Ventricular myoarchitecture in tetralogy of Fallot · Nine specimens from cases of tetralogy of Fallot and four normal hearts were studied. The specimens with tetralogy of Fallot

Heart 1996;76:280-286

Ventricular myoarchitecture in tetralogy of Fallot

Damian Sanchez-Quintana, Robert H Anderson, Siew Yen Ho

AbstractBackground-Little attention has beenpaid to the architecture of the musclefibres of the ventricular walls in congeni-tally malformed hearts. In this study thegross pattern of myocardial fibres in nor-mal hearts was compared with that incases of tetralogy of Fallot.Methods and results-After morphologi-cal examination nine specimens withtetralogy were dissected to study the ven-tricular myoarchitecture. Changes werefound in the shape of the malformed ven-tricles. The ventricular walls werearranged in layers in all hearts.Superficial and deep layers were presentin both ventricles, with the superficiallayer showing a more oblique orientationin the specimens with tetralogy than innormal hearts. Modifications of musclefibre that were related to the type of mal-formation were seen in the deep layer. Amiddle layer was present in the left ven-tricles of normal hearts and specimenswith tetralogy: this showed a horizontalorientation in both groups. In contrast, amiddle layer was found in the right ven-tricle only in specimens showing tetral-ogy.Conclusions-The malformed heartsshowed modifications in ventricularshape, in the arrangement of muscle inthe right ventricle, and in the overallmyoarchitecture. These changes couldwell be the consequence ofthe same agent(or agents) that caused the structuraldefect.

(Heart 1996;76:280-286)

Departamento deAnatomia Humana,Facultad de Medicina,Universidad deExtremadura,Badajoz, SpainD Sanchez-QuintanaDepartment ofPaediatrics, NationalHeart and LungInstitute, DovehouseStreet, LondonR H AndersonS Y HoCorrespondence to:Dr S Y Ho, Department ofPaediatrics, National Heartand Lung Institute,Dovehouse Street, LondonSW3 6LY.

Accepted for publication25 April 1996

Keywords: anatomy; tetralogy of Fallot; ventricularmyoarchitecture

That the heart is a muscular organ with a com-

plex architectural arrangement of its ventricularfibres was known to Harvey' over 300 yearsago. Many workers since then have investi-gated this architecture in the normal heart,mostly basing their findings on gross dissec-tion.2-8 Others have combined dissection andhistology.910 More recently, sophisticatedmethods have been used based on three-dimensional reconstruction from serial sec-

tions." 12 Comparison of these various studieshas revealed several controversies. Some arguethat there are discrete systems of fibres in eachventricle,2 whereas others describe a single

system encompassing both ventricles.8 Somehave proposed the fibrous trigones as points ofanchorage of the muscle fibres,45 while othershave proposed the aortic and pulmonary rootsas the only areas of insertion.8 Yet anotherview is that the myocardial fibres branch fromone another, as if they were inserted in adja-cent muscle fibres, rather than taking their ori-gin or insertion from the fibrous skeleton.9Despite these discrepancies, these studies haveshown that the myocardium represents a com-plex three-dimensional network of cells, witheach layer having a preferred orientation. Itseems reasonable to propose that changes inheart shape, and in the force generated duringsystole, depend on the relative orientation of,and interaction between, these bundles offibres. Studies of the muscular architecture,for the most part, have been confined to nor-mal hearts, with few studies comparing dissec-tions of normal and congenitally malformedhearts.'3 To extend this field of study we com-pared the ventricular myoarchitecture of thenormal heart with that in one congenital mal-formation, namely tetralogy of Fallot.

