Coronary artery fstulas

REVIEW ARTICLE

Coronary artery fstulas

S.A.M. Said, A.A.H.J. Thiadens, M.J.C.H. Fieren, E.J. Meijboom, T. van der Werf, G.B.W.E. Bennink

The aetiology ofcongenital coronary artery fistulasremains a challenging issue. Coronary arteries withan anatomically normal origin may, for obscurereasons, terminate abnormay and communicatewith different single or multiple cardiac chambersor great vessels. When this occurs, the angiographicmorphological appearance may vary greatly fromdiscrete channels to plexiform network ofvessels.Coronary arteriovenous fistulas (CAVEs) haveneither specific signs nor pathognomonic symp-toms; the spectrum of clinical features variesconsiderably. The clinical presentation of symp-tomatic cases can include angina pectoris, myo-cardial infarction, fatigue, dyspnoea, CHE, SBE,ventricular and supraventricular tachyarrhythmiasor even sudden iac death. CAVFs may, however,be a coincidental finding during dagnostic coronaryangiography (CAG). CAG is considered the goldstandard for diagnosing and delineating themorphological anatomy and pathway of CAVFs.There are various tailored therapeutic modalitiesfor the wide spectrum ofclinical manifestations ofCAVFs, induding conservative pharmacologicalstrategy, percutaneous transluninal embolisationand surgical ligation. (NeIkHeartJ2002;10:65-78.)

Key words: aetiology, angiographic morphology,clinical picture, congenital and acquired, coronaryartery fistula, treatment

S.A.M. Said.Department of Cardiology, SMT Hospital, Geerdinksweg 141,7555 DL Hengelo.AA.HJ. Thiadens.M.J.C.H. Feren.E.J. MelJboom.G.B.W.E. Bennink.Division of Paediatric Cardiology, University Medical Centre,Lundlaan 6, 3584 E4 Utrecht.T. van der Werf.Department of Cardiology, Heartcenter, University HospitalNyjmegen, PO Box 9101, 6500 HB Ni#megen.

Address for correspondence: S.A.M. Said.E-mail: [email protected]

The aetiology of congenital coronary artery fistulas(CAFs) is very complex. A coronary artery with an

anatomically normal origin may terminate abnormallyand communicate with different single or multiplecardiac chambers or great vessels. In such cases, theangiographic morphological appearance varies greatlybetween discrete channels and plexiform network ofvessels.

Arteriovenous malformations (AVM) may bepresent throughout the entire vascular system. Theymay be congenital or acquired, occurring after diag-nostic or therapeutic endovascular interventions.1I- Thehead, extremities and visceral organs are the mostcommon sites ofcongenitalAVM,whereas the thoracicwall appears to be a rare site.36 The symptoms ofcongenitalAVM do not usually appear until adult life,mostly in the second or third decade.' The same holdstrue for congenital coronary arteriovenous fistulas.Cardiac symptoms such as precordial pain, cardiacdysrhythmia and dyspnoea2 may rarely occur, especiallywhen theAVM are localised in the chest wall.

According to Levin, coronary artery fistulas are themost common haemodynamically significant congeni-tal defect ofthe coronary arteries.7 Even though manypatients with this condition are asymptomatic, latecomplications occur especially in the presence ofa largeleft-to-right shunt and include congestive heart fail-ure,9 myocardial ischaemia,9"10 endocarditis,9"1' atrialfibrillation,""2 pulmonary hypertension,""3 rupture,thrombosis or venous obstruction.9 Syncope andsudden death have also been reported in patients withCAVFs.'4 Consequently, surgical ligation of thearteriovenous or arteriocameral fistula has been recom-mended in most reported series in an effort to preventthese complications; perioperative mortality rates rangefrom 2 to 4%.91p

Although coronary arteriovenous fistulas (CAVFs)are infrequent, they are becoming increasinglyimportant and their early recognition is imperative, asmanagement and treatment could prevent seriouscomplications. Many large or symptomatic CAVFs areamenable to cure by surgical or percutaneous trans-catheter embolisation techniques.

Other abnormalities resulting from persistence of

Nctherlands Hcart Jounal, Volume 10, Number 2, Fcbruary 2002 65

Coronary artery fistulas

embryonal arrest such as ventriculo-venous com-

munications'6 are excluded from this study.

Prevalence of CAVFsCAVFs comprise 13 to 14% of the angiographicallyrecognised coronary artery anomalies.79"4 CongenitalCAVFs are found in approximately 1 in every 50,000patients with congenital heart disease.'7 The angio-

graphic prevalence is presented in table 1.The first reported post-mortem case ofCAVF was

by Krause in 1865.18 In the second decade ofthe 19thcentury, Trevor described the post-mortem findings ina case with a right coronary-right ventricular fistula.'9However, it was not until 1947 that Biorck andCrafoord made the first ante-mortem diagnosis ofthecondition during operation for presumed patent ductusarteriosus.30 In 1958, Munkner and colleaguesdescribed an ante-mortem congenital coronary arteryaneurysm associated with a coronary arteriovenousfistula.2' Historically, according to the site oftermina-tion, these fistulas may in some cases be present withcharacteristic continuous murmurs and occasionallymay be confused with patent ductus arteriosus.2

The results of physical examination are variable;the continuous murmur may be absent. Furthermore,during catheterisation intracardiac shunts are oftenundetectable.'4 Dating from the 1970s and from a

clinical point ofview, a CAVF was most liable to beconfused with a patent ductus arteriosus because ofthe similarity in physical findings and the formerlymuch higher incidence of the latter lesion. In 1970,PDA was the cause of a continuous murmur in 55%of adult patients.23 Nowadays, in children PDA is thecause of continuous murmur in only 10%.24 Even asrecently as 1989 there were still patients operated fora presumptive diagnosis ofPDA21 which peroperativelywas found to be a coronary artery fistula.

Coronary arteriovenous fistulas have a prevalenceof 0.1 to 0.2% (table 1), which has been reported in

subjects undergoing selective coronary angiography.'4'26This figure is surely too low since such lesions are

uncommon but not rare, and many single cases arenot reported or sometimes only reported in a hospitaljournal or local periodicals.27-30 Therefore Eie and hiscolleagues suggested that if all patients with anginalcomplaints were examined using selective coronary

angiography, the prevalence ofthis anomaly might proveto be higher than the currently accepted impression.

Deflnftlon of CAVFsCAVFs (figures 1 and 2) are defined as a congenital oracquired abnormal precapillary communicationbetween one or several coronary arteries (characterisedby normal origin of the coronary arteries) and anycardiac vein, chamber or great thoracic vessel bypassingthe myocardial capillary bed. They may present asarteriovenous fistulas (CS, cardiac veins, SVC andpulmonary artery) or arteriocameral fistulas (RA, RV,LA and LV). The arterioarterial fistulas (LV, LA andpulmonary veins) are very rare. These CAVFs shouldbe visualised without wedging of the catheter intocoronary artery to prevent rapid circulation ofcontrastmedium, which may give rise to erroneous identi-fication ofa pseudo-fistula.

To diagnose of true CAVFs, the following con-

ditions should be avoided:1. Forceful injection of a large amount of contrast

material into the coronary artery or side branch;2. Wedging and deep catheter engagement into

coronary artery or side branch.

Origin of fistulous communicationUnilateral CAVFs more frequently originate from theright than from the left coronary arteries.7'9 However,in 1986, Gillebert and associates26 found that the left

Figure 1. Frame ofklftanterior obliqueprojection of rigt coronary

artery angiogram depictng a prvximally locatedfistula (arrow)

with multiple origin and single termination into the pulmonary

artery.

Nctherlands Heart Journal, Volumc 10, Number 2, February 2002

Table 1. Prevalence of congenital coronary artery fistulas,angiographic series.

First author Year Subjects no PrevalenceTotal Flstula (%)

Querimit123 1971 2,500 6 0.2Baltaxe89 1977 1,000 2 0.2Gillebert26 1986 14,708 19 0.13Yamanaka14 1990 126,595 225 0.18

66


Figure2. Frame ofrghtanterior obiqueprojection ofkft coronaryartery angiogram demonstrating LAD-LVfrtula (arrows) withmultipk origin and multipk termination.

coronary artery was more frequently the origin ofCAVFs. This finding was in contrast to the figuresreported by McNamara et al." and in accordance withthe findings ofGoebel et al.32 who described the originofthe fistula by the left coronary artery in 75% oftheircases.

Pathway of fistulous communicationThe fistulous tract has been demonstrated to be asolitary single vessel or multiple convoluted plexusesofserpentive tortuous vessels.33 Aneurysmal formationcould be detected along the fistulous tract.2'34-37CAVFs terminate into the sites summarised in table 2.Over 90% ofthe CAVFs drain into the systemic low-pressure venous system.7

Aetiology and developmentThe aetiology ofcongenital CAVFs remains obscure.The primitive coronary circulation consists of wide,endothelial-lined spaces between the muscle columnsof the embryonal heart and ofsome endothelial out-growths towards the epicardi surfaces. The inter-

Table 2. Site of termination of CAVFs.

