Arteriovenous Fistula of the Splenic VesselsProducing Ascites

By WILLIAM C. CASSEL, JOHN A. SPITTEL, JR., F. HENRY ELLIS, J1t., AN) ANI)RE .J. BR v-1:,:

Arteriovenous fistula involving the portal vein or its tributaries is a rare condlition that in some

cases can be treated successfully by, suigery if it is recognized. The clinical manifestations and

(liagnostic criteria are presented.

T HE opportunity to cure ascites is a gratify-ing clinical experience but is seldom en-

countered. Recently we have observed andsuccessfully treated a patientt with as(ites andan arteriovenous fistula of the spleniic arteryand vein.

Arteriovenous fistulas may occur whereverarteries and veins lie in proximity. The usualclinical maanifestations, such as thrill, machin-ery murmur, increased venous pressure withits sequelae in the involved region, and at timescardiac enlargement and failure, are wellknown. An arteriovenous communication be-tween a systemic artery and the portal vein orone of its tributaries quite logically mightproduce portal hypertension and its sequelae.Sigwartl reviewed the literature prior to 1953and found 3 cases2-4 of splenic arteriovenousfistula reported in detail and another5 mems-tioned, and he added 1. In 1935 Stener6 re-ported a case. Of these, only 1, the patient ofGoodhart,3 had ascites, while 4 patients pie-sented with repeated gastrointestinal bleedingfrom esophageal varices.1' 3 4, 6 Two instancesof hepatoportal arteriovenous fistula have beenreported7' and 1 of these patients had ascites.7

CASE REPORT

A 34-year-ol0( housewife eamnc to the _Mayo Clinicon October 29, 1956 because of swelling of the abdo-men of 4 to 5 weeks' duration. Three months priorto admission her third pregnancy was terminatednormally. The pregnancy was complicated by hyper-tension and by edema of the ankles during the eighthand ninth months. For 2 months post partum shefelt well. Four to 5 weeks prior to admission shenoted rapi(1 increase in the size of her abdomen un-accompanied by dyspnea, peripheral edema, fever,or pain. Two to 3 weeks prior to admission anorexia

From the Mayo Clinic and the MIayo Foundation,Rochester, AIinn. The Mayo Foundation, Rochester,Minnesota, is a part of the Graduate School of theUniversity of Minnesota.

nausea, an(l vomiting (leveloped and she noted afull sensation in her abdomen. X-rav studlies re-vealed the presence of calcified cyst-like structturesin the left upper quadrant of the abdomen. Laparot-oiny was I)erforme(l on October 26, 1956, with Iapreoperative diagnosis of pancreatic cyst. After4,500 ml. of straw~-colored ascitic fluid wvere remnoved,the left kidney was seen to be (lepressed by a cysticmass that was said to involve the left kidney and tobe fixed to the spleen. Aspiration of the mass (lis-closed 1)loo0(. Further exploration was not performedand the abdomen was closed. Three daxys postopera-tivelv the patient was referred to the Mayo Clinicfor further (liagnosis and treatment.

The history reveale(l that 11 years prior to acl-mission the patient had sustained a bullet wound ofthe left lower part of the thorax. The bullet enteredanteriorly at the sixth intercostal spacc in the Iniil-clavicular line, and came out at the costal marginin the left posterior axillarv line. The patient washospitalized and treated conservatively, and re-covered in 2 weeks.

Physical examination revealed a slender, (hlO1ri-call- ill young woman whose wveight was 135 pouncls.Entrance and exit scars of the old bullet woun(l werepresent on the left lower part of the thorax. Therewas a recent left abdominal incision. The abdomenwas disten(ledl, with evidlence of free fluid. The edgeof the liver, felt 1 to 2 fingerbreadths below the rightcostal margin, was smooth and nontender. The tipof the spleen was Ialpable. A continuous multiple-pitche(l murmur was audible over the left postero-lateral part of the thorax about 2 cm. lateral to thebullet scar. The results of physical examinationwere otherwise negative. There was no peripheraledlenma, distention of the veins of the neck, or spi(lerangiomas.

