angio-pathological of ventricular interpretation of

Br Heart J 1982; 47: 281-9

Angio-pathological appearances of pulmonary valve inpulmonary atresia with intact ventricular septum

Interpretation of nature of right ventricle from pulmonaryangiographyELIZABETH A BRAUNLIN, AUGUSTIN G FORMANEK, JAMES H MOLLER, JESSE EEDWARDSFrom the Dwan Cardiovascular Learning Center and the Departments of Pediatric Cardiology, Radiology, andPathology, University ofMinnesota, Minneapolis, andfrom the Department ofPathology, United Hospitals, St Paul,Minnesota, USA

SUMMARY Correlative angiographic-anatomical studies in 19 cases of pulmonary atresia with intactventricular septum showed the following relations between the angiographic appearance of thepulmonary valve and the morphology of the right ventricle.

(1) Doming of the pulmonary valve was associated with a nearly normal-sized right ventricle and a

wide infundibulum patent to the level of the pulmonary valve.(2) A fixed valve was associated either with (a) pronounced hypoplasia of the ventricular chamber

and stenosis of the infundibulum or (b) less commonly, a massive right ventricle and Ebstein'smalformation of the tricuspid valve.

(3) An intermediate type valve was associated with a small right ventricle and a small infun-dibulum which was, however, patent to the level of the pulmonary valve.

It is suggested that the configuration of the pulmonary valve is a result of haemodynamic stressesplaced upon it. These stresses, in turn, are determined by the morphological nature of the rightventricle. Thus, the nature of the pulmonary valve as seen angiographically may be used as an indexof right ventricular morphology.

Infants with pulmonary atresia and intact ventricularseptum are often critically ill and require urgent diag-nosis and treatment in the neonatal period. ' The typeof operation performed, whether pulmonary val-votomy or a combination of an aorto-pulmonary shuntand the creation of an atrial septal defect, is basedupon angiographic determination of right ventricularsize and morphology.25 Several authors haveemphasised the variability of infundibular morphol-ogy and its importance in influencing the outcome ofpulmonary valvotomy.5-8 In cases where the infun-dibulum is patent to the level of the pulmonary valveand the atretic valve takes the form of a thin dia-phragm, surgical right ventricular to pulmonaryartery continuity may be obtained more readily thanThis study was supported by US Public Health Service Research grants from theNational Heart, Lung and Blood Institute.

Accepted for publication 15 September 1981

in those instances of severe infundibular hypoplasia oratresia.4 5 8

Zuberbuhler and Anderson6 recently described theanatomical characteristics of the pulmonary valve intheir necropsy specimens of pulmonary atresia withintact ventricular septum; there were two distinctappearances. In the first type, "prominent commis-sural ridges converged and met at the centre of the'valve"', while in the second type the commissuralridges were "present only at the periphery of themembranous pulmonary valve, the centre beingsmooth and bulging into the pulmonary trunk".Additionally, they found that the first type of pulmo-nary valve "was invariably associated either withinfundibular atresia or with a severely stenotic or re-gurgitant tricuspid valve". Using this as a basis, wehave attempted to correlate the angiographic appear-ance of the pulmonary valve, not only with its anatom-

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ical appearance, but also with the underlying rightventricular and infundibular morphology. Such a cor-

relation, if available, would be of considerable clinicalinterest, since it would distinguish between infantsin whom pulmonary valvotomy alone might be in-adequate to establish right ventricular to pulmonaryarterial continuity and those in whom continuitycould be easily established and right ventriculargrowth encouraged.The purpose of this study, therefore, was to deter-

mine whether the angiographic character of the pul-monary valve in cases of pulmonary atresia with intactventricular septum was a reliable basis from which topredict the size and morphology of the right ventricu-lar chamber.