Percent Site of temnination

41 Right ventricle (RV)26 Right atrium (RA)17 Pulmonary artery (PA)7 Coronary sinus (CS)5 Left atrium (LA)3 Left ventricle (LV)1 Superior vena cava (SVC)

trabecular spaces or sinusoids freely communicate withthese newly fonned epicardial vessels and together formthe original sinusoidal circulation.

Intracardiac coronary artery termination may beinto the capillary plexus, into a myocardial sinusoid ordirectly into a lumen ofventricle. Generally speaking,blood entering the coronary arteries has a possible exitthrough any one or all of four routes:1. By extracardiac anastomoses (mediastinum, lungs,

parietal pericardium and diaphragm);2. By way of the arterio-luminal vessels directly into

the cardiac chambers (CC);3. By way of the capillaries and veins; either into the

coronary sinus (CS) or great cardiac veins (CV) andthence into the right atrium (RA) (conventionalroute), or through the Thebesian veins (TV) into thecardiac chambers;

4. Byway ofthe arterio-sinusoidal vessels through themyocardial sinusoids into the cardiac chambers.

The last three systems also anastomose with oneanother.

Speculations about the genesis of congenitalCAVFsThe pathogenesis of CAVFs is congenital in theoverwhelming majority ofcases or has, as has recentlybeen shown', an acquired pathogenesis due to in-creasing application of intravascular diagnosticinstrumentation and therapeutic procedures.

Normally, the outermost intertrabecular spacesshrink and melt with the coronary vessels to form acapillary network. The intertrabecular vessels retaintheir ventricular communications to form theThebesian veins of the adult heart. It could thus bespeculated that CAVFs develop due to an 'embryologicarrest' ofnormal closure ofthe intertrabecular spacesconnecting coronary arteries, veins and the cardiacchambers giving rise to persistence ofsuch sinusoidaltrabeculae.38 In its most primitive form, multiplecommunications may be present between a coronaryartery and cardiac chambers, since these are due topersistence ofembryonal vascular sinusoids in the heartmuscle communicating freely with coronary vessels.An accessory coronary artery originating from a cardiacchamber or the sinus ofValsalva has also been proposedin the case of a fistula as a single vessel with a singleorigin and termination.39

The precise pathogenesis is unknown but someauthors have speculated about such genesis consideringthe existence of right ventricular hypertension,40 thatthe failure of expansion of the right ventricular myo-cardium might allow the persistence of embryonicsinusoids4l and that some teratogenic factors may causea delay in development and result in an arrest ofcoronary vascular transformation.42 Factors that mightcontribute to the development ofCAVFs are:- Chemotactic factors43- Haemodynamic factors"- Chemical factors45

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Table 3. Acquired coronary arteriovenous fistulas.

Conditlon

Blunt and penetrating chest traumaRepeated endomyocardial biopsiesPermanent pacing-lead erosionCardiac or coronary surgerySecondary to severe coronary atherosclerosisand myocardial infarction

Complicating PTCA procedures

Acquired CAVFsCAVFs are most commonly congenital in origin butthey may also be acquired (table 3) secondary tovarious local and general pathological conditions.

Blunt and penetrating chest traumaCAVFs may develop after traumatic accidents andcontusion ofthe anterior thoracic wall. Automobile46and motorcycle29 blunt chest accidents were heldresponsible for the occurrence offistulas between theleft anterior descending and right coronary arteries andthe right ventricle (RV), respectively. Also penetratingthoracic wounds may cause a CAVF.4749

Repeated endomyocardial biopsiesRepeated endomyocardial biopsies are necessary inrecipients of heart transplants to diagnose tissuerejection. CAVFs orginating from one ofthe coronary

arteries and terminating into the RV have beenreported in such patients.5054 Fifty-two percent

originated from the right, 43% from the left anteriordescending artery (LAD) and 5% from the circumflexcoronary arteries in the series published by Sandhu etal.50 CAVFs occur in about 8% of cardiac transplantpatients. Spontaneous resolution of the fistulas inasymptomatic patients has been reported in the seriesof Sandhu et al.50 Direct ligation of the fistula andcoronary artery bypass grafting has been reported in a

symptomatic recipient oforthotopic heart transplant.54Obliteration of the fistula between the LAD and theRV by coil embolisation improved the symptoms in a

cardiac transplant patient.55

Pennanent pacing-lead erosionIt is strongly suggested that endocardial-pacingelectrodes may induce CAVFs. CAVFs arising fromthe LAD or septal artery and communicating with theRV have been reported by Saeian and associates56 in twopatients. The suggested mechanism is chronic erosionofthe interventricular septum by the pacing lead.

Cardiac or coronary surgeryCAVFs can occur after coronary artery bypass surgery

Morgan 1972,46 Cheng 1973,47 Toda 19919Sandhu 198950Saeian 199156Rothschild 1985,58 Lee 1988,59 Pattee 199260Searcy 1971,63 King SB IlIl 1971,64 Ryan 1977,65 Yu 1986,67Lee 1989,69 Shimizu 1993,62 Somsen 199430Meng 1985,70 Cherry 1987,7' lannone 1990,72 Grill 1991,73 Bata 1993,74El-Omar 199575

when sequential saphenous vein bypass grafts are

inadvertently anastomosed between coronary arteriesand cardiac veins. Furthermore, a fistula between theLAD-saphenous vein bypass graft and right ventriclewas reported ten years following CABG57 and a singleright coronary artery-pulmonary artery arteriovenousfistula was reported 16 years after surgical correctionof atrial septal defect.58

Also after mitral valve replacement, due to rightatrial artery injury, a postoperative fistula between a

right atrial artery and the right atrium (site ofaccess forcardiopulmonary bypass) has been described.59 Afterclosed commissurotomy, it has been demonstratedthat selective coronary angiography prior to surgicalintervention in patients with previous cardiac surgery

is useful since a fistula between the first diagonal arteryand the left lower pulmonary vein was recognisedoccurring 21 years after closed mitral valvulotomy.0Such a CAVF may also develop after septal myectomyfor hypertrophic obstructive cardiomyopathy.6' Bluntor sharp surgical traumas ofthe heart are held respon-sible for the induction of such fistulas in the absenceofbypass grafting.

Secondary to severe coronary atherosclerosis andcomplicating MlCAVFs may be a consequence of coronary athero-sclerosis especially in the presence ofsevere stenosis ortotal occlusion. Various mechanisms have been pro-

posed to explain the fistula formation in the presenceof severe narrowing and after myocardial infarction.Postulated mechanisms ofCAVF formation after MIare as follows:- New growth or dilatation ofarterioluminal vessels or

capillaries or anastomosis between Thebesian veins;62- Collateral channel formation stimulated by myo-

cardial hypoxia and reopening with anastomosis ofthe Thebesian veins,63-66Rupture of the proximal portion of the coronaryartery with extravasation and haematoma formationrupturing into a neighbouring cardiac vessel or

chamber;"- Growth ofnew vessels to a thrombus;62

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lst author/year/reference

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- Erosion of a localised cardiac chamber calcificationinto a coronary vessel."

It has been demonstrated angiographically and atautopsy that an acquired CAVF after MI haddeveloped from the diagonal branch ofthe LAD andhad communicated with the left ventricular cavity.62'67Phillips et al. described a CAVF from the LAD to thegreat cardiac vein detected on selective coronaryangiography following myocardial infarction.68 Leeand colleagues described a patient who developed acircumflex coronary artery fistula that communicatedwith a left ventricular false aneurysm after MI.69 Never-theless it remains difficult to differentiate, on clinical,electrocardiographic and angiographic grounds, be-tween congenital and acquired CAVFs detected afterMI 30,65

Complicating PTCA procedureslatrogenic CAVF formation is a very rare complicationof percutaneous transluminal coronary angioplasy(PTCA). This complication develops due to per-foration ofthe coronary artery during PTCA or ruptureofa false aneurysm into a cardiac chamber after PTCA.This complication has been reported with angioplastyto native coronary arteries70-74 and via a venous bypassgraft to the left anterior descending coronary artery.75

Findings at necropsyThe following findings have been recognised at post-mortem investigation: dilated epicardial coronaryarteries participating in the fistula formation andenlargement of cardiac chamber at which the fistulaterminates. Furthermore, vascular channels lined withendothelium communicating with the cardiac chamberhave been shown and left ventricular hypertrophyassociated with subendocardial fibrosis has also beenreported.76

At necropsy of a patient with congenital multiplecoronary artery-left ventricular fistulas Black andassociates found, on microscopic examination, thin-walled vascular channels lined by endothelium andcommunicating with the left ventricular lumen. The sizeofthese vessels ranged between 10 and 500 pm. Under-lying fibrous tissue was also present.76 Shimizu andcolleagues found during post-mortem examination ofa patient with an acquired CAVF post myocardialinfarction that the walls ofthe communicating vesselswere thick and the elastic membrane could be identified,confirming their arterial descent.62 Histologically, ithas been shown that the vessels participating in theformation of CAVFs have an arterial origin bydemonstrating a thick muscular media layer and a well-defined internal and external elastic membrane.77

Types of CAVFs

Anatomical typesThe individual anatomy ofthe fistula varies consider-

ably. Wearn et al. categorised CAVFs into threeanatomical types.78I. Arterioluminal type: Originates directly from the

coronary arteries to the lumen ofa heart chamber.They appeared to be more numerous in theventricles than in the atria.