Laboratory stu(lies revealed the followving: mol-erate albuminuria with miicrohematturia; hemio-globin, 12 Gm. pier 100 ml. of bloo1(; leuko(y-tecount, 12,100 per mm.3; erythrocyte se(limentationrate, 65 mm. in the first hour (Westergren); floccu-lation reaction for syphilis, negative; fasting 1)loodsugar, 128 Img. per 100 ml.; blood urea, 38 mg. per100 ml.; serum bilirubin, negative reaction (lirect,and 0.9 mg. per 100 ml. indirect; sulfobromnophtha-lein (Bromsulphalein) retention after 1 hour, grade 3(34 per cent); thymol turbidity, 0 unit; cephalin-cholesterol flocculation, negative; alkaline phospha-

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1078 ARTERIOVE-NOUS FISTULA OF THE SPLENIC VESSI'LS PIROI)U(ING ASCITIS

FIG. 1. a. Roentgeinogram of the abdomen showing crescentic areas of calcification in the leftupper quadrant. b. Aortogram showing enlarged tortuous splenic artery- anl opacificatioli withinthe calcified areas. c. Aortogramn folloxi lug second injection of dye. There is opacificatiori of thevenous aneurysm adj acent an(1 medli al to the calciurm-cont aining aneurysms. d. Roentgenogramtaken 10 seconds after the one represented in c, showing enlarge(1 splenic a(1d p)ortal veinXs.

tase, 58 King aIndlArmistrong units per 100 ml. ofserumi; serumI proteins, 7 Gim. per 100 mIl., waith5 Gm. of albumin and 2 Gmn. of globulin.

Roentgenographic examination (licl not (liscloseany abnormality of the thorax, lut (lid show linearcalcification in the shape of aln incomplete oval,measuring 4 by 3 cm., in the left upper quadrantof the abdomen.

Excretory urography showed 2 egg-shaped areasof calcification 4 cm. in diameter in the left supra-renal area (fig. la). These were thought to be extra-renal, and the upper pole of the left kidney appearedto be compressed as if b1 a suprarenal mass. Leftretrograde pvelographic examination gave no addi-tional information.

Abdlominal l).lrace(ntesis vieled83,000 mnl. of sero-sanguineous fluid. Culture of the ascitic fluid forbacteria andl examination of it for malignant cellsgave negative results.

The ascites, the (lassie murmur of aIn arterio-venous fistula over the left lower l)art of the thoraxthe calcifilations in the left upper (Qua(lrant of theabdomen as revealed roentgenographically, and thehistory of a bullet wound of the left lower plart ofthe thorax 11 years previously suggeste(l a sl)l(eiicarteriovenous fistula.

Aortogral)lhy, was performed to confirm the (lini-cal impression. Because of the possible danger ofpassing a nee(dle into an aneurysm, it was d(leidedthat .aortogir.lphli performed via a catheter in the

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CASSEL, SP'ITTIEL, ELLIS, AND BRUWER

FIG. 2. Biopsy specimen from the liver. Theparenchyma is normal (hematoxylin and eosin;X 200).

aorta would be safer than translumbar aortography.However, an attempt to pass a catheter down thedescending thoracic aorta via the left brachial arterywas unsuccessful. Routine translumbar aortographywas therefore performed, the needle being passedinto the aorta at the level of the first lumbar verte-bra. When the tip of the needle was about half waybeteleen the skin and the aorta, blood wsas aspiratedfrom a low pressure site; it seemed probable thatthe venous sac of the arteriovenous aneurysm wastraversed.

After the needle had been placed in the aorta,two injections of 70 per cent acetrizoate (Urokon)sodium were made. After the first injection, consist-ing of about 10 ml., the roentgenogram (fig. lb) re-vealed an enlarged, tortuous splenic artery anddense opacification within the calcified areas in theleft upper quadrant. At the end of the second injec-tion, consisting of about 35 ml. of opaque material,the roentgenogram showed that a large uncalcifiedaneurysm had become opacified adjacent and medialto the calcium-containing aneurysms (fig. 1c). An-other roentgenogram (fig. Id) taken about 10 sec-onds after the end of the second injection demon-strate d that the opaque material that had pooled inthe uncalcified area emptied into the splenic vein,and that the splenic and portal veins weere c(onsider-ably enlarged. It was evident from these studies that

FIG. 3. Drawing of gross specimen.