Subjects and methods

The following observations were made: (1) the natureof the pulmonary valve as seen in angiocardiograms;(2) the nature of the pulmonary valve in necropsyspecimens; (3) the size and morphology of the rightventricular chamber in angiocardiograms; and finally(4) the size and morphology of the right ventricle andtricuspid valve in necropsy specimens.To determine the nature of the pulmonary valve

angiographically, use was made of the lateral views ofthose left ventriculograms, aortograms, or the latephase of venous angiograms that showed the base ofthe pulmonary trunk. Angiograms from 27 patientswere available for review, and in 19 of these the baseof the pulmonary trunk was clearly seen angiographi-cally (nine aortograms, four left ventriculograms,three pulmonary arteriograms performed after aorto-pulmonary shunting procedure, one left atriogram,and two late phase venous angiograms). In the othereight patients in whom angiography had been done,the pulmonary valve was not well visualised becauseof either an insufficient amount of contrast material(an aortogram in two patients) or the fact that thevalve was obscured by overlying cardiac structures(forward angiograms in six patients). In the 19 satis-factory angiograms, the pulmonary valve wasclassified angiographically by one of us (AGF) asdomed, fixed, or an intermediate form. This part ofthe study was done with the knowledge that pulmo-nary atresia with intact ventricular septum was pres-ent but without that of other details of the cases.A domed valve was identified when, during ven-

tricular systole, the valve plate was mobile and formedeither a large domed or box-like bowing into the pul-monary trunk. Pulmonary valve sinuses were often vis-ible at the base of the dome. With a fixed valve, thebase of the pulmonary trunk did not change in shapeduring the cardiac cycle and consistently appeared asa "pouch". Pulmonary valve sinuses were identified

Braunlin, Formanek, Moller, Edwards

in some but not all cases. An intermediate form of thevalve was present when doming, though present,involved only a small central portion of the valveplate. Well-formed valve sinuses were visible at thebase of the pulmonary trunk.Ten of the 19 patients with satisfactory angiograms

had eventually died. Using the eight necropsy speci-mens available from these cases we compared theangiographic characteristics of the pulmonary valvewith its anatomical appearance. In five specimens thepulmonary valve had not been operated upon. In twospecimens (each with a fixed valve), an eccentricallyplaced single incision pulmonary valvotomy had beenperformed but each of these two valves could be easilyreapproximated and the details of the anatomy deter-mined. In the final necropsy specimen (that with adomed valve), though a small portion of pulmonaryvalvular tissue had been surgically removed, itappeared that sufficient tissue remained intact inorder to classify the valve.The size and morphology of the right ventricle were

determined by at least one of the following methods ineach of the 19 cases: right ventriculography (15 cases),necropsy (eight cases), at operation (one case). In fivecases both the right ventriculogram and the necropsyspecimen were available.The available right ventriculograms were analysed

for the presence and size of the infundibulum, thepresence of myocardial sinusoids, the size of theinflow portion of the right ventricle, and the presenceof tricuspid regurgitation.

In the eight necropsy specimens, the diameter ofthe infundibular chamber was measured by calibratedsound. Right ventricular and left ventricular inlet andoutlet dimensions were measured as previouslydescribed6 and were compared with previously pub-lished age-related normal values.9 A rightventricular/left ventricular index was obtained bymultiplying right ventricular inlet and outlet dimen-sions and dividing this product by the product of leftventricular inlet and outflow dimensions.6

Difficulties were encountered in measuring the verysmallest ventricles with confidence. Though weremeasured these chambers on subsequent occasionsand were satisfied that we could reproduce ourfigures, it is possible that the size of the very smallestright ventricles has been overestimated because ofthe presence of myocardial sinusoids in these speci-mens.The circumference of the true tricuspid valve

annulus was measured in each case and comparedwith previously published age-related normal values.9The circumference of the pulmonary trunk immedi-ately proximal to its bifurcation was measured in eachspecimen.The tricuspid valve was examined where possible in



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Pulmonary atresia with intact venticular septum

each of the eight specimens for Ebstein's malforma-tion and for dysplasia of the valve. Tricuspid valvedysplasia was characterised as previously described byBecker and associates'I and included focal or diffusethickening of the valve leaflets, deficient developmentof chordae and papillary muscles, improper separa-tion of the valve components from the ventricularwall, and focal agenesis of valvular tissue.