II. Arteriosinusoidal type: From the coronary arteriesvia myocardial sinusoids into the lumen of aventricle. The communication is through themyocardial sinusoidal network.

III. Arteriocapillary type: The fistula drains into thecapillaries and then through the Thebesian systeminto a cardiac chamber.

Angiographic morphologySeveral angiographic dassifications ofCAVFs have beenreported. One ofthese divides CAVFs into two types:33Type 1: The fistula consists of one large channel orone or more small but discrete channels terminatinginto the pulmonary trunk.Type 2: The fistula is composed ofa plexiform networkofvessels.Another method classifies the disorder into five types.26

Associated lesionsAbout 20% ofpatients with CAVFs have an associatedcongenital cardiac anomaly. The commonest are aorticor pulmonary valvular atresia or patent ductus arterio-sus." In another series by Upshaw, associated con-genital cardiovascular defects were present in 34% ofthe patients.79 In various series, it has been reportedthat CAVFs may incidentally coexist with almost anycongenital or acquired disorder.808'

Cardiac lesions frequently associated with CAVFsThe association of patent ductus arteriosus (Botalli)with CAVFs has frequently been found.""2'79'81'82 Otherassociated cardiac lesions are pulmonary valvularatresia;"'79'8' aortic valvular atresia79'82 with reportedmortality shortly after birth;55 and ventricular or atrialseptal defect.79'8'

Cardiovascular lesions probably flstula-relatedassociated with CAVFsCAVFs have been associated with premature coronaryatherosclerosis 631,6,66,68,81 Bilateral CAVFs are rare andmultiple ones are even rarer.31'32'76'80'8387

Disorders incidentally coexisting with CAVFsAssociation ofCAVFs with congenital, rheumatic ordegenerative valvular disease have been reported.33M",88Mitral regurgitation secondary to papillary muscledysfunction has been described;46 as well as tetralogyof Fallot;46'82'89 asymmetric septal hypertrophy;26 andtricuspid valvular atresia.8' Furthermore, CAVFs havebeen reported incidentally in association with temporalarteritis,86 persistent left superior vena cava90 and inconcurrence with chronic myeloproliferative dis-order.9'

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The clinical picture of CAVFs

Asymptomatic presentationPatients with CAVFs are to a great extent asymptomatic.It has been reported that more than halfofthe patientswith CAVFs may be completely asymptomatic.92

Symptoms of complicationsUnless the CAVF is large enough to cause aconsiderable left-to-right shunt (Qp:Qs ratio>2), thisanomaly does not usually produce symptoms before theage of 30 years. It has been shown that fistulouscommunication between a coronary artery and acardiac chamber may cause anginal symptoms,although ECGs are normal.3' In patients with CAVFsno signs of redistribution on thallium-201 perfusionscintigraphy were found.93 The majority ofCAVFs arefound incidentally during coronary angiographicstudies. They produce no symptoms and show a benignlong-term course.'4 Fifty-nine percent ofpatients wereasymptomatic in the review ofRittenhouse in 1975.92

The reported symptoms of CAVFs are: anginapectoris, atypical chest pain, syncope, dizziness, fatigue,dyspnoea at rest and during exertion, palpitations,peripheral oedema and haemoptysis.9294 In the firsttwo decades of life, CAVFs hardly ever produce anysymptoms, but in adulthood they may be associatedwith an increased risk of complications giving rise todisorders such as congestive heart failure.9'90'95

Congestive heart failure (CHF) has been shown tobe a common cause ofdeath in untreated cases.96 CHFwas found in slightly more than fifty percent ofcases inthe series of Ogden.97 Cardiac failure in early infancywith a large size left-to-right shunt was reported byMcNamara" but CHF generally occurs after 30 yearsofage.95 In the series ofLiberthson and associates, itwasnoted that none of the symptomatic patients aged 20years and older had symptoms or complications beforethe age of30 years, although all were symptomatic afterthat age. Shunt size may still contribute to clinicalsequelae with advancing age since a significant differencein mean Qp/Qs (1.7:1 versus 1.4:1, p<0.05) has beenshown in a non-longitudinal study in older reportedpatientswho had neither symptoms nor complications.95Recurrent respiratory tract infections have been reportedin patients with CAVFs.3' Myocardial infarction has alsobeen reported in adults and children.'0'4680,82'98 Severalreports have included CAVF patients associated withatrial fibrillation. 11,126,84,0,99,10 Rarely, sudden death dueto rupture of an aneurysm95"10' was reported. Further-more, ventricular tachyarrhythmias'02 and atrioventri-cular valvular regurgitation46 have been postulated tobe subsequent to the CAVFs.

Physical examinationThe findings on physical examination are very variablein patients with a CAVF but it can be suspectedclinically when any or all of the following signs arepresent during physical examination.

Arterial and venous pressures: The pulse pressure maybe normal or widened. The jugular venous pressure isinitially normal and in later stages elevated in cases oflarge shunts to the right heart.

Continuous murmur: On physical examination, acontinuous murmur may be heard at an unusuallocation.82 In some cases the continuous murmur isabsent.'4 When the murmur is present, the location ofthe murmur is related to the drainage site ofthe fistula.When the fistula drains into the right atrium, thecontinuous murmur is best heard in the second andthird right intercostal parasternal areas. When entry isinto the right ventricle, the maximum continuousmurmur is located at the third, fourth and fifth leftintercostal spaces. When drainage into the pulmonaryartery occurs, the maximum point of the murmur isheard at the second or third left intercostal space.Differentiation by auscultation between the murmurofpatent ductus arteriosus and a CAVF draining intothe pulmonary artery is difficult.

Diagostic approachIn the past, the diagnosis of CAVFs was made onclinical grounds but because ofthe inaccuracy ofclinicaldiagnosis it was oflittle value. Furthermore, the clinicaldiagnosis is non-specific because none ofthe signs orsymptoms ofCAVFs are unique to this condition andall may be caused by other cardiac conditions.

CAVFs may cause small (Qp/Qs ratio <1.5) orlarge (Qp/Qs ratio (>2.0) left-to-right and rarely left-to-left (arterio-systemic) shunts. Most fistulas draininto the low-pressure right heart chambers, thecoronary sinus and the pulmonary artery, creating aleft-to-right shunt. This may result in right or leftventricular overload depending on the site of ter-mination of the CAVFs giving rise to exertionaldyspnoea, or overt congestive heart failure. Drainageinto the left atrium, the left ventricle and the bronchialcirculation (arterio-arterial shunt) is infrequent. Smallleft-to-right shunts are relatively common.'4 Thesignificance of such a communication depends uponthe magnitude and duration of shunting, whether ornot myocardial blood flow is affected by the shunt,and the presence or absence of coexisting cardiac orcoronary abnormalities. The left-to-right shunts aredifficult or impossible to detect. Coronary blood flowrepresents only 4 to 6% of the cardiac output, cor-responding to 280 to 420 rnl/min.

The shunts, small as they are, may however be animportant fraction of the total coronary blood flow.The volume of shunted blood may be considerable;actual measurements of 700 to 1800 ml/min havebeen taken during operations.'03 In 1978, Kiso et al.'04described a patient with right coronary-to-leftventricular fistula where intraoperative mean rightcoronary flow was recorded as 315 ml/min anddropped to 35 ml/min after repair of the fistula,suggesting that a large amount ofblood, around 280ml/min, was stolen by the fistula. The physiological

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effect of a coronary artery fistula depends on the sizeof the shunt, on the pressure gradient difference overthe shunt and on whether it empties into the left or theright side of the heart. When the fistula empties intothe left side or to the pulmonary trunk there is increasein volume load on the left ventricle. When the CAVFsterminate into the left ventricular cavity a haemo-dynamic pattern mimicking aortic regurgitation occurs.

Several non-invasive and invasive methods for thediagnosis of suspected CAVFs have been introducedin the past two decades.