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1080 ARTERIOVENOUS FISTULA OF THE SPLENIC VESSELS PRODUCING ASCITES

FIG. 4. Opened surgical specimen with probe in arteriovenous fistula.

the calcified shadows in the left upper quadrantwere related to the arterial aneurysm and that theeven larger venous aneurysm contained no calcium.

All other branches of the abdominal aorta wereof normal caliber.

Operation was undertaken on the ninth day afteradmission. A left thoraco-abdominal incision wasmade, the old scar being excised and the incisionbeing continued laterally over the costal arch andinto the thorax through the seventh intercostalspace. The diaphragm was opened partially in theline of the incision.The liver was tremendously enlarged and the left

lobe extended laterally well under the left leaf of thediaphragm. The liver was smooth in contour. Biopsyshowed normal hepatic parenchyma (fig. 2). Thegastrohepatic omentum was opened and an en-larged, tortuous splenic artery was visualized; thiswas doubly ligated near its origin. Immediately thecontinuous murmur audible to the anesthesiologistover the left posterior part of the thorax disappeared.The veins in the mesentery of the small intestinewere not dilated. The remainder of the abdomen atexploration appeared normal except for the regionof the spleen.

In the hilar region of the spleen a lobulated aneu-rysm of the splenic artery was visualized, and asso-ciated with it was a much larger aneurysm of thesplenic vein; the latter aneurysm lay anteriorly andsomewhat inferiorly (fig. 3). The spleen was denselyadherent to the diaphragm and was dissected awaywith some difficulty. It was eventually retracted up-ward and medially, whereupon the aneurysms of thesplenic vein and artery were thoroughly exposed. Asthe dissection continued, a portion of the splenicvein was reached that, although enlarged, was smallenough to permit ligation and division. The splenic

artery was likewise ligated and divided. It wasnecessary to remove a portion of the tail of thepancreas as well.The excised specimen therefore consisted of the

spleen, the aneurysms of the splenic artery and thesplenic vein, and a portion of the tail of the pancreas.When the specimen was opened, a communication4 mm. in diameter was found between a bilocularaneurysm of the splenic artery and an aneurysm ofthe splenic vein (fig. 4). Each locule of the arterialaneurysm measured 4 cm. in diameter, and the ve-nous aneurysm measured 8 by 5 by 5 cm.

The cut end of the pancreas was oversewn, thediaphragm was closed, the costal arch was reapproxi-mated, and the thorax and abdomen were closed.The patient's postoperative course was unevent-

ful. The mild diabetes, as evidenced by the increasedconcentration of blood sugar, was managed withoutincident by a diabetic diet. The platelet count rosefrom 240,000 per mm.3 on November 10 to 572,000on November 13 and to 653,000 on November 16.A routine urinalysis on November 9 gave negativeresults. The serum bilirubin reaction remained nor-mal postoperatively, and the concentration ofalkaline phosphatase decreased to 38.7 King andArmstrong units per 100 ml. of serum by the tenthpostoperative day. Sulfobromophthalein retention atthe end of 1 hour on the ninth postoperative (lay wasgrade 1 (6 per cent). Three months postoperativelythe patient said that she was well and had notedno further ascites.

DISCUSSION

The mechanism of formation of ascites is notfully understood. Volwiler, Grindlay, and Boll-man9 observed in dogs with normal plasma

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CASSEL, SPITTEL, ELLIS, AND BRUWER

TABLE 1.-Features of Reported Cases of Splenic Arteriovenous Fistula

Author

Weigert2(1886)

Goodhart3(1889)

Blakemore4(1948)

Sigwart'(1953)

Stener6(1955)

Authors'case

Age Gastrointestinaland sex bleeding

49F

49F

23F

25F

38F

34F

Notstated

Repeatedhema-temesisandmelena,5 mo.

Repeatedhema-temesis,20 yr.

Repeatedhema-temesis,9 yr.

Repeatedhema-temesisandmelena,20 yr.

