contributions of intramyocardial sinusoids pulmonary

British HeartJournal, I974, 36, I06I-I065.

Contributions of intramyocardial sinusoids inpulmonary atresia and intact ventricular septum to aright-sided circular shunt

Robert M. Freedom and Donald P. HarrmngtonFrom the Department of Pediatrics, Division of Pediatric Cardiology (RMF), and Department of Radiology,Cardiovascular Division, TheJohns Hopkins University and Hospital, Baltimore, Maryland, U.S.A.

In the patient with congenital heart disease, the phenomenon termed 'circular shunt' implies that some of theright-to-left shunted blood returns to its chamber of orgin through intracardiac channels or communications,hence bypassing the systemic capillary bed. We are reporting the angiographic appearance of a right-sided'circular shunt' in 2 patients with pulmonary atresia, diminutive, hypertensive right ventricle, and intactventricular septum. In these patients the intramyocardial sinusoids and diverticulaform the anatomical basisfor the right-sided 'circular shunt': blind, hypertensive right ventricle->intramyocardial sinusoids-1coronaryartery--coronary venous system-*coronary sinus--right atrium--right ventricle. It is suggested that retro-gradeflow through these intramyocardial sinusoids may impede or limit normal diastolic coronary artery per-fusion and may predispose to myocardial ischaemia and dysfunction. In addition, the natural history of theseintramyocardial sinusoids and diverticula is discussed.

The concept of a 'circular shunt' in the patient withcongenital heart disease was previously introducedby Shone and associates (I962). In the typical right-to-left intracardiac shunt, the blood participatingin the shunt passes through the systemic capillarybed before it returns to its chamber of origin. In thephenomenon termed 'circular shunt', however,some of the shunted blood returns to its chamber oforigin through intracardiac channels or communi-cations, hence bypassing the systemic capillary bed.There have been 3 adequately documented cases

of 'circular shunt' (though undoubtedly there aremore that are unreported). In 2 (Jue, Noren, andEdwards, I966), pulmonary atresia with a left ven-tricular-right atrial communication formed theanatomical basis for the circular shunt. In the othercase (Shone et al., I962), right atrial blood wasshunted into the left atrium. Some of this blood wasfurther shunted through a small ventricular septaldefect into the right ventricle. Then in the presenceof tricuspid regurgitation and severe pulmonarystenosis, some of the blood which had originated inthe right atrium returned to that chamber to com-plete the circular shunt.

In two recently studied patients with pulmonary

Received 8 April 1974.

atresia, diminutive right ventricle, and intact ven-tricular septum, a right-sided 'circular shunt'was demonstrated angiographically. The role ofintramyocardial sinusoids as the basis for the circu-lar shunt in these patients is the subject of thisreport.

PatientsBoth patients presented in the first two days of life withcardiac cyanosis and profound hypoxaemia. Clinicalexaminations, chest radiographs, and electrovector-cardiograms were typical of pulmonary atresia, hypo-plastic right ventricle, and intact ventricular septum(Gamboa, Gersony, and Nadas, I966; Gersony et al.,I967). Both patients underwent cardiac catheterizationand angiography. Their haemodynamic data are sum-marized in the Table. Subsequent to this study, bothwere palliated by a systemic to pulmonary artery anasto-mosis.

Angiographic findingsCase r has undergone three cardiac catheterizations. Aselective right ventricular angiocardiogram (not suitablefor reproduction)performed at 2 daysofage demonstratedpulmonary atresia, a hypoplastic, poorly contractile rightventricle, significant tricuspid stenosis, and intramyo-cardial sinusoids which either terminated blindly within

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FIG. I Case I, age 22 months. A right ventricular angiocardiogram in the anteroposteriorprojection demonstrates a small, eccentrically shaped right ventricular chamber (RV). An ex-tensive network ofmyocardial sinusoids (arrow) communicates with the right ventricle. Opacifica-tion of the pulmonary artery is not seen.

w= _ __ .................

FIG. 2 Case I, age 22 months. A right ventricular angiocardiogram in the lateral projection(same study as Fig. x, later film). The right-sided circular shunt is well seen. The coronary vein(CV) and coronary sinus (CS) are in direct continuity with the myocardial sinusoids and smallright ventricle. No opacification of the coronary ostia or aortic root is appreciated in this sequence.