Electrocardiography and roentgenographyIt is widely accepted that electrocardiography and chestroentgenography are not helpful in establishing thediagnosis.82'105 When the CAVF is large enough, chestX-ray shows the secondary haemodynamic changesincluding cardiac enlargement or increased pulmonaryvasculature, depending on the termination site. A largeCAVF could be suggested on chest X-ray."i6

CAVFs may rarely cause calcification on the chestX-ray. Intracardiac calcifications have been reportedin patients with CAVFs.107 A very rare radiographicfinding is that ofa localised excrescence on either heartborder.38

PhonocardiographyIn the seventies, phonocardiography was shown to beof great value in distinguishing CAVF from otheranomalies with a continuous murmur,l08 but this waschallenged by others.3'

Radionuclide exercise perfusion scanningMyocardial perfusion scan could not demonstrate areversible ischaemia or 'steal' phenomenon in patientswith CAVFs associated with atypical angina.2693 Oshiroand associates demonstrated the occurrence ofmultipleperfusion defects in a patient with multiple coronary-left ventricular fistulas in the presence of typicalangina.85 The occurrence of'coronary steal' phenom-enon in coronary artery-to-left ventricular fistula hasbeen previously documented by Cheng.'w

Doppler echocardiographyRecent reports have suggested the supplementary roleof several non-invasive techniques in the diagnosisand follow-up of these anomalies, such as Dopplerechocardiography, 1105 magnetic resonance imaging(MRI)36"'16 and transoesophageal echocardiography(TEE).90"17- 119 Echocardiographic diagnostic featuressuggestive for CAVFs are:- Demonstration of a dilated 'proximal' coronary

artery by two-dimensional echocardciography;- Assessment ofthe continuous flow turbulence in theinvolved drainage sites by pulsed Doppler echo-cardiography.

These diagnostic criteria, although widely accepted,are not well defined and therefore coronary arterydilatation from other causes should be differentiated

and recognised. Previous medical history may be ofimportance in such interpretation, especially whenpatients have coronary artery disease secondary toKawasaki's disease.""',20 In such a disease coronaryartery dilatation, aneurysms and/or obstructive lesionsmay occur.121,122

Indicator dilution techniquesQuerimit and his colleagues were the first to use theindicator-dilution technique to localise left-to-rightshunt in patients with CAVFs.123 Using this technique,they applied indocyanine green (Cardio-Green) as anindicator. Indicator-dilution curves were applied usingindocyanine green at a dose of0.06 mg/kg per injec-tion. The shunt was maximally visible after selectiveinjection ofthe dye into the suspected coronary arteryparticipating in the fistula formation.

Dye-dilution curves failed to differentiate patentarterial duct from CAVFs'05 and proved normal in theseries ofIskandrian and associates.33 Hydrogen studiesalso proved negative in the series of Iskandrian andassociates. Right heart catheterisation alone will notdisclose a coronary artery fistula to the left heart. Themagnitude ofthe shunt is often small and each shuntdetection technique has its limitations. The left-to-right shunts of CAVFs may be impossible to detect.Liberthson and colleagues95 and Urrutia-s et al.80 foundno statistically significant difference in the mean shuntsize between symptomatic and asymptomatic patients.

Selective coronary arteriographySelective coronary arteriography is considered to bethe 'gold standard' and cardiac catheterisation is theinvestigation ofchoice as these studies allow assessmentof haemodynamics, quantitation of the intracardiacshunt, delineation of the fistulous pathway and the

I

FE _I_Figure 3. Frame ofrightantriorobliqueprojection ofkft eoronayartery showingproximally ortginating LAD-PAfAisla (arrow).

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Figure 4. Frame ofkft lateral projection ofkft coronary arteyillustrating obtuse marginal-LVfistula (arrow).

entire anatomy of the coronary vessels. Coronaryangiography is essential for definite diagnosis ofCAVFs(figures 3 and 4). Coronary angiographic diagnosticfeatures suggestive for CAVFs are:- The coronary vessel involved in the congenital CAVFformation is usually tortuous and dilated;

- The contrast medium spurts through the fistula intothe affected cardiac chamber. The involved cardiacchamber may also be enlarged;

- Identifiable origin, pathway and termination ofthefistula.

It has been postulated that CAVFs are visualised onlybecause of the pressure of injection during selectivecoronary angiography and mayvery well be functional-ly closed at other times.3363 There is an importantlimitation with respect to the applicability of theangiographic diagnostic criteria. This limitation isrelated to technique and quality of coronary arterio-grams. Poor technique often results in incompletefilling of the coronary artery that may result inangiograms that do not provide sufficient informationto achieve an accurate diagnosis.

Differential diagnosisAll lesions associated with continuous cardiac murmurshould be considered. Generally, there are twomechanisms responsible for continuous murmurs:1. Abnormal vascular flow: may occur in either arteries

or veins.2. Translesional shunt flow: may be intracardiac or

extracardiac.The definition of a continuous murmur is a murmurbeginning in systole and extending through the secondheart sound into diastole. The differential diagnosis ofmost common causes ofa continuous murmur indudes:

In normal physiologic conditions: The venous hum isthe most frequent, innocuous and not associated withcirculatory disorders or symptoms. This murmur ischaracteristically louder in diastole and is obliteratedwhen the jugular vein is gently compressed. Themammary murmur is heard in about 15% ofpregnantwomen during the second or third trimester ofpregnancy.'24

In abnormal conditions: The diagnosis of coronaryarteriovenous fistula is important because it plays a rolein the differential diagnosis of cardiac disordersassociated with a continuous precordial murmur, suchas:'05 Patent ductus arteriosus (Botalli); rupturedaneurysm of a sinus of Valsalva into the right heart;supravalvular pulmonic stenosis; arteriovenous mal-formation of chest wall;6 aorta-right ventricle fistula;aorto-pulmonary fenestration (window); ventricularseptal defect with aortic regurgitation; arteriovenousfistula ofthe internal mammary vessels;'25",26 pulmonaryarteriovenous fistula;'27 anomalous pulmonary arteriesor veins;'28 and solid mediastinal mass.'29 Continuousmurmurs are rarely heard in solid tumours ofthe chest.

CAVFs should enter the differential diagnosis ofintracardiac calcifications, as calcified lesions have beenreported in association with CAVFs.'07

Prognosis and natural historySmall coronary arteriovenous fistulas have a benignnatural history.'4 The fate ofCAVFs, with or withoutaneurysmal formation, is still unknown, but spon-taneous regression ofcongenital and acquired fistulashas been reported.46'50 CAVFs may expose thrombosisand spontaneous closure'30'133 or may rarely rupturecausing hemopericardium and death.95"l0'

The natural history ofmost large CAVFs involvesthe development of a progressive dilatation andelongation ofthe affected coronary artery and the vesselor chambers receiving the shunted blood, as a resultof a progressive increase in blood flow.I05 It has beenreported that neighbouring intrathoracic structuresmay be obstructed secondary to massive dilatation ofthe recipient coronary artery or cardiac chamber.35'37 Onthe other end ofthe spectrum it has been shown thatCAVFs are compatible with longevity.40

Compilcatlons of CAVFsThe incidence offistula-related complications appearsto increase with older age groups.95 Several com-plications (intracardiac and extracardiac) have beenencountered in patients with CAVFs.

Excessive load to cardiac chambers- Chronic volume overload as a consequence of

intracardiac shunting can give rise to increased leftventricular end-diastolic pressure, left ventricularhypertrophy (LVH) and in older age groups tocongestive heart failure.90'95 Evidence ofLVH orstrain was most frequently noted regardless ofwhich

Netherlands Hcart Journal, Volume 10, Number 2, February 200272


cardiac chamber the fistula drained into. Electro-cardiographical changes of right or left ventricularoverload were noted in 61% of patients withCAVFs."1

- Massive dilatation ofthe recipient cardiac chambercould lead to mechanical interference with the car-diac function.35137 Floyd35 described a case of giantatriomegaly subsequent to right coronary artery-leftatrial fistula causing distortion of the heart andincomplete obstruction of the inferior vena cava.Rein and associates37 described a four-year-old girlwith congenital right coronary artery-right atrialfistula and infective endocarditis with concurrentunexplained facial swelling. Echocardiography wasable to demonstrate the giant fistula causingobstruction of the distal superior vena cava. Thefistula was successfully ligated.

- Cardiac rhythm disturbances: Atrial fibrillation andventricular tachyarrhythmias have been associatedwith CAVFs. 11,12,26,84,90,92,99,102 Atrial fibrillation is fre-quently seen in older patients with CAVFs and mayresult in congestive heart failure when it occurs.'07

Coronary complications- Ipsilateral myocardial infarction in children and

adults: 0,46,80,82,92'98"34 In 1972, Morgan and asso-ciates46 were among the first to describe electro-cardiographic evidence ofinfarction in children withCAVFs.

- 'Coronary steal' producing myocardial ischaemiadue to diversion of blood from the high-resistancecapillary bed to the low-resistance fistula seems tooccur much less commonly than expected.