None

Ascites

Notstated

Present

Notstated

Absent

Absent*

Present

Bruit

Notstated

Present

Notstated

Notstated

Present

Present

Site of fistula

Hilus ofspleen

2 in. fromhilus ofspleen

Not re-portedade-quately

In spleen

Hilus ofspleen

Splenichilararea, 2cm. fromspleen

* Ascites occurred postoperatively but was temporary.

Miscellaneous

Cause of death not given. Multiple ar-teriovenous communications at nec-ropsy.

Died from hematemesis. Single arterio-venous communication at necropsy.

Died postoperatively. Multiple arteri-ovenous communications. Portalpressure 350 mm. of water.

No gastrointestinal bleeding after re-moval of arteriovenous fistula andspleen. Portal pressure at operation430 mm. of water. Single communica-tion.

No gastrointestinal bleeding after re-moval of arteriovenous communica-tion and spleen. Multiple arterio-venous communications.

Ascites disappeared after removal ofarteriovenous communication andspleen. Single arteriovenous commu-tion.

protein that there had to be some element ofhepatic congestion to produce marked, spon-taneous, progressive ascites; such congestionwas produced by constriction of the thoracicinferior vena cava. In another group of dogsconstriction of the inferior vena cava and portalvein produced slight to moderate ascites whenthe dogs were made hypoproteinemic by plas-mapheresis. Baggenstoss and Wollaeger10 foundascites in 5 of 15 necropsy cases in which portalhypertension was due to occlusion of the extra-hepatic portion of the portal vein and in whichthere was no complicating disease that mightin itself have been a cause of ascites. They con-cluded that portal hypertension per se was animportant factor in the development of ascitesin these cases. They found evidence that asciteswas more likely to occur when the hepatopetalcollateral circulation was inadequately de-veloped.

Schilling and McKeell produced hepatopor-

tal arteriovenous fistulas in dogs and foundthat ascites developed in only 1 of them, thisoccurring 30 months postoperatively; thisanimal had evidence of disturbed hepaticfunction, and microscopic examination of itsliver revealed marked scarring and fatty infil-tration in many places. Servello and Rossi12did not observe ascites in dogs in which theyproduced splenic arteriovenous fistulas; thisfact may be related to the brief period of ob-servation (45 days). They did, however, notehepatic congestion and microscopic evidenceof dilatation of the hepatic vascular bed.

Besides our patient, only 1 other patient witharteriovenous communication of the splenicvessels has been reported as having ascites(table 1). Bleeding from esophageal varices,often repeated over many years, was a morecommon clinical manifestation. Blakemore4 andSigwartl found an increase of portal pressure intheir patients. The typical bruit of an arterio-

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1082 ARTERIOVENOUS FISTULA OF THE SPLENIC VESSELS PIRODUCING ASCITES

venous fistula has been noted in only 3 cases,including the present case.The cause of the arteriovenous fistulas in the

previously reported cases reviewed in table 1is obscure. Pre-existing trauma is not men-tioned in any of them. Three patients hadmultiple arteriovenous communications and 3,including ours, had a single communication.The existence of multiple communications sug-gests a congenital origin. In Sigwart's1 casethe communication was single but within thespleen and, in his opinion, was probably con-genital. In the 2 cases with multiple communi-cations and in which the history was reported,and in Sigwart's case, evidence of portal hyper-tension (gastrointestinal hemorrhage) appearedin childhood or early adult life; this suggests acongenital anomaly. Goodhart's3 patient, theonly one other than ours who had ascites, was49 years old and had hematemesis and melenafor only 5 months prior to death; the sin-gle arteriovenous communication was likely ac-quired and possibly the result of rupture ofan aneurysm of the splenic artery into the ad-jacent vein.The close relationship of the development of

ascites to parturition observed in our case sug-gests the possibility that an aneurysm of thesplenic artery ruptured into the splenic vein asa result of changes in intra-abdominal pressureincident to parturition. Owens and Coffeyl3have shown a relationship between pregnancyand rupture of a pre-existing aneurysm of thesplenic artery. It is equally possible that thesplenic arteriovenous fistula developed in ourcase at the time the bullet wound was inflicted11 years prior to the onset of ascites.