Results

DOMED PULMONARY VALVEIn four of the 19 angiocardiographic studies (cases 1 to4) the pulmonary valve appeared "domed" (Fig. la).The central part of the valve plate was mobile and

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smooth and bulged forward into the pulmonary trunkduring ventricular systole. The angiographic appear-ance of the valve was similar to classical critical pul-monary valvular stenosis except that a jet was notidentified. Necropsy in two of the four patients withdomed valves who died showed the pulmonary valveto have the following characteristics (Fig. lb).The atretic pulmonary valve plate was thin and

dome-shaped. On its arterial aspect were three shal-low, thick, equidistant raphes, each terminating at thecentral part of the plate. Three well-formed sinuseswere present.The circumferences of the pulmonary trunks were

18 and 20 mm, respectively.Three of the four patients with a domed pulmonary

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Fig. 1 Domed pulmonary valve in pulmonary atresia with intact ventricular septum. (a) Pulmonary arteriogram, lateralview. Pulmonary valve domed (arrow) into pulmonary trunk. Insert. Line drawing ofpulmonary trunk as seen inaccompanying angiogram. (b) Specimen ofdomed pulmonary valve from above. (c) and (d) Right ventriculogram,anteroposteior view (c) and lateral view (d). Right ventricl smaler than normal. Infundibulum patent to level ofpulmonaryvalve (arrow).



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valve had had right ventriculograms. In each, the rightventricular inflow portion was highly trabeculated andof nearly normal size. "Significant" tricuspid regurgi-tation was present in each, though part of this regurgi-tation may have been catheter-induced. Myocardialsinusoids were not seen. The infundibulum was ofnormal calibre and appeared patent to the level of thepulmonary valve in each case (Fig. Ic and d).

In the two available necropsy specimens with adomed pulmonary valve, analysis of the right ventri-cle disclosed the following characteristics. The infun-dibulum admitted a 2 to 3 mm probe, and the probecould be advanced to the pulmonary valve. Right andleft ventricular dimensions were within the limits ofnormal for age,9 but the right ventricular/left ven-tricular indices of 058 and 0O81 disclosed the relativehypoplasia of the right ventricle in these cases (Fig.2).The circumference of the tricuspid valve annulus in

both specimens was below the average age-relatedvalue.9 Neither specimen showed gross evidence ofEbstein's malformation, but both showed signs ofdysplasia, consisting of focal thickening of the leafletsand shortened chordae.

FIXED PULMONARY VALVEAngiograms of nine patients (cases 5 to 13) showedthe pulmonary valve to be of the "fixed " type (Fig.3a). The pulmonary arterial root retained a pouch-like

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Fig. 2 Right ventricularlIeft ventricular indices determinedfor all necropsy specimens with pulmonary atresia and intactventricular septum. Cases grouped by valve type.

shape throughout the cardiac cycle, and no doming ofthe valve was seen. Five patients in this group died,and necropsy specimens were available in four ofthese cases. In each specimen the base of the pulmo-nary trunk appeared primitive and poorly defined(Fig. 3b). The valve plate was a flat firm membrane.Upon its arterial aspect two or three thin ridges con-verged to meet at the centre of the valve plate. Thepulmonary valve sinuses were poorly formed.The circumference of the pulmonary trunk ranged

from 14 to 24 mm.In seven of the nine patients with a fixed valve, a

right ventriculogram was available. From these, twodistinct types of ventricular morphology were found.In two patients the right ventricle was much enlargedand associated with massive tricuspid regurgitation(Fig. 4a and b). The infundibular chamber in each waswidely patent, and myocardial sinusoids were notdemonstrated. In each of the other five patients with afixed pulmonary valve the right ventricular chamberwas minute and the infundibulum tiny. Myocardialsinusoids were prominent in each case, and tricuspidregurgitation was minimal or absent (Fig. 4c and d).Necropsy specimens were available in four of the