- Mechanical interference secondary to massiveaneurysmal enlargement of recipient coronaryartery:34-37 Dilatation of the coronary artery par-ticipating in the CAVFs varies significantly. CAVFscan be complicated by enormous aneurysmaldilatation of the coronary artery (8-10 cm indiameter and 26 gram total weight), which mayappear as a mediastinal mass.34 In 1958, Edwards8suggested that aneurysmal dilatation results fromstructural weakening of the vessel wall due toexcessive blood flow through the CAVFs.

- Premature coronary atherosclerosis:'692 It is thoughtthat the shear-induced intimal damage, as a resultofhigh flow through the fistula-related vessel, mayform a substrate for the development ofprematurecoronary atherosclerotic lesions.

Valvular and endocardial complications- Valvular regurgitation secondary to papillary muscledysfinction has been described in children and adultswith CAVFs.46

- Infective endocarditis: In 1962 Lee and colleagues'35demonstrated experimentally in dogs that thepresence ofan arteriovenous fistula not only rendersthe animal more susceptible to bacteraemia but alsotends to prolong the bacteraemia and lengthen the

time needed for effective antibiotic therapy.'35Infective endocarditis is a real complication ofcoronary arteriovenous fistulas, with an incidencevarying from 0% to 12%.9, 1,95,96 Consequently, afterthe fistula is detected, endocarditis prophylaxisshould be recommended in these patients.

Extracardiac complications- Haemopericardium secondary to rupture of an as-

sociated aneurysm:95"l0' Fistula dissection and ruptureare rare in CAVFs. Habermann and colleagues havereported a single case of sudden cardiac deathsecondary to rupture ofCAVF in an adult in 1963.

- Moderate pulmonary hypertension: This has beenreported in literature in only few patients especiallywhen the left-to-right shunt magnitude is consider-able. 11,13,36,95

Treatment and management of CAVFsAs soon as the diagnosis is established, antibioticsshould be given as prophylaxis against subacutebacterial endocarditis (flow-chart, table 4).

Conservative approachAsymptomatic patients with small shunts should betreated conservatively,'25 since small fistulas appear tohave a relatively benign natural history.'4 CAVFs mayremain asymptomatic for decades and they may closespontaneously.'3' This spontaneous obliteration oftheCAVFs establishes a rationale for clinical observationin such patients. But periodical non-invasive analysisremains recommended to establish any regression orprogression ofthe CAVFs.

Surgical approachBiorck and Crafoord performed the first successfulligation in 1947.20 It is generally agreed that CAVFswith large left-to-right shunt (Qp:Qs ratio (>2) shouldbe treated, depending on the type, size and localisationof shunt, either surgically or using a percutaneoustranscatheter embolisation technique. Patients shouldbe selected for operation according to the magnitude ofthe left-to-right shunt, symptoms andECG changes.'25It has been reported that surgical treatment has resultedin a low mortality from 0 to 4% and morbidity from 10to 15%.915,809295 It has been suggested that the best agegroup for operative repair ofthese CAVFs is between 10and 45 years. Operative correction in patients youngerthan 10 years or older than 45 years ofage is probablycoupled with an increased risk of morbidity andmortality.79'95 In a review carried out by McNamara etal. through 1967, 57% of all reviewed cases (93/163)were treated surgically. In these 93 operated patientsonly three (3/93) operative deaths were reported.

Non-surgical approachPharmacological: Therapy with f-blockers has beensuccessfillly established in patients with coronaryarterio-arterial and arterio-venous fistas. 3637

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Table 4. Row-chart of treatment of CAVFs (future perspective)

C A V F

When discovered

Congenital or acquired

Subacute bacterial endocarditis prophylaxis

SHUNT

SmallLarge

Symptomatic or asymptomatic

Treatment

- Surgical ligation- Non-surgical embolisation- Pharmacological* Beta blocking agents* Calcium channel antagonists

T imTreatment

Reevaluation

Also calcium channel blockers are reported to beeffective.'38 Improving and counterbalancing thediminished coronary blood oxygen supply in relationto the myocardial blood demand probably producesthese effects. These types oftherapy, which reduce themyocardial oxygen demand, are recommendedespecially when surgical repair seems to be technicallyimpossible. These therapeutic modalities, however,have never been tested in a randomised trial.

Percutaneous transcatheter embolisation techniques(detachable balloon, microcoils, embolisation partides(or microspheres): Although several authors believe thatCAVFs should be repairedwhen diagnosed,"',38,95108 therole of surgery in asymptomatic patients with CAVFs

Qp/Qs ratio of <1.5

Symptomatic asymptomatic

I4

Close follow-upTM

Periodical examination* Physical examination* ECG* Echocardiography* Exercise testing

Symptomatic Disorders

remains to be defined. The generally small size of thefistulas, and the tendency for spontaneous dosure arguefor nonsurgical management.50"130-133 Not only successfilclosure of CAVFs using transcatheter embolisationtechniques has been reported93"39 142 but also un-

successfil procedures have been described occurring inan octogenarian.'43

Surgical indicationsThe indication for operation depends on:1. Fistula-related indications: The site and type oftheCAVFs; magnitude ofthe left-to-right shunt (Qp:Qs>2.0);92 and the degree of dilatation of the re-

cipient coronary artery or cardiac chamber.

Nethcriands Heart Journal, Volume 10, Number 2, February 2002

Qp/Qs ratio of .2.0

74


2. Symptomatic reliefofchest pain or congestive heartfailure in the absence of other causes in patientswith large left-to-right shunt (Qp: Qs>2 .0)1177

3. Prevention of development of future complica-tions: Congestive heart failure, pulmonary hyper-tension,"'79 coronary insufficiency,97 and rupture ofan associated aneurysm.95"10'

4. Prevention of bacterial endocarditis.5. Prevention of eventual mechanical obstruction or

mechanical interference with cardiac function.

ConclusionCongenital coronary artery fistulas are intriguingentities with unsolved aetiological issues. They possessdifferent angiographic morphological spectra varyingbetween discrete single channels and multiple serpigin-ous network ofvessels. Antibiotic prophylaxis againstendocarditis for patients with CAVFs is advised. Forpatients with symptomatic CAVFs, individualisedsurgical or interventional procedures, depending onthe anatomy of the fistula and concomitant heartdisease, are chosen. Pharmacological treatment isreserved for 'symptomatic' small CAVFs shunts orinoperable cases. -

Abbreviations and acronymsAVM=arteriovenous malformationCAF=coronary artery fistulaCAG=coronary angiographyCAVF=coronary arteriovenous fistulaCC=cardiac chamberCHF=congestive heart failureCS=coronary sinusCV=cardiac veinIE=infective endocarditisIVC=inferior vena cavaLA=left atriumLAD=left anterior descending coronary arteryLV=left ventricleLVH=left ventricular hypertrophyMI=myocardial infarctionMIBI=Technetium-99m methoxy isobutyl isonitrileMRI=magnetic resonance imagingPA=pulmonary arteryPDA=patent ductus arteriosus (Botalli)PTCA=percutaneous transluminal coronary angio-plastyPTE=percutaneous transcatheter embolisationRA=right atriumRV=right ventricleSBE=subacute bacterial endocarditisSIN=cardiac sinusoidsSVC=superior vena cavaTEE=transoesophageal echocardiographyTV=Thebesian veins

References

1 Salo JA, Ketonen PS. Congenital arteriovenous fistula in the chestwall. ScandJ Thor Cardiovasc Sur,g 1988;22:7-1O.

2 Szilagyi DE, Elliott JP, DeRusso FJ, Smith RF. Peripheral con-genital arteriovenous fistulas. Surgery 1965;57:61-81.

3 VoUlmar JF, Stalker CG. The surgical treatment of congenital ar-teriovenous fistulas in the extremities. J Cardiovasc Surg1976;17:340-7.

4 Baim DS, Grossman W. Percutaneous approach and transseptalcatheterization. In: Cardiac catheterization and angiography, 3dedition. Philadelphia: Lea & Febigger, 1986:59-75.

5 Waksman R, King SB 3rd, Douglas JS, Shen Y, Ewing H, Muel-ler L, Ghazzal ZM, et al. Predictors of groin complications afterballoon and new-device coronary intervention. Am J Cardiol1995;75:886.

6 Said SAM, Bloemendaal K Successful venous coronary artery by-pass grafting in association with congenital arteriovenous malfor-mation of the chest wall and left upper extremity. Cardiologie1996;3:151-3.

7 Levin DC, Fellows KE, Abrams HL. Hemodynamically significantprimary anomalies of the coronary arteries. Angiographic aspects.Circulation 1978;58:25-34.

8 Edwards JE. Anomalous coronary arteries with special reference toarteriovenous-like communications. Circulation 1958;17:1001-6.