Ascites in arteriovenous fistula involving theportal system could be produced by either orboth of 2 factors portal hypertension andhepatic congestion. As previously mentioned,portal hypertension was shown to exist in suchcases by Blakemore4 and Sigwart' at the timeof operation. According to Baggenstoss andWollaeger,10 portal hypertension in itself cancause ascites. In addition, transmission ofarterial pressure to the portal system maycause hepatic congestion and ascites in a man-ner analogous to that in the experiments ofVolwiler and co-workers9 in which occlusion ofthe thoracic inferior vena cava caused hepaticcongestion and massive ascites. Significantly,

those patients whose fistulas were presumablycongenital did not have ascites. It is possiblethat in patients with multiple arteriovenousfistulas involving the portal system there issufficient hepatofugal circulation during thedevelopmental stage to prevent ascites.

Strickler7 and M\Iadding,8 with their co-workers, have each recently reported a case ofsingle communication between the hepaticartery and the portal vein, which would providean analogous alteration in the hemodynamicsof the portal vein, namely transmission of arte-rial pressure to the portal vein. The patient ofStrickler and co-workers had ascites andhematemesis. The arteriovenous fistula wasthought to have been acquired as a result ofrupture of a congenital aneurysm into theportal vein, as may have occurred in Goodhart'scase. The patient of Madding and co-workers8had gastrointestinal bleeding without ascites.These authors expressed the belief that thearteriovenous fistula was of congenital origin.

In 3 of the reported cases' 4, 6 (table 1) andin our case surgical approaches were made.The fistula was successfully removed in 3. Inthe 2 reported cases of hepatoportal arterio-venous fistula operation was unsuccessful.When calcium is present in an aneurysm of

the splenic artery the diagnosis can be madewith considerable confidence by routine roent-genologic methods. In 1932 Lindboel" made thisdiagnosis roentgenologically, and since thenthe roentgenologic features of such aneurysmshave been described repeatedly. There is noreason to believe that the arterial componentof a splenic arteriovenous aneurysm, once cal-cified, should have a different appearance.Calcium deposition in an aneurysm of the

splenic artery usually is manifested as a linearopacity in the shape of a complete or incom-plete oval representing shadows caused by thetangential trajectory of the beam. Thesecrescentic densities enclose mottled, ill-defined,calcific densities, representing the regionswhere the roentgen rays have passed throughthe aneurysm en face.

Culver and Pirson'15 have indicated that itmay take 10 to 20 years for calcification to de-velop in the walls of an aneurysm of the splenicartery. Particularly in cases prior to calci-fication, abdominal aortography should beperformed on the basis of clinical suspicion.

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CASSEL, SPITTEL, ELLIS, AND) BRUWER

Furthermore, aortography should always beperformed when the question of an intra-abdominal arteriovenous fistula arises, becauseby this means only can the extent of the uncal-cified portion of the lesion be demonstrated pre-operatively. In our case the venous (uncalcified)aneurysm was larger than the arterial (calci-fied) component.

SUMMARY AND CONCLUSIONS

Arteriovenous fistula involving the portalvein or its tributaries is a rare condition andmay be accompaniied by ascites. In this paperthe reports of 5 cases are reviewed and a newcase is reported; in addition, reports of 2 casesof hepatoportal fistula are reviewed.

Ascites, which was reported in 2 of the 6cases of splenic arteriovenous fistula, may beexplained on the basis of portal hypertensionor hepatic congestion or a combination of boththese factors. It occurred only in patients witha single arteriovenous fistula of the splenicvessels.

In patients with ascites or signs of portalhypertension, arteri ovenous fistula involvingthe portal system should be suspected, par-ticularly if a machinery murmur can be heard orif there is x-ray evidence of calcification in theregion of the portal vein or its tributaries. Thediagnosis can be established by aortography.Surgical cure is possible in some cases.

SUMMARIO IN INTERLINGUA

Fistula arteriovenose afficiente le venaportal o su tributarios es un condition rar epote esser accompaniate de ascites. Le pre-sente articulo passa in revista le reportos de 5casos e reporta un caso additional. In plus,reportos de 2 casos de fistula hepatoportal espassate in revista.