MethodsNine specimens from cases of tetralogy ofFallot and four normal hearts were studied.The specimens with tetralogy of Fallot wereselected from the cardiopathological collectionof the National Heart and Lung Institute,Royal Brompton Hospital, London. To beregarded as an example of tetralogy, a hearthad to show four features: namely a ventricu-lar septal defect, subpulmonary stenosis oratresia, biventricular origin of the leaflets ofthe aortic valve, and right ventricular hypertro-phy. The patients with tetralogy of Fallot fromwhom the hearts were obtained ranged in agefrom eight hours to 59 years. The normalhearts came from subjects aged from seven to61 years old who died of causes unrelated tocardiac pathology. The normal hearts werefixed by immersion in 10% formaldehyde forabout two weeks before study. The heartsfrom the cardiopathological collection havebeen fixed in 10% formaldehyde for manyyears, but their initial preparations were simi-lar. They were initially fixed intact by perfu-sion through the orifice of the inferior cavalvein after ligation of other connecting vessels.

Our specimens formed three subgroups rep-resenting the range of morphologies in tetral-ogy of Fallot. One specimen showedrudimentary formation of the pulmonary valve(so-called absent pulmonary valve syndrome).

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Ventricular myoarchitecture in tetralogy ofFallot

Valvar and subpulmonary infundibular steno-sis was found in six specimens. Pulmonaryatresia was present in the remaining two.The protocol used for dissection was similar

to that followed in earlier studies,'4 but in somecases the atria were not detached along the lineof the atrioventricular grooves. The hearts weredissected with watchmakers' tweezers and scis-sors, taking care not to disrupt superficial anddeep myocardial fibres when the epicardium orendocardium was removed. Special care wastaken to study the anatomy of the fibrous skele-ton, along with the interrelations betweenmyocardial fibres and the leaflets of the arterialatrioventricular valves. In studying architectureof the myocardium, we used the term "musclefibre" to describe a bundle of myocytes visibleby gross inspection. Thus fibres aligned in thesame orientation were exposed by step-by-steppeeling from the subepicardium to the suben-docardium. Each step was documented by ser-ial photography. The myocardial layers weredescribed as superficial, deep, and middle; witheach layer being distinguished on the basis of achange in orientation of muscular fibres fromthe adjacent layer.

ResultsEXTERNAL MORPHOLOGICAL FEATURESIn normal hearts the aortic orifice occupies akey position between the atrioventricularorifices and that of the pulmonary valve. Theright edge of the ventricular mass is sharp(acute) when seen from the apex, in contrastto the left margin which is much morerounded (obtuse margin) (fig 1A). Vortices areseen on the tips of both ventricles, althoughthe left vortex is always sharper and forms theapex of the heart itself (fig 1A).

These typical external morphological fea-tures of the normal hearts were altered in themalformed hearts. In our first case, charac-terised by rudimentary formation of the pul-monary valve, the anterior wall of the rightventricle in the outflow tract was dilated, whilethe aortic root was displaced markedly right-wards (figs 1B and 2C). Right ventricularhypertrophy was obvious, and both margins ofthe ventricular mass were obtuse. Moreover,at the level of the apex, the right vortex was asimilar size to the left (fig 1B). The interven-tricular grooves were clearly evident.When there was pulmonary inftmdibular

stenosis together with valvar stenosis, rightventricular hypertrophy remained a significantfeature (fig 1C). A bifid apex was formed byboth ventricles, but the right margin remainedsharp. Such morphological features wereobserved irrespective of the nature of pul-monary valve stenosis.When tetralogy was complicated by pul-

monary atresia, right ventricular hypertrophywas particularly marked, enlarging the antero-posterior diameter of the heart and givingobtuse margins on both right and left sides (fig1D). Although, when seen from the front orposteriorly, the apex seemed to be formed byboth ventricles (figs 2E and F), when viewedend-on it was shown to be formed only by thevortex of the left ventricle (fig 1D).

MYOARCHITECTUREIn all the hearts it was possible to distinguishthree different layers of muscle fibres: superfi-cial (subepicardial), deep (subendocardial),and middle. The distinction between one layerand the next was made on the basis of achange in the orientation of the muscle fibres.No discrete planes or fibrous septa were pre-

Figure 1 Apical views ofthe hearts ofnormal (A)and tetralogy (B,C,D)specimens, showing thearrangement of thesuperficialfibres at theapex. In (A) note theanterior (AH) andposterior (PH) horns at thelevel of the left vortex.Note the hypertrophy of theright ventricle and themarked separation of thevortices in the case withabsence of the leaflets of thepulmonary valve (B) andsubpulmonary infundibularstenosis (C), with somefibres of the diaphragmaticaspect (arrow) of the heartending in the right vortex.In pulmonary atresia (D)only the left vortex wasobserved, showing anincrease offibres at itsanterior horn (AH), withboth margins of the heartbeing very obtuse. P,pulmonary trunk.