patients with a fixed pulmonary valve. In each of thetwo cases with an enlarged right ventricle the infun-dibulum was a poorly defined extension of the body ofthis chamber. Measured right ventricular dimensionsexceeded the limits of normal for age-related controls,while left ventricular dimensions were within thenormal range.9 The right ventricular/left ventricularindices of 2-45 and 1-71 (Fig. 2) indicated the degreeof right ventricular enlargement. Ebstein's malforma-tion of the tricuspid valve was present in both cases.The atrialised portion of the right ventricle wassignificant in each specimen. Nevertheless, in contrastto cases with isolated Ebstein's malformation, the trueright ventricular chamber, as measured from the baseof the abnormal tricuspid valve leaflet, was also largerthan the average age-related value.9The circumference of the true tricuspid annulus

was obtained in each of these specimens, and in bothwas larger than the average age-related value.9 Inaddition to Ebstein's malformation, each tricuspidvalve showed signs of dysplasia, including focal thick-ening of the leaflets, deficient chordal development,attachment of valvular tissue directly to the right ven-tricular wall, and, in one case, focal agenesis of valvu-lar tissue.

In the two remaining necropsy specimens with theangiographic appearance of a fixed pulmonary valve,the infundibulum was very stenotic, and a 2 mmprobe could not be advanced into it, there being mus-cular obstruction between it and the pulmonary valve.

Right ventricular dimensions were abnormallysmall, while left ventricular dimensions were within

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Fig. 3 Fixed pulmonary valve in pulmonary atresia with intact ventricular septum. (a) Left ventriculogram, lateral view.Pulmonary arterial root appears as afixed single pouch-like sac (arrow) during ventricular systole. Neither valve sinuses norcentral area ofdoming are present. Insert. Line drawing ofpulmonary trunk as seen in accompanying angiogram. (b)Specimen offixed type ofpulmonary valve from above. Three raphes (arrows) meet in centre of valve plate.

normal limits and the right ventricular/left ventricularindices were 0*19 and 0 11, reflecting the extremehypoplasia of the right ventricle (Fig. 2).

In one survivor of the group with the fixed type ofvalve no right ventriculogram was performed, but atoperation a very hypoplastic tricuspid valve and rightventricle were seen.The circumference of the tricuspid valve annulus

was measured in each case and found to be less thanthe average age-related value.9 Severe tricuspid valvedysplasia was present in both specimens and consistedof thickened valve tissue, abnormal chordae andpapillary muscles, and focal agenesis of valvular tis-sue.

INTERMEDIATE PULMONARY VALVEFrom angiograms in the remaining six cases (cases 14to 19), the pulmonary valve was classified as of the"intermediate" type. The valve sinuses were wellformed. A small area of separation was seen betweenthe sinuses centrally. During ventricular systole thearea of separation widened and the tiny central por-tion of the atretic valve plate domed (Fig. Sa). Three

patients died, and specimens were available from two.In both, the pulmonary valve bore a strong resemb-lance to the domed pulmonary valve in that threethick ridges or raphes were present but did not extendto the centre of the valve plate. The central area of thevalve was smooth and thin but, in contrast to theclassical domed valve, formed only a small portion ofthe total valve surface (Fig. 5b).The circumferences of the pulmonary trunks were

18 and 26 mm, respectively. In four of the fivepatients with an intermediate type of pulmonaryvalve, right ventriculograms were available for study.In each case the inflow portion of the right ventriclewas small. The infundibulum was present andappropriate for the size of the ventricle but appearedsmaller than normal (Fig. Sc and d). Myocardialsinusoids were seen in two of the right ventriculo-grams, but in the other two their presence could not bedetermined. Tricuspid regurgitation was mild in eachcase. Three patients from this group died, and nec-ropsy specimens were available in two. A 2 mm probecould be advanced into each infundibulum to the levelof the pulmonary valve. Right ventricular dimensions

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Fig. 4 Two cases ofpulmonary atresia withfixed type ofpulmonary valve. (a) and (b) Enlarged right ventricle and tricuspidregurgitation. Right ventniculogram in frontal view (a) and lateral view (b). (c) and (d) Minute right ventricle. (c) Frontalview shows prominent myocardial sinusoids through which opacfication of the aorta occurs. (d) Lateral view. Hypoplasticinfundibulum (arrow).

