herz-Kreislaufschaden beimarterio-venosen Aneurysma . Chirurg, 14 : 609, 1942 .

31 . JOUVE, A., AUGIER, P., PAYAN, H., GERARD, R .,MEDVEDOWSKY, J.-L . and GUILLEMAUD, J . Lescommunications arterio-veneuses renales . Pressemid., 66 : 1669, 1958 .

32 . SCHULZE-BERGMANN, G . Uber das arterio-venoseAneurysma der Niere. Ztschr . Urol ., 47 : 661, 1954 .

33 . BORNE, A. W . and HENDERSON, G . L. Intrarenalarteriovenous aneurysm. Case report . In: Pro-ceedings of the North Central Section of theAmerican Urological Association, p. 67 . Minne-apolis, 1957 . Burgess Publishing Co .

34 . PEARSE, R. and MACMILLAN, R. L. Congenitalarteriovenous aneurysm of the renal artery . J.Urol., 58 : 235, 1947 .

35 . SAUTER, K. E. and SARGENT, J. W . Spontaneousrupture of intrarenal arteriovenous fistula. Reportof a case. J . Urol ., 83 : 17, 1960 .

36 . THOMAS, R. G., GRIEVE, S. and LEWIN, B. Spon-taneous renal arteriovenous fistula and contra-lateral renal artery aneurysm . Brit. J. Radiol .,35 : 128, 1962 .

37 . EDSMAN, G . Angionephrography and suprarenalangiography. A roentgenologic study of the normalkidney, expansive renal and suprarenal lesions andrenal aneurysms. B. Arterio-venous aneurysms .Acta radiol., (supp. 155), p. 110, 1957 .

38. HUTCH, J. A. and CHISHOLM, E . R. Intrarenalarteriovenous fistula . J. Urol ., 88 : 150, 1962 .

39 . Rosss, P., GAMBINI, E . and CINOTTI, G. A. Le fistoleartero-venose renali . Rass . fisiopat. clin., 32 : 136,1960 .

40 . HOFFMAN, H. A. and FONTOURA, H. Arteriovenousaneurysm of the kidney . J. Internat . Coll. Surgeons,29: 729, 1958 .

41 . PUCHLEw, A . Zur Hamodynamik des arteriovenosenAneurysma. Ztschr. Kreislaufforsch ., 34: 665, 1942 .

42. GARRITANO, A . P ., WOHL, G. T ., KIRBY, C. K . andPIETROLUONGO, A. L. The roentgenographicdemonstration of an arteriovenous fistula of renalvessels. Am. J. Roentgenol., 75: 905, 1956.

43. HARBISON, S. P ., GREGG, F . J . and GUTIERREZ, I . Z .Arteriovenous fistula following nephrectomy.Report of a case complicated by severe azotemiaand congestive failure . Ann. Surg ., 152 : 281, 1960.

VOL . 37, OCTOBER 1964

Renal Arteriovenous Fistula-Maldonado et al . 513

44 . ARAVANIS, CH., MICHAELIDES, G., ALIVIZATOS,C. N . and LAZARIDES, D . Renal arterio-venousfistula following nephrectomy. Ann. Surg ., 156 :749, 1962 .

45 . ELLIOT, J . A. Post-nephrectomy arteriovenousfistula. J. Urol., 85 : 426, 1961 .

46 . GOKARN, A. and SWINNEY, J . Arteriovenous aneu-rysm of the renal artery after nephrectomy . Brit .J . Urol ., 34 : 15, 1962 .

47 . MULLER, W. H., JR. and GOODWIN, W. E. Renalarteriovenous fistula following nephrectomy . Ann.Surg ., 144 : 240, 1956 .

48 . SHIREY, E. K. Cardiac disease secondary to post-nephrectomy arteriovenous fistula. Report of acase . Cleveland Clin. Quart., 26 : 188, 1959 .

49 . TYSON, K. R. T . and DERRICK, J. R. Renal arterio-venous fistula after nephrectomy . A case report.Southern M. J., 55 : 558, 1962 .

50 . DUBOST, C. and MATHIS, P . Un cas d'anevrysmearterio-veineux reno-renal apres nephrectomie .Mim. Acad. de chir ., 82 : 132, 1956.

51 . ELKIN, D . C . Aneurysm following surgical pro-cedures. Report of five cases . Ann . Surg ., 127 : 769,1948 .

52 . SCHWARTZ, J. W ., BORSKI, A . A. and JAHNKE, E. J .Renal arteriovenous fistula . Surgery, 37 : 951, 1955 .

53 . GROSGOGEAT, Y., MAURICE, P . and DUBOST, C .Insuffisance cardiaque par fistule arterio-veineuserenale. Arch. mal . coeur., 54 : 1150, 1961 .

54 . POUTASSE, E. F. Renal artery aneurysm. Report of12 cases, two treated by excision of the aneurysmand repair of renal artery . J. Urol., 77 : 697, 1957 .

55 . HOLLINGSWORTH, E . W. Arteriovenous fistula of therenal vessels. Am. J. M. Sc ., 188 : 399, 1934.

56 . HOLMAN, E . The physiology of an arteriovenousfistula . Arch . Surg ., 7 : 64, 1923 .

57 . HOLMAN, E. Experimental studies in arteriovenousfistulas . I. Blood volume variations . Arch . Surg., 9 :822, 1924 .

58 . HOLMAN, E. Experimental studies in arteriovenousfistulas . In . Cardiac dilatation and blood vesselchanges. Arch . Surg ., 9 : 856, 1924 .

59 . REID, M . R. The effect of arteriovenous aneurismsupon the heart : with the report of a case studied byProfessor Rudolph Matas, Dr. Georger Herrmannand the author . Ann . Surg ., 95 : 578, 1932 .

60 . LASHER, E. P ., JR. and GLENN, F . Effects on kidneyand blood pressure of artificial communicationbetween renal artery and vein . Arch . Surg ., 38 :886, 1939 .

61 . BLAKE, S ., HEFFERNAN, S. and MCCANN, P. Renalarteriovenous fistula after percutaneous renalbiopsy. Brit. M. J., 1 : 1458, 1963 .

62 . FEINBERG, S. B . and GOLDBERG, M. E. Arteriovenouscommunication of the kidney in a patient withhypertension . Report of a case in which the diag-nosis was suggested by routine pyelography .Radiology, 81 : 601, 1963 .

63. BRANDT, J . L. Hypertension after closure of post-nephrectomy arteriovenous fistula . A case reportand hypothesis . Canad. M. A . J., 89 : 405, 1963.