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Sanchez-Quintana, Anderson, Ho

Figure 2 Front and back views of the hearts ofnormal (A and B) and tetralogy (C-F) specimens, showing the arrangement of the superficial layer. In Aand B the fibres run obliquely across the interventricular grooves (arrow). Note the right ventricular hypertrophy in the case with rudimentary formation ofthe pulmonary valve (C and D), and pulmonary atresia (E and F), with fibres more obliquely or longitudinally orientated in the right ventricle ofspecimens with tetralogy. A, aorta; P, pulmonary trunk; T and M, tricuspid and mitral valvar orifices; star; longitudinal and transversefibres.

sent between the layers. Obvious differenceswere noted, however, in the arrangement andorientation of the layers in the ventricularwalls, both between right and left ventriclesand between the normal and malformedhearts.

Superficial layerThe architecture of the superficial layershowed features common for both normalhearts and those with tetralogy. This layer wastraced from the base of the heart toward theapex, extending from one ventricle to theother (fig 2). At the level of the apex the super-ficial layer invaginated in a spiral pattern toform a deep or subendocardial layer for eachventricle. The invagination at the left vortexformed anterior and posterior horns. Theanterior horn was derived from muscle fibresarising from the posterior region of the base ofthe heart, whereas the posterior horn wasformed by fibres arising from the anteriorregion of the base (fig 1). The fibres on thesternocostal aspect ran obliquely from right toleft, crossing the anterior interventriculargroove (fig 2A, C, and E), while on thediaphragmatic aspect they ran left to right andcrossed the posterior interventricular groove(fig 2B, D, and F). In normal hearts, the fibresin the superficial layer ran more horizontally inthe right than in the left ventricle (figs 2A andB).

Markedly different features were seen inhearts with tetralogy. At the base, the speci-

men with rudimentary formation of the leafletsof the pulmonary valve showed a more obliqueorientation of the fibres distally on the dilatedsubpulmonary outflow. In contrast, in thespecimens with pulmonary atresia, the fibresshowed an almost circular arrangementaround the aorta. An intermediate configura-tion was found in the cases with pulmonaryvalvar and infundibular stenosis.The specimen with rudimentary leaflets of

the pulmonary valve and those withpulmonary valve stenosis showed a markedseparation between the ventricular vortices atthe apex, with major development of the rightvortex, composed of muscle fibres arisingdirectly from the posterior region of the base(figs 1B and C). In contrast, in pulmonaryatresia, the fibres formed a spiral pattern onlyaround the left ventricular vortex, with anincrease in the fibres of the anterior horn (fig1D).The sternocostal right ventricular fibres

were more obliquely orientated than for thenormal heart, particularly in the hearts withpulmonary atresia (fig 2E). At the diaphrag-matic aspect, the left ventricular fibres ran in amore oblique orientation, again markedly so inpulmonary atresia, where they acquired analmost longitudinal orientation (fig 2D and F).In all the hearts, the fibres were irregularly ori-entated in the upper third of the diaphrag-matic surface of the right ventricle, next to theright margin, with longitudinal fibres inter-mingling with transverse ones (fig 2F).

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Deep layerIn the normal hearts the deep or subendocar-dial layer comprised preferentially arrangedlongitudinal fibres which passed through thevortices and coursed in three different direc-tions, toward the papillary muscles, to the atri-oventricular and arterial orifices, and to themembranous interventricular septum.