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FIG. 3 Case 2, age 8 hours. Right ventricularangiocardiogram in the lateral projection. The dim-inutive right ventricle (RV) and myocardial sinusoids(arrow) are well visualized. There is prompt opacifi-cation of the apparent anterior descending and leftcoronary artery (LCA) and aortic root (AO).

the myocardium or communicated with the anteriordescending coronary artery. Opacification ofthe coronarysinus was noted. The patient was recatheterized at 6months and at 22 months of age. The selective rightventricular angiocardiogram at 22 months of age demon-strated similar anatomical features (Fig. i). However,using only I 0 ml of Hypaque 75, slow hand injectioninto the right ventricle led to rapid opacification of

intramyocardial sinusoids, coronary artery, coronaryvein, and coronary sinus before visualization of theaortic root (Fig. 2). Indicator dilution curves performedby injection of green dye into the right ventricle withsampling in the coronary sinus and the ascending aortayielded similar appearance times.

Case 2 was catheterized at 8 hours of age and again at5 months. Selective right ventricular angiograms were

performed at both studies. As in Case i, pulmonaryatresia, a diminutive right ventricle, and minimal in-competence of the tricuspid valve were seen. In additionan extensive network of intramyocardial diverticula andsinusoids are present which communicate with the leftcoronary artery and densely opacify the left coronaryostia and aortic root (Fig. 3). Faint opacification of cor-onary sinus is noted.

DiscussionSince Grant first recognized intramyocardial sinu-soid-coronary artery communications at necropsy(Grant, I926), many reports relating to the embryo-logy, anatomy, and angiographic findings haveaccumulated (Anselmi et al., I96I; Baker, Vogel,and Blount, I967; Celermajer et al., I968; Davignonet al., i96ia, b; Elliott, Adams, and Edwards, I963;Guidici and Becu, I960; Lauer et al., I964; Williams,Kent, and Edwards, I95I).

In the patient with pulmonary atresia and intactventricular septum, egress of blood from the blindright ventricle may take two possible courses. i)During right ventricular systole, blood may regurgi-tate through an incompetent tricuspid valve backinto the right atrium and hence into the left atrium,left ventricle, and the systemic circulation, or 2)blood may be pumped during right ventricularsystole from the hypertensive right ventricularcavity into the intramyocardial sinusoids (Sissmanand Abrams, I965). Histopathological and angio-graphic studies of these intramyocardial sinusoids

TABLE Catherization data

Pressure data (mmHg) Oxygen saturation (%)

RA LA RV LV Ao RA Ao

2 dy a=I3 a=I2 60/I0 59/4 54/45 28 45g ~~~m=6 m=6

Case I 6 mth a= I2 a=6 I82/II 89/7 87/54 51 78m=7 m=4

22 mth a=i8 a=ii I50/I3 98/io II5/70 48 64

(Io) m=6r 8 hr a=5 I50/I0 60/6 65/37 47 55

Case2 m m=2 m=2|5 mth a= 20 a=I2

m=8 5 m=7 I50/I7 85/7 85/45 45 87



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z064 Freedom and Harrington

LEFT ATRIUMRIGHT /ATRIUM

BLIND RIGHTCORONARY VENTRICLESINUS

C--NARYINTRAMYOCARDIAL _END BLINDLY

.SINUSOIDS IN MYOCARDIUMcb ONARY /

VENOUS SYSTEM

CORONARYARTERY %VAORTA

FIG. 4 Schematic portrayal of the right-sided circular shunt in the patient with pulmonaryatresia, diminutive and hypertensive right ventricle, and intact ventricular septum. The intra-myocardial sinusoids are the anatomical basis for this circular shunt.

suggest that they may either end blindly within themyocardium (Lauer et al., I964) or may communi-cate with the coronary arteries (Elliott et al., I963).It is not surprising, then, that injection of contrastmaterial into the blind right ventricle could lead toimmediate opacification of the coronary ostium andaortic root.