9 Wide P, Watt I. Congenital coronary artery fistulae: six new caseswith a collective review. Clin Radiol 1980;31:301-11.

10 St John Sutton MG, Miller GAH, Kerr IH, Traill TA. Coronaryartery steal via large coronary artery to bronchial artery anastomosissuccessfully treated by operation. Br HeartJ 1980;44:460-3.

11 McNamara JJ, Gross RE. Congenital coronary artery fistula. Sur-gery 1969;65:59-69.

12 Sakakibara S, Yokoyama M, Takao A, Nogi M, Gomi H. Coronaryarteriovenous fistula. Am HeartJ 1966;72:307-14.

13 Davison PH, McCracken BH, McIlveen DJ. Congenital coronaryarteriovenous aneurysm. Br Heartj 1955;17:569-62.

14 Yamanaka 0, Hobbs RE. Coronary artery anomalies in 126,595patients undergoing coronary arteriography. Cathet CardiovascDiagn 1990;21:28-40.

15 Kirklin JW, Barratt-Boyes BG. Cardiac surgery 2d edition. Chur-chill Livingstone, 1167-93.

16 Said SAM, Geeraedts LGM. Ventriculo-venous communicationsin adults: Ventriculographic observations in two female patients.IntJ Cardiol 1997;62:161-5.

17 Wenger NK Rare causes of coronary artery disease. In Hurst JW(ed): The Heart. New York, McGraw-Hill, 1978:1348-9.

18 Krause W. Uber den Ursprung einer akzessorischen A. coronanaaus der A. pulmonalis. ZRationell Med 1865;24:225-7.

19 Trevor RS. Aneurysm of the descending branch of the right cor-onary artery situated in the wall ofthe right ventricle and openinginto the cavity of the ventricle, associated with great dilatation ofthe right coronary artery and non-valvular infective endocarditis.Proceedings of the Royal Society ofMedicine 1912;5:20-6.

20 Biorck G, Crafoord C. Arteriovenous aneurysm on the pulmon-ary artery simulating patent ductus arteriosus botalli. Thorax1947;2: 65-74.

21 Munkner T, Petersen 0, Vesterdal J. Congenital aneurysm of thecoronary artery with an arteriovenous fistula. Acta Radiologica1958;50:333-40.

22 Kimbiris D, Dasparian H, Knibbe P, Brest AN. Coronary artery-coronary sinus fistula. AmJ Cardiol 1970;26:532-9.

23 Huffman T, Leighton RF, Goodwin RS, Ryan JM, Wooly CF.Continuous murmurs associated with shunts in the acyanotic adult:an anatomic classification. AmiMed 1970;49:160-9.

24 Rohmer J. In aangeboren hartafwijkingen. Arntzenius AC, Mou-laert AJMG, eds. Bunge, 1986.

25 Bogers AJJC. Congenital coronary artery anomalies: clinical andembryological aspects. Thesis, Leiden, 1989.

26 Gillebert C, HoofR van, Werf F van de, Piessens J, Geest H de.Coronary artery fistula in an adult population. EurHeartJ1986;7:437-43.

27 Aelfers EWM, Huige MC. Coronairfistels: een opmerkelijke toe-valsbevinding. MedischJournaal 1992;4:220-2.

28 Tiraboschi R, Salomone G, Napoleone A, Bande A, Valsecchi 0,Carminati M, et al. Congenital coronary fistulae. Comments on 9surgical cases. G Ital Cardiol 1988;18:104-8.

29 Toda S, Nakamura A, Iwamoto T, Nakaji S. Successful surgicaltreatment of aortic regurgitation with coronary artery fistula dueto blunt chest trauma. Acase report. JJpn Assoc Thorac Surg 1991;39:1087-92.

Netherlands Heart Jounal, Volume 10, Number 2, February 2002 75


30 Somsen GA, Liem KS. Coronary artery-left ventricular fistulasprobably due to transmural myocardial infarction: a case report.Cardiologie 1994;1:65-7.

31 Eie H, Hillestad L. Arterio-venous fistulae ofthe coronary arteries.A report of six cases. ScandjJ Thor Cardiovasc Surg 1971;5:34-8.

32 Goebel N von, Gander MP, Steinbrunn W. Small coronary arteryfistulae. Ann Radiol 1979;22:277-9.

33 Iskandrian AS, Kimbiris D, Bemis CE, Segal BL. Coronary arteryto pulmonary artery fistulas. Am HeartJ 1978;96:605-9.

34 Meyer MH, Stephenson HE, Ketas TE, Martt JM. Coronary ar-tery resection for giant aneurysmal enlargement of arteriovenousfistula. Am HeartJ 1967;74:603-13.

35 Floyd WL, Young WG, Johnsrude IS. Coronary arterial-left atrialfistula: Case with obstruction of the inferior vena cava by a giantleft atrium. Am J Cardiol 1970;25:716-22.

36 Wertheimer JH, Toto A, Goldman A, DeGroat T, Scanlon M,Nakhjavan FK, Kotler M. Magnetic resonance imaging and two-dimensional and Doppler echocardiography in the diagnosis ofco-ronary cameral fistula. Am HeartJ 1987;114:159-62.

37 Rein AJJ, Yatsiv I, Simcha A. An unusual presentation oftight cor-onary artery fistula. Br HeartJ 1988;59:598-600.

38 Gasul BM, Arcilla RA, Fell EH, Lynfield J, BicoffJP, Luan LL.Congenital coronary arteriovenous fistula. Clinical, phonocardio-graphic, angiocardiographic and hemodynamic studies in five pa-tients. Pediatrics 1960;25:531-60.

39 Lester RG. Congenital communication of a coronary artery witha cardiac chamber or the pulmonary trunk. Circulation 1961;24:171-9.

40 Williams RR, Kent GB, Edwards JE. Anomalous cardiac bloodves-sel communicating with the right ventride: observations in a caseofpulmonary atresia with an intact ventricular septum. Arch Pathol1951;52:480-7.

41 Sissman NJ, Abrams HL. Bidirectional shunting in a coronary ar-tery-right ventricular fistula associated with pulmonary atresia andan intact ventricular septum. Circ 1965;32:582-8.

42 Dusek J, Ostadal B, Duskova M. Postnatal persistence of spongymyocardium with embryonic blood supply. Arch Pathol 1975;99:312-7.

43 Mikawa T, Fischman DA. Retroviral analysis of cardiac morpho-genesis: Discontinuous formation of coronary vessels. Proc NatlAcad Sci USA 1992;89:9504-8.

44 Hutchins G, Abigail KH, Moore GW. Development of the cor-onary arteries in the embryonic human heart. Circ 1988;77(6):1250-7.

45 Vrancke Peeters MPFM, Gittenberg-de Groot AC, MentinkMMT, Hungerford JE, Little CD, Poelmann RE. Differences indevelopment of coronary vessels and differentiation into arteriesand veins in the embryonic quail heart. Cardiovascular Research1997;36:101-10.

46 Morgan JR, Forker AD, O'Sullivan Jr MJ, Fosburg RG. Coron-ary arterial fistulas. Seven cases with unusual features. AmJ Car-diol 1972;30:432-6.

47 Cheng TO, Adkins PC. Traumatic aneurysm of left anterior des-cending coronary artery with fistulous opening into left ventricleand left ventricular aneurysm after stab wound of chest. Report ofcase with successful surgical repair. AmJCardiol 1973;31:384-90.

48 Jones RC, Jahnke EJ. Coronary artery atrioventricular fistula andventricular septal defect due to penetrating wound of the heart.Circ 1965;32:995-1000.

49 Tsagaris RJ, Bustamante RA. Coronary arteriovenous fistula andmyocardial infarction due to trauma. AmJCardiol 1966;18:777-80.

50 Sandhu JS, Uretsky BF, Zerbe TR, Goldsmith AS, Reddy S, Kor-mos RL, et al. Coronary artery fistula in the heart transplant pa-tient. A potential complication of endomyocardial biopsy. Cir-culation 1989;79:350-6.

51 Henzlova MJ, Nath H, Bucy RP, Bourge RC, Kirklin JK, RogersWJ. Coronary artery to right ventricle fistula in heart transplantrecipients. JAm Coll Cardiol 1989;14:258-61.

52 Sutsch G, Heywood T, Turina J, Buchi M, Schneider J, GallinoA, et al. Coronary artery - right ventricular fistula in a heart trans-plant patient. JHeart Transplant 1990;9:32-5.

53 Yeoh JK, Anderson ST, Federman J, Esmore D. Coronary arteryto middle cardiac vein fistula following endocardial biopsy in a hearttransplant patient. Cathet cardiovasc Diagn 1991;24:108-10.

54 Uchida N, Baudet E, Roques X, laborde N, Biles MA. Surgical ex-

perience ofcoronary artery-right ventricular fistula in a heart trans-plant patient. EurJCardiothorac Surg 1995;9:106-8.