Multiple differences were seen in the heartswith tetralogy. In the case with absent or rudi-mentary pulmonary leaflets or those with pul-monary valvar stenosis, the fibres from theright vortex ran upward longitudinally to fol-low the septomarginal trabeculation and theventriculo-infundibular fold to the tricuspidannulus (fig 3A). In all cases, as the fibresapproached the site of the ventricular septaldefect, they divided. Some fibres bordered thedefect anteriorly, following the outlet septum,while others extended posteriorly, following

the junction of the ventriculo-infundibularfold with the septomarginal trabeculation (fig3B-D). The fibres above the outlet septum ranupwards, reaching the pulmonary valve toform part of the subpulmonary infundibulum(fig 3B and C). The fibres surrounding theventricular septal defect were closely related tothe leaflets of the aortic valve. In those withpulmonary infundibular stenosis, the sep-toparietal trabeculations were formed by athick bundle of fibres arranged longitudinally,which reached the pulmonary valve superiorlyto narrow the subpulmonary outflow tract.

In the cases with pulmonary atresia the out-let septum was either rudimentary or absent,with the aorta being the only arterial outlet.The subendocardial fibres ascended longitudi-nally in the right ventricle (fig 3D). Towardthe rim of the ventricular septal defect somefibres extended anteriorly and ran towards the

Figure 3 Deep layer ofthe right ventricle (A, B,C, D) and left ventricle(E, F) from specimenswith tetralogy that havebeen sectioned and openedlongitudinally. Note thatin the case withrudimentary leaflets of thepulmonary valve (A), thelongitudinally orientatedfibres in the septomarginaltrabeculation continue astransversefibres in theoutlet septum, and that insubpulmonary infundibularstenosis (B) hypertrophy ofseptoparietal trabeculationsnarrows the pulmonaryoutflow tract (arrows).The fibres that border theventricular septal defectand the overriding aorticvalve (C) run toward theaortic valve. In the case ofpulmonary atresia (D) thefibres near the rim of theventricular septal defectdivide to pass anteriorlyand posteriorly to thedefect. In the left ventricle(E, F) the fibres dividenear the rim to approachthe aortic valve. A, aorta;asterisk, ventricular septaldefect; ML, middle layer ofthe left ventricle; OS,outlet septum; P,pulmonary trunk; ST,septomarginaltrabeculation; T, tricuspidvalvar orifice; PM,papillary muscle.

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Figure 4 Front (A) andapical (B) views of thenormal heart showing acircular pattern of musclefibres in the middle layer ofthe left ventricle. Front(C) and interventricular(D) views in a specimenwith tetralogy (pulmonaryatresia) show the middlelayer together withhypertrophy of the rightventricle (C) but at thelevel of the ventricularseptal defect (asterisk)there is discontinuity andonly the deep layer (arrow)can be seen. A, aorta; LV,left ventricle; RV, rightventricle; P, pulmonarytrunk.

attachment of the right and left leaflets of theaortic valve. Others ran towards the non-coro-nary leaflet of the aorta (fig 3D and E). Athird, smaller, group of fibres crossed the rimof the defect and interwove with subendocar-dial fibres of the left ventricle (fig 3E).The arrangement of the subendocardial

fibres in the left ventricle was very similar in allhearts, approximating to the arrangement seenin the right ventricle in cases with pulmonaryatresia. Other fibres of the left ventricle werearranged longitudinally, with insertions intothe papillary muscles and the mitral annulus(fig 3F).

Middle layerIn normal hearts a thick middle layer ofmyocardial fibres was found only in the leftventricle, where it formed an almost circularpattern, with no apparent insertion into theaortic-mitral annulus. No proper middle layerwas found in normal right ventricles, with nochanges seen in the orientation of the fibres inthe mid-portion of the ventricular wall (fig 4Aand B).

Several changes were seen in the hearts withtetralogy. In all cases, the fibres of the left ven-tricle showed a marked circular arrangement(figs 4C and D). Most significantly, again inall types, the right ventricle possessed a well-defined middle layer composed of circularfibres. The layer was discontinuous only at thelevel of the ventricular septal defect, where thefibres of the subendocardial layer of the rightventricle could be seen (fig 4C and D).