In the present cases, the intramyocardial sinu-soids obviously communicate with the coronaryarterial tree. Contrast material densely opacifiedsequentially the sinusoids, coronary artery, coronaryvenous system, and coronary sinus as well as thecoronary ostium and aortic root. Thus, the intra-myocardial sinusoids form the basis for this right-sided circular shunt in pulmonary atresia with in-tact ventricular septum (Fig. 4).The observation that dense opacification of the

coronary venous system occurs quite early is sug-gestive of direct communication between the intra-myocardial sinusoids and the coronary venoussystem, though this has not been substantiated.Though these sinusoids act as a passive conduit

for the egress of blood from the blind right ventriclein the patient with pulmonary atresia and relativelycompetent tricuspid valve, do they by virtue oftheir communication with the coronary arteries con-tribute to myocardial ischaemia ? Numerous reportshave documented the communication of thesesinusoids with the anterior descending coronaryartery (Cornell, I966; Davignon et al., i96ib;Elliott et al., I963; Guidici and Becu, I960; Laueret al., I964). As right ventricular systole will beprolonged in the patient with pulmonary atresia andintact ventricular septum, it is conceivable thatnormal aortic diastolic filling of the coronaryarteries will be impaired by retrograde filling of the

coronary arteries via the sinusoids, thus predis-posing to ischaemic changes and myocardial dys-function. It is of interest that left ventricular strainpatterns have been recognized in the electrocardio-grams of patients with pulmonary atresia and intactventricular septum, before the performance of asystemic to pulmonary anastomosis (Celermajeret al., I968; Elliott et al., I963; Gamboa et al., I966;Schrire, Sutin, and Barnard, I96I). In our patient(Case i), in the absence of significant left ventriculardiastolic overload, the ejection fraction both byultrasound and by angiography was less than o 4o,consistent with significant left ventricular dysfunc-tion. While it has been previously documented thatleft ventricular subendocardial muscle must receiveall or most of its flow during diastole because intra-myocardial compressive forces are highest in thisarea and hence prevent systolic perfusion of thismuscle layer (Vincent, Buckberg, and Hoffman,I974; Buckberg et al., 1972), it is possible that theleft ventricular ischaemia and dysfunction mightbe related to the intramyocardial-sinusoids-cor-onary artery communications in the patient withsevere right ventricular hypertension.The natural history of the intramyocardial sinu-

soids in the patient with pulmonary atresia, hyper-tensive right ventricle, and intact ventricularseptum is largely undefined. Regression of intra-myocardial sinusoids has been observed in thosepatients in whom satisfactory decompression of thehypertensive right ventricle has been achieved bypulmonary valvotomy and infundibulectomy. Insome patients studied serially in our institution theangiographic appearance may appear the same, orsignificant changes may be observed. In at least onepatient a single large communication between



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Contributions of intramyocardial sinusoids in pulmonary atresia Io65

intramyocardial sinusoid and coronary artery wasidentified at 2 days of age. Repeat study usingsimilar angiographic technique at 5 months of agefailed to demonstrate this intramyocardial sinusoid-coronary artery communication. There are twopossible explanations for this observation. In situthrombosis may have led to obliteration of theintramyocardial sinusoid and its communications.This seems unlikely because thrombosis in thesechannels has not been noted previously in publishedreports or in our own experience. It is more likelythat secondary endocardial sclerosis may haveoccluded the endocardial orifice to the intramyo-cardial sinusoid. This seems more tenable becausesecondary endocardial sclerosis is well documentedin these patients (Elliott et al., I963).

Although intramyocardial sinusoids are notunique to the patient with pulmonary atresia andintact ventricular septum, they are found mostcommonly in this group. Grant has previously sug-gested (Grant, I926) that the intramyocardialsinusoids and diverticula represent abnormal per-sistence and ectasia of the intratrabecular spaces andtheir primitive communications with the coronaryartery system, and their persistence is related to thesevere fetal right ventricular hypertension.

Intramyocardial sinusoidal-coronary artery com-munications can occur with other significant anato-mical variations in the coronary arteries. Recently, amost unique case was reported (Lenox and Briner,I972). They described the clinical and necropsyfindings of a 2-month-old infant with absent proxi-mal coronary arteries, pulmonary atresia, intactventricular septum, hypoplastic right ventricle,and Ebstein-like anomaly of the tricuspid valve.The coronary arteries in this patient were not con-nected to either the aorta or pulmonary artery, butoriginated from the intramyocardial sinusoids.

In summary, the intramyocardial sinusoids anddiverticula are basic to a right-sided circular shuntin the patient with pulmonary atresia, hypoplasticand hypertensive right ventricle, and intact ven-tricular septum. They serve as a passive conduit forthe egress of blood from the blind right ventricle,and may hinder normal diastolic coronary arteryperfusion and hence predispose to ischaemic myo-cardial dysfunction.