55 Furniss SS, Mitchell L, Kitipawong P. Coil embolization of a cor-onary fistula in a post-transplant patient. Eur HeartJ 1995;16:1147-8.

56 Saeian K, Vellinga T, Troup P, Wetherbee J. Coronary artery fistulaformation secondary to permanent pacemaker placement. Chest1991;99:780-1.

57 Riahi M, Stone KS, Hanni CL, Fierens E, Dean RE. Right ven-tricular-saphenous vein graft fistula. J Thorac Cardiovasc Surg1984;87:628-8.

58 Rothschild AH, Adatepe MH, Magovem GJ, Rothschild MA, Joy-ner CR Right coronary artery-pulmonary artery arteriovenousfistula secondary to open heart surgery. JAm Coll Cardiol 1985;6:933-6.

59 Lee RT, Mudge GH, Colucci WS. Coronary artery fistula aftermitral valve surgery. Am HeartJ 1988;5:1128-30.

60 Pattee PL, Chambers RJ. Acquired postoperative coronary ar-teriovenous fistula. Cathet Cardiovasc Diagn 1992;26:140-2.

61 Chenzbraun A, Pinto FJ, Meyer B, Stinson EB, Popp RL. Fre-quency of acquired coronary-cameral fistula after ventricular sep-tal myectomy in hypertrophic cardiomyopathy. Am J Cardiol1993;71:1244-6.

62 Shimizu M, Yoshio H, Ino H, Takeda R, Okada Y. Histopatho-logic findings of a left coronary artery fistula to the left ventricleafter myocardial infarction. Cardiology in the Elderly 1993;1:335-6.

63 Searcy RA, Stein PD, Ganesan G, Bruce TA. Arterio-atrial shunt-ing in coronary atherosclerosis. Chest 1971;59:398-401.

64 King SB III, Schoonmaker FW. Coronary artery to left atrial fistulain association with severe atherosclerosis and mitral stenosis: Re-port of surgical repair. Chest 1975;67:361-3.

65 Ryan C, Gertz EW. Fistula from coronary arteries to the left ven-tricle after myocardial infarction. Br HeartJ 1977;39:1147-9.

66 Ray SG, Cowan MD, Kennedy JA. Spontaneously acquired fistulafrom the right coronary artery to the right ventricular cavity. BrHeartJ 1992;67:323-4.

67 Yu R, Sharma B, Franciosa JA. Acquired coronary artery fistula tothe left ventricle after acute myocardial infarction. AmJ Cardiol1986;58:557-8.

68 Phillips PA, LibanoffAJ. Arteriovenous communication associatedwith obstructive arteriosclerotic coronary artery disease and myo-cardial infarction. Chest 1974;65:106-8.

69 Lee KMH, Pichard AD, Lindsay J Jr. Acquired coronary artery-leftventricular pseudoaneurysm fistula after myocardial infarction. AmJCardiol 1989;64:824-5.

70 Meng RL, Harlan JL. Left anterior descending coronary artery-right ventricle fistula complicating percutaneous transluminalangioplasty. JThorac Cardiovasc Surg 1985;90:387-90.

71 Cherry S, Vandormael M. Rupture of a coronary artery and hem-orrhage into the ventricular cavity during coronary angioplasty.Am HeartJ1987;113:386-8.

72 lannone LA, Iannone DP. Iatrogenic left coronary artery fistula-to-left ventricle following PTCA: A previously unreported com-plication with nonsurgical management. Am Heart J 1990;5:1215-7.

73 Grill HP, Chew PH, Weiss JL, Merillat JC, Hill G, Cadden J, et al.Contrast echocardiographic diagnosis ofPTCA-induced coronaryartery-left ventricle fistula. AmJ Cardiol 1991;121:194-8.

74 Bata IR, MacDonald RG, O'Neill BJ. Coronary artery fistula as acomplication of percutaneous transluminal coronary angioplasty.CanJCardiol 1993;9:331-5.

75 El-Omar MM, Hargreaves MR, Venkataraman A, Been M. Cor-onary ventricular fistula as a complication ofPTCA: A case reportand literature review. IntJCardiol 1995;51:113-6.

76 Black IW, Loo CKC, Allan RM. Multiple coronary artery-left ven-tricular fistulae: Clinical, angiographic, and pathological findings.Cathet Cardiovasc Diagn 1991;23:133-5.

77 Gobel FL, Anderson CF, Baltaxe HA, Amplatz K,Wang Y. Shuntsbetween the coronary and pulmonary arteries with normal originof the coronary arteries. AmJCardiol 1970;25:655-61.

78 Weam JT, Mettier SR, Klumpp TG, Zschiescho LJ. The natureof the vascular communication between the coronary arteries andthe chambers ofthe heart. Am HeartJ1933;9:143-9.

79 Upshaw CB Jr. Congenital coronary arteriovenous fistula. Reportofa case with an analysis ofseventy-three reported cases. Am HeartJ 1962;63:399-404.

76 Netherlands Hcart Journal, Volumc 10, Number 2, February 2002


80 Urrutia-s CO, Falaschi G, Ott DA, Cooly DA. Surgical manage-ment of 56 patients with congenital coronary artery fistulas. AnnThorac Surg 1983;35:300-7.

81 Bogers AJJC, Quaegebeur JM, Huysmans HA. Early and lateresults of surgical treatment of congenital coronary artery fistula.Thorax 1987;42:369-73.

82 NefJJE de, Varghese PJ, Losekoot G. Congenital coronary arteryfistula. Analysis of 17 cases. BrHeartJ 1971;33:857-62.

83 Martens J, Haseldoncks C, WerfF van der, Geest H de. Silent leftand right coronary-left ventricular fistulas: an unusual prominentThebesian system. Acta Cardiol 1983;38:139-42.

84 Singham KT, Anuar M. Left coronary to pulmonary artery fistula.AustralasRadiol 1988;32;385-6.

85 Oshiro H, Shimabukuro M, Nakada Y, Chibana T, Yoshida H, Na-gamine F, et al. Multiple coronary LV fistulas: demonstration ofcoronary steal phenomenon by stress thallium scintigraphy andexercise hemodynamics. Am HeartJ1990;120:217-9.

86 Cross SJ, Lee HS, Jennings KP. Two coronary artery fistulae in apatient with temporal arteritis and chest pain. Scot MedJ 1991;36:117-8.

87 Podolsky L, Ledley GS, Goldstein J, Kotler MN, Yazdanfar S. Bi-lateral coronary artery to left ventricular fistulas. Cathet CardiovascDiagn 1991;24:271-3.

88 Baltaxe HA, Wixson D. The incidence ofcongenital anomalies ofthe coronary arteries in the adult population. Radiology 1977;122:47-52.

89 Saxena A, Sharma S, Shrivastava S. Coronary arteriovenous fistulain tetralogy of Fallot: an unusual association. IntJ Cardiol 1990;28:373-4.

90 Kugelmass AD, Manning WJ, Piana RN, Weintraub RM, Baim S,Grossman W. Coronary arteriovenous fistula presenting as con-gestive heart failure. Cathet Cardiovasc Diagn 1992;26;19-25.

91 Ho YL, Chen WJ,Wu CC, Lee YT. Acute myocardial infarction ina case of myelofibrosis with patent coronary arteries and arterio-venous fistulae draining into the main pulmonary artery. IntJ Car-diol 1994;46:49-51.

92 Rittenhouse EA, Doty DB, Ehrenhaft JL. Congenital coronaryartery-cardiac chamber fistula. Review of operative management.Ann Thorac Surg 1975;20:468-85.

93 Reidy JF, Anjos RT, Qureshi SA, Baker EJ, Tynan MJ. Trans-catheter embolization in the treatment ofcoronary artery fistulas.JAm Coll Cardiol 1991;18:187-92.

94 Senac JP, Adda M, Molina L, Thevenet A, Puech P, Grolleau RCommunications anormales entre arteres coronaires et branchesperipheriques des vaisseaux pulmonaires. Apropos de deux cas.Ann Radiol 1979;22:280-4.

95 Liberthson RR, Sagar K, Berkoben JP, Weintraub RM, Levine FH.Congenital coronary arteriovenous fistula. Report of 13 patients,review ofthe literature and delineation ofmanagement. Circula-tion 1979;59:849-54.

96 Ogden JA, Stansel HC. Coronary arterial fistulas terminating inthe coronary venous system. J Thorac Cardiovasc Surg 1972;63:172-82.

97 Ogden JA. Congenital variations ofthe coronary arteries. Thesis,Yale University, School ofMedicine, 1968.

98 Shirai K, Ogawa M, Kawaguchi H, Kawano T, Nakashima Y, Ara-kawa K Acute myocardial infarction due to thrombus formationin congenital coronary artery fistula. EurHeartJ1994;15:577-9.