were smaller than the average age-related normal val-ues, but left ventricular dimensions were within nor-mal limits.9 The right ventricular/left ventricularindices of 0O42 and 0-32 were intermediate betweenthe values in those specimens with a tiny right ventri-cle and fixed pulmonary valve, and those with a nearly

normal ventricular size and domed pulmonary valve(Fig. 2).The circumference of the tricuspid valve annulus

was measured in both specimens and was found to beless than the average value but still within the range ofnormal for age-related controls.9 Tricuspid valve dys-

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Fig. 5 Intermediate type ofpulmonay valve in pulmonary atresia with intact ventricular septum. (a) Left ventriculogram,lateral view. Two well-formed pulmonary valve sinuses are seen, the posterior sinus being partially obscured by the overlyingascending aorta and coronary artery. A tiny central dome separates the valve sinuses (point ofarrow). Insert. Line drawing ofpulmonary trunk as seen in accompanying angiogram. (b) Specimen ofintermediate type pulmonary valve viewedfrom above.(c) and (d) Right ventriculogram, anteroposteior view (c) and lateral view (d). Right ventrick small. Infumdibulum patent tokvel ofpulmonary valve (arrow).

plasia was present in both specimens, consisting ofabnormal chordae and thickened leaflets in one caseand an arcade-like tricuspid valve in the other.

Comment

This study confirmed the general concepts of Zuber-buhler and Anderson6 that in pulmonary atresia withintact ventricular septum there is variation in thestructure of the pulmonary valve and, moreover, that

there is a tendency for certain structural types of pul-monary valve to be associated with particular rightventricular features.

Additionally, the direct relation between the cir-cumference of the tricuspid valve annulus and theright ventricular chamber size reported in this study,as well as the finding of some degree of tricuspid valvedysplasia in all specimens, supports the conclusionsnot only of Zuberbuhler and Anderson but also ofothers. "I That no correlation could be found between

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the pulmonary arterial size and the underlying rightventricular morphology was also in accord with previ-ous findings.6

This study also showed that there is a close correla-tion between the angiocardiographic appearance ofthe pulmonary valve and the state of the valve whenexamined directly.

Zuberbuhler and Anderson6 designated two struc-tural main types of atretic pulmonary valves conform-ing to the types we have called the domed and fixedtypes. Our observations indicate that a third formmay be identified angiographically, the intermediatetype.The correlation between the type of pulmonary

valve, and the morphology of the right ventricle,seems to be a logical expression of the haemodynamicstresses upon the pulmonary valve caused by rightventricular anatomy. Whatever causes atresia of thepulmonary valve, it may be assumed that the condi-tion is established early in embryonic life. Thus,stresses upon the valve plate occur for many monthsbefore birth and these stresses have an influence inmoulding its structure.Our study showed the association of the domed

type of valve with a near-normal sized right ventricleand infundibulum, while tricuspid regurgitation waseither absent or minimal. It is likely that under theseconditions the right ventricular pressure is abnor-mally high, and the full force of this pressure isapplied to the pulmonary valve plate, causing it todome.When the valve plate is of the fixed type, rep-

resented by a flat membrane, we found that the rightventricle was either large and associated with tricus-pid regurgitation or the right ventricle and its infun-dibulum were hypoplastic. Under either of these cir-cumstances relatively low levels of pressure would beapplied to the valve plate, leaving it in a non-domedstate.The intermediate type of valve is characterised by

minimal doming and in this type it is reasonable thatthe haemodynamics of the right ventricle are inter-mediate between those associated with the domed andfixed types of valve.

Thus, it appears evident that the appearance of thepulmonary valve plate is a consequence of stressesupon it, and the anatomical nature of the right ventri-cle determines the haemodynamics which, in turn,influence the valve configuration.From the clinical point of view, this concept may be

helpful, as from a given configuration of the pulmo-nary valve, subvalvular haemodynamics may be infer-red. From the latter, in turn, a concept of right ven-tricular morphology may be assumed, though thepotential for right ventricular growth after pulmonaryvalvotomy may also depend upon several other factors

as well, including right ventricular compliance, thepresence of myocardial sinusoids, and the nature ofthe tricuspid valve.