ReferencesAnselmi, G., Mufnoz, S., Blanco, P., Carbonnell, L., and

Puigb6, J. J. (i96i). Anomalous coronary artery connectingwith the right ventricle associated with pulmonary stenosisand atrial septal defect. American Heart journal, 62, 406.

Baker, W. P., Vogel, J. H. K., and Blount, S. G., Jr. (I967).Coronary artery - right ventricular communicationassociated with pulmonary atresia and ventricular septaldefect. Circulation, 35, 923.

Buckberg, G. D., Fixler, D. E., Archie, J. P., and Hoffman,J. I. E. (1972). Experimental subendocardial ischemia indogs with normal coronary arteries. Circulation Research,30, 67.

Celermajer, J. M., Bowdler, J. D., Gengos, D. C., Cohen,D. H., and Stuckey, D. S. (I968). Pulmonary valve fusionwith intact ventricular septum. American Heart Journal,76, 452.

Cornell, S. H. (1966). Myocardial sinusoids in pulmonaryvalvular atresia. Radiology, 86, 421.

Davignon, A. L., DuShane, J. W., Kincaid, 0. W., and Swan,H. J. C. (i96ia). Pulmonary atresia with intact ventricularseptum. Report of two cases studied by selective angio-cardiography and right heart catheterization. AmericanHeart J'ournal, 62, 690.

Davignon, A. L., Greenwold, W. E., DuShane, J. W., andEdwards, J. E. (i96ib). Congenital pulmonary atresia withintact ventricular septum. Clinicopathologic correlationof two anatomic types. American Heart J'ournal, 62, 591.

Elliott, L. P., Adams, P., Jr., and Edwards, J. E. (I963).Pulmonary atresia with intact ventricular septum. BritishHeart Journal, 25, 489.

Gamboa, R., Gersony, W. M., and Nadas, A. S. (I966). Theelectrocardiogram in tricuspid atresia and pulmonaryatresia with intact ventricular septum. Circulation, 34, 24.

Gersony, W. M., Bernhard, W. F., Nadas, A. S.; and Gross,R. E. (I967). Diagnosis and surgical treatment of infantswith critical pulmonary outflow obstruction. Study ofthirty-four infants with pulmonary stenosis or atresia, andintact ventricular septum. Circulation, 35, 765.

Grant, R. T. (1926). Unusual anomaly of coronary vessels inmalformed heart of child. Heart, 13, 273.

Guidici, C., and Becu, L. (I960). Cardio-aortic fistula throughanomalous coronary arteries. British Heart j3ournal, 22,729-

Jue, K. L., Noren, G., and Edwards, J. E. (I966). Pulmonaryatresia with left ventricular-right atrial communication:basis for 'circular shunt'. Thorax, 2I, 83.

Lauer, R. M., Fink, H. P., Petry, E. L., Dunn, M. I., andDiehl, A. M. (I964). Angiographic demonstration ofintramyocardial sinusoids in pulmonary-valve atresiawith intact ventricular septum and hypoplastic rightventricle. New EnglandJournal of Medicine, 271, 68.

Lenox, C. C., and Briner, J. (I972). Absent proximal coronaryarteries associated with pulmonic atresia. American3Journalof Cardiology, 30, 666.

Schrire, V., Sutin, G. J., and Barnard, C. N. (I96I). Organicand functional pulmonary atresia with intact ventricularseptum. American Journal of Cardiology, 8, ioo.

Sissman, N. J., and Abrams, H. L. (I965). Bidirectional shunt-ing in a coronary artery - right ventricular fistula assoc-iated with pulmonary atresia and an intact ventricularseptum. Circulation, 32, 582.

Shone, J. D., Anderson, R. C., Elliott, L. P., Amplatz, K.,Lillehei, C. W., and Edwards, J. E. (I962). Clinical patho-logical conference. American Heart journal, 64, 547.

Vincent, W. R., Buckberg, G. D., and Hoffman, J. I. E.(I974). Left ventricular subendocardial ischemia insevere valvar and supravalvar aortic stenosis. A commonmechanism. Circulation, 49, 326.

Williams, R. R., Kent, G. B., Jr., and Edwards, J. E. (I95I).Anomalous cardiac blood vessel communicating with theright ventricle. Observations in a case of pulmonaryatresia with an intact ventricular septum. Archives ofPathology, 52, 480.

Requests for reprints to Dr. Robert M. Freedom,Hospital for Sick Children, 555 University Avenue,Toronto, Ontario, Canada MsG iX8.



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