99 Brack MJ, Hubner PJB, Firmin RK Successful operation on a co-ronary arteriovenous fistula in a 74-year-old woman. Br HeartJ1991;65;107-8.

100 Glynn TP, Fleming RG, Haist JL, Hunteman RK Coronary ar-teriovenous fistula as a cause for reversible thallium-201 perfusiondefect. i Nucl Med 1994;35:1808-10.

101 Habermann JH, Howard ML, Johnson ES. Rupture of the cor-onary sinus with hemopericardium: a rare complication ofcoronaryarteriovenous fistula. Circulation 1963;28:1143-4.

102 Moro-Serrano C, Martinez J, Madrid AH, Rufilanchas JJ, NovoL, Huerta EM, et al. Ventricular tachycardia ih a patient with con-genital coronary arteriovenous fistula. Am HeartJ1992;124:503-5.

103 Hudspeth AS, Linder JH. Congenital coronary arteriovenousfistula. Arch Surg 1968;96:832-5.

104 Kiso I, Itoh T, Morishita M, Kato K, Ishikura Y. Blood flow andpressure measurements ofright coronary artery to left ventricularfistula. Thorax 1978;33:253-6.

105 Edis AJ, Schattenberg TIT, Feldt RH, Danielson GK Congenitalcoronary artery fistula. Surgical considerations and results of op-eration. Mayo Clin Proc 1972;47:567-71.

106 Takeda K, Okuda Y, Matsumura K, Sakuma H, Tagami T, Naka-gawa T. Giant fistula between the right coronary artery and the leftventricle: diagnostic significance of right posterior oblique chestradiograph. AmjRoentgenol 1992;159:1087-90.

107 Colbeck JC, Shaw JM. Coronary aneurysm with arteriovenousfistula. Am HeartJ1954;48:270.

108 Roos JP, Hartman H, Schaar H van der, Brom AG. Diagnosis andsurgical treatment ofcoronary artery fistula. Thorax 1970;25:259-66.

109 Cheng TO. Left coronary artery-to-left ventricular fistula: Dem-onstration of coronary steal phenomenon. Am HeartJ 1982;104:870-2.

110 Rodgers DM, WolfNM, Barrett MJ, Zuckerman GL, Meister G.Two-dimensional echocardiographic features ofcoronary arterio-venous fistula. Am HeartJ1982:104:872-4.

111 Yoshikawa J, Yanagihara K, Owaki T, Kato H, Takagi Y, Okuma-chi F, et al. Cross-sectional echocardiographic diagnosis ofcoronaryartery aneurysms in patients with the mucocutaneous lymph nodesyndrome. Circulation 1979;59:133-9.

112 Chen CC, Hwang B, Hsiung MC, Chiang BN, Meng LC, WangDJ, et al. Recognition of coronary arterial fistula by Doppler 2-dimensional echocardiography. AmJ Cardiol 1984;53:392-4.

113 Oliver JM, Lopes de Sa E, Dominguez F, Sobrino JA, Munoz JE,Iglesias A. Congenital right coronary artery-to-left atrium fistuladetected by two-dimensional and Doppler echocardiography. AmHeartJ 1987;114:165-6.

114 Bahl VK, Shrivastava S. Non-invasive diagnosis of congenital cor-onary arteriovenous fistula by cross-sectional and Doppler echo-cardiography. IntJcardiol 1987;17:89-91.

115 Yoshikawa J, Kato H, Yanagihara K, Takagi Y, Okumachi F, Yos-hida K, et al. Noninvasive visualization ofthe dilated main coronaryarteries in coronary artery fistulas by cross-sectional echocardio-graphy. Circulation 1982;65:600-3.

116 Kubota S, Suzuki T, Murata K Cinemagnetic resonance imagingfor diagnosis of right coronary arterial-ventricular fistula. Chest1991;100:735-7.

117 Chen YT, Lee YS, Kan MN, Chen JS, Hu WS, Lin WW, et al.Transesophageal echocardiographyin adultswith a continuous pre-cordial murmur. IntJ Cardiol 1992;36:61-8.

118 Fernandes F, Alam M, Smith S, Khaja F. The role of transesopha-geal echocardiography in identifying anomalous coronary arteries.Circ 1993;88:2532-40.

119 Giannacro PJ, Sochowski RA, Morton BC, Chan KL. Comple-mentary role of transesophageal echocardiography to coronaryangiography in the assessment of coronary artery anomalies. BrHeartJ 1993;70:70-4.

120 Kawasaki T. Acute febrile mucocutaneous syndrome with specificdesquamation ofthe fingers and toes.JpnJAlergy 1967;16:168-222.

121 Nakanishi T, TakaoA, Nakazawa M, Endo M, Niwa K, TakahashiY. Mucocutaneous lymph node syndrome: clinical, hemodynamicand angiographic features of coronary obstructive disease. Am JCardiol 1985;55:662-8.

122 Said SAM, Veerbeek A, Werner HA, Herweyer TJ, SchuilenburgRM. Echocardiographic visualization ofcoronary aneurysms in themucocutaneous lymph node syndrome 'Kawasaki disease'. NethJCardiol 1991;4:92-7.

123 Querimit AS, Rowe GG. Localization of coronary arteriovenousfistula by indicator-dilution curves. AmJCardiol 1971;27:114-9.

124 Tabatznik B, Randall TW, Hersch C. The mammary souffle ofpregnancy and lactation. Circ 1960;22:1069-73.

125 Reed WA, Kittle CF. Congenital coronary artery fistula. Indica-tions for operative treatment. Arch Surg 1966;93:772-5.

126 Boontje AH, Kruyswijk HH. Ateriovenous fistula of the internalmammary vessels. JIhorac Cardiovasc Surg 1971;62:618-23.

127 Moyer JH, Glantz G, Brest AN. Pulmonary arteriovenous fistulas:physiologic and clinical considerations. AmJMed 1962;32:417-35.

128 Craige E, Millward DE. Diastolic and continuous murmurs. ProgCardiovasc Dis 1971;14:38-56.

129 Cooke M, Wolk PJ, Cheitlin MD. Mediastinal tumor causing con-tinuous murmur. Am HeartJ 1984;107:1282-4.

130 Jaffe RB, Glancy DL, Epstein SE, Brown BG, Morrow AF. Cor-onary artery right heart fistula: Long term observations in seven pa-tients. Circulation 1973;47:133-43.

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131 Griffiths SP, Ellis K, HordofAJ, Martin E, Levine OR, GersonyWM. Spontaneous complete closure ofa congenital coronary arteryfistula. JAm Coll Cardiol 1983;73:1169-73.

132 Hackett D, Hallidie-Smith KA. Spontaneous closure of coronaryartery fistula. Br Heart] 1984;52:477-9.

133 Roughneen PT, Bhattacharjee M, Morris PT, Nasser M, Reul GJ.Spontaneous thrombosis in a coronary artery fistula with aneurys-mal dilatation ofthe sinus ofValsalva. Ann Thorac Surg 1994;57:232-4.

134 Bishop JO, Mathur VS, Guinn GA. Congenital coronary artery fis-tula with myocardial infarction. Chest 1974;65:233-4.

135 Lee SH, Fisher B, Fisher ER, Little A. Arteriovenous fistula andbacterial endocarditis. Surgery 1962;52:463.

136 Sheikhzadeh A, Stierle U, Langbehn AF, Thoran P, Diederich KW.Generalized coronary arterio-systemic (left ventricular) fistula: Casereport and review ofliterature. Jpn HeartJ 1986;27:533-44.

137 Duckworth F, Mukharji J, Vetrovec GW. Diffuse coronary arteryto left ventricular communications: An unusual cause of demon-strable ischemia. Cathet Cardiovasc Diagn 1987;13:133-7.

138 McLellan BA, Pelikan PCD. Myocardial infarction due to multiplecoronary-ventricular fistulas. Cathet Cardiovasc Diagn 1989;16:247-9.

139 Reidy JF, Jones ODH, Tynan MJ, Baker EJ, Joseph MC. Embo-lisation procedures in congenital heart disease. Br Heartj 1985;54:184-92.

140 Bennett JM, Maree E. Successful embolization of a coronary ar-terial fistula. Intjcardiol 1989;23:405-6.

141 Brand M van de, Pieterman H, Suryapranata H, Bogers AJJC.Closure ofa coronary fistula with a transcatheter implantable coil.Cathet Cardiovasc Diagn 1992;25:223-6.

142 Lacombe P, Rocha P, Marchand X, Mulot R, Rigaud M, JondeauG, et al. High flow coronary fistula closure by percutaneous coilpacking. Cathet Cardiovasc Diagn 1993;28:342-6.

143 Millaire A, Goullard L, Groote P de, Ducloux G. Congenital highflow coronary cameral fistula in an 81-year-old woman: manage-ment problems. Can J Cardiol 1992;8:917-20.

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Coronary artery fstulas