Although we have not used this classification in aprospective fashion, we believe, from the evidencepresented, that a pulmonary valvotomy in the new-born period in an infant with a fixed type pulmonaryvalve should probably be avoided. In the cases wheresuch a valve exists with a large right ventricle, tricus-pid regurgitation in concert with neonatal pulmonaryhypertension may, as others have noted,6 12 result incardiac output inadequate to sustain life. In caseswhere a fixed pulmonary valve exists with a tiny rightventricle, establishing continuity between the ventri-cle and pulmonary artery almost certainly cannot beachieved by valvotomy alone. In addition, severetricuspid stenosis and dysplasia may preclude adequ-ate growth and function in spite of successful rightventricular outflow tract reconstruction.On the other hand, in cases of pulmonary atresia

and intact ventricular septum where the pulmonaryvalve appears to be either domed or "intermediate", avalvotomy in the newborn period appears technicallyfeasible, either alone or together with an aortopulmo-nary shunting procedure. In addition, right ventricu-lar chamber size in both of these categoriesapproaches normal values more closely and thus thepotential for growth of the right ventricle may be anti-cipated.

References

1 Gersony WM, Bernhard WF, Nadas AS, Gross RE.Diagnosis and surgical treatment of infants with criticalpulmonary outflow obstruction. Study of thirty-fourinfants with pulmonary stenosis or atresia, and intactventricular septum. Circulation 1%7; 35: 765-76.

2 Dhanavaravibul S, Nora JJ, McNamara DG. Pulmonaryvalvular atresia with intact ventricular septum: problemsin diagnosis and results of treatment. J Pediatr 1970; 77:1010-6.

3 Luckstead EF, Mattioli L, Crosby IK, Reed WA, DiehlAM. Two-stage palliative surgical approach for pulno-nary atresia with intact ventricular septum (type I). Am JCardiol 1972; 29: 490-6.

4 Cole RB, Muster AJ, Lev M, Paul MH. Pulmonaryatresia with intact ventricular septum. Am J Cardiol1968; 21: 23-31.

5 Dobell ARC, Grignon A. Early and late results in pul-monary atresia. Ann Thorac Surg 1977; 24: 264-74.

6 Zuberbuhler JR, Anderson RH. Morphological varia-tions in pulmonary atresia with intact ventricular sep-tum. Br Heart J 1979; 41: 281-8.

7 Arom KV, Edwards JE. Relationship between right ven-tricular muscle bundles and pulmonary valve.Significance in pulmonary atresia with intact ventricitlarseptum. Circulation 1976; 54, suppl III: 79-83.

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8 Patel RG, Freedom RM, Moes CAF, et al. Right ven-

tricular volume determinations in 18 patients with pul-monary atresia and intact ventricular septum. Analysis offactors influencing right ventricular growth. Circulation1980; 61: 428-40.

9 Rowlatt UF, Rimoldi HJA, Lev M. The quantitativeanatomy of the normal child's heart. Pediatr Clin NorthAm 1963; 10: 499-588.

10 Becker AE, Becker MJ, Edwards JE. Pathologic spec-

trum of dysplasia of the tricuspid valve. Features incommon with Ebstein's malformation. Arch Pathol 1971;91: 167-78.

11 Freedom RM, Dische MR, Rowe RD. The tricuspid

valve in pulmonary atresia and intact ventricular septum.A morphological study of 60 cases. Arch Pathol 1978;102: 28-31.

12 Barr PA, Celermajer JM, Bowdler JD, Cartmill TB.Severe congenital tricuspid incompetence in the neonate.

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Requests for reprints to Dr Jesse E Edwards,Department of Pathology, United Hospitals, 333North Smith Aveniue, St Paul, Minnesota 55102,USA

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