Ascites, que esseva reportate in 2 del 6casos de splenic fistula arteriovenose, poteesser explicate super le base de hypertensionportal o de congestion hepatic o de un com-bination de iste factores. Illo occurreva sol-mnente in patientes con un unic fistula arterio-vrenose del vasos splenic.

In patientes con ascites o signos de hyper-tension portal, fistula arteriovenose afficientele systema portal debe esser suspicite, special-mente si un murmure de locomotiva es audi-

bile o si il ha evidentia roentgenologic decalcification in le region del vena portal o sutributarios. Le diagnose pote esser establiteper aortographia. Curation chirurgic es possi-bile in certe casos.

REFERENCESSIGWART, H.: Portalcr Hochdruck dureh arterio-

v(nos(s Ancurysma d(r MIilzgcbarbe. Chirurg.24: 318, 1953.

2 WEIGERT, V. C.: In (lie MIilzvene geborstenesAneurvsma einer Milzarterie. Arch. path. Anat.104: 26, 1886.

3 GOODHART, .J. F.: Arterio-venous aneurysm ofsplenic vessels, with thrombosis of mescntericveins an(l localised acute colitis. Tr. Path. Soc.London 40: 67, 1889.

4BLAKEMORE, A. H.: Portacaval anastomosis forthe relief of portal hvpertension. Gastroenter-ology 11: 488, 1948.

ADAMS, H. I).: Congenital arteriovenous and cir-soid aneurysms. Surg., Gynec. & Obst. 92: 693,1951.

6 STENER, B.: Arterio-venous shunt in the spleendiagnosed before operation: Case report. Actachir. scandinav. 108: 344, 1955.

STRICKLER, ,J. H., LUFKIN, N., ANI) RICE, C. 0.:Hepatic portal arterio-venous fistula: A casereport. Surgery 31: 583, 1952.

8 M\IAI)DING, G. F., SMITH, AV. L., AND HERSH1BE}R-GER, IJ. R.: Hepatoportal arteriovenous fistula.J.A.AI.A. 156: 593, 1954.

9 VOLWILER, MW., GRINDLAY, J. H., ANI) BOLLMAN,,J. L.: The relation of portal vein pressure to theformation of ascites: An experimental study.Gastroenterology 14: 40, 1950.

10 BAGGENSTOSS,SA. H., ANI) AOLLAEGER, E. E.:Portal hypertension due to chronic occlusion ofthe extrahepatic portion of the portal vein: Itsrelation to ascites. Am. J. -Med. 21: 16, 1956.

11 SCHILLING, J. A., AND McKEE, F. W.: Late fol-low-up on experimental hepatic-portal arterio-venous fistulae. Am. Coll. Surgeons Clin. Cong.(39th), Proc. S. Forum. 4: 392, 1953.

12 SERVELLO, M\., AND Rossi, R.: L'arterializzazionedel fegato mediante anastomosi artero-venosespleno-splenische c spleno-portali: I. Ricerchesperimentali istologiche. Arch. ital. chir. 76:300, 1953.

13 OWENS, J. C., AND COFFEY, R. J.: Aneurysm ofthe splenic artery, including a report of 6 addi-tional cases. Internat. Abstr. Surg. 97: 313,1953.

14 LINDBOE, E. FR.: Aneurysm of the splenic arterydiagnosed by x-rays and operated upon withsuccess. Acta chir. scandinav. 72: 108, 1932.

15 CULVER, G. J., AND PIRSON, H. S.: Splenic arteryaneurysms: report of 17 cases showing calcifica-tion on plain roentgenograms. Radiology 68:217, 1957.

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ANDREÉ J. BRUWERWILLIAM G. CASSEL, JOHN A. SPITTEL, JR., F. HENRY ELLIS, JR. and

Arteriovenous Fistula of the Splenic Vessels Producing Ascites

Print ISSN: 0009-7322. Online ISSN: 1524-4539 Copyright © 1957 American Heart Association, Inc. All rights reserved.

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