DiscussionOur findings demonstrate a normal pattern ofventricular myoarchitecture characterised, inthe left ventricle, by three concentric layers(superficial or subepicardial, middle, and deepor subendocardial). Only superficial and deeplayers, in contrast, are found in the normalright ventricle. These findings are in keepingwith several earlier descriptions,569 10 but are inmarked contrast to the hypothesis which pro-poses a single system of spiralling fibresextending across the ventricles from the aorticto the pulmonary root.8Marked departures from this normal

arrangement were found in all hearts studiedwith the anatomical features of the variousmorphologic subsets of tetralogy of Fallot.Despite some continuing disagreementsregarding the interpretation and nomenclatureof muscle bands surrounding the ventricularseptal defect,'5-17 and disagreements about theextent of subpulmonary infundibular steno-SiS,16 18 it is generally agreed that the morpho-logical hallmarks that unify tetralogy are aventricular septal defect, subpulmonaryinfundibular stenosis, biventricular connectionof the leaflets of the aortic valve, and hypertro-phy of the right ventricle. The classic anatomi-cal feature that is diagnostic in most heartswith tetralogy of Fallot is antero-cephaladdeviation of the outlet septum,16 such that thisseptum takes up an exclusively right ventricularposition. Despite their obvious similarities,nonetheless, no two cases of tetralogy areexactly alike,19 a feature of major surgical sig-

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nificance. These disparities were further con-firmed by our dissections of the myocardialarchitecture. Despite the individual differ-ences, we could divide our material into onespecimen with absence of the leaflets of thepulmonary valve, and others with either pul-monary stenosis or with pulmonary atresia. Inthe first two subsets, the anatomical hallmark,the antero-cephalad deviation of the outletseptum, is readily apparent irrespective of thelength of the subpulmonary infundibulum.The outlet septum was deviated in a similarfashion in one of the hearts with pulmonaryatresia, but was absent in the other. It isarguable whether hearts with pulmonary atre-sia should be included in the overall categoryof tetralogy. Indeed, our specimen withabsence of the outlet septum exhibits overridingof the aorta, pulmonary atresia at the ven-triculo-arterial junction, and a doubly commit-ted and juxta-arterial ventricular septal defect.But despite having pulmonary atresia, ratherthan stenosis, these two hearts are still moreclosely related to tetralogy than to other sub-sets of hearts with different segmental combi-nations which are also described as pulmonaryatresia with ventricular septal defect.20Taken together, these morphological types

differ from the normal heart and among them-selves not only in terms of ventricular shape,but also with regard to the architecture of theventricular muscle fibres. In general, the ven-tricular shape was dominated by the state ofthe right muscular outlet. In the presence ofrudimentary formation of the leaflets of thepulmonary valve, the outlet tract was dilated,with more obtuse angles of the margins than inthe normal ventricles. In contrast, the caseswith pulmonary stenosis show obvious hyper-trophy of the right ventricle, but with variouslengths of outlet tracts, albeit usually largerthan normal. The ventricular shape is moreangular than in the heart with rudimentaryleaflets of the pulmonary valve. In our particu-lar hearts with pulmonary atresia, the subpul-monary outlet tract of the right ventricle wasmarkedly reduced in one, and lacking in theother. The margins of the ventricles showedthe most obtuse angles. In all forms of tetral-ogy of Fallot, therefore there is an altered ven-tricular configuration.

It has been suggested that the shape of theheart reflects an adaptation to the needs ofboth systole and diastole, and that thosechanges in ventricular shape may in them-selves produce cardiac dysfunction.2' In thisrespect, therefore, it may well be significantthat the basic architecture of the myocardiumin tetralogy is also very different from that inthe normal heart. The most significant findingis a circular middle layer in the right ventricle.Previous studies in normal hearts have demon-strated the existence of such a middle layer inthe left, but not in the right ventricle.5-7 10 Inthe hearts with tetralogy, the overall architec-ture is markedly influenced by the presence ofright ventricular hypertrophy. Earlier studieshave already reported that, when the right ven-tricle is hypertrophied13 21 22 it exhibits anincrease of fibres at the level of the ventricular

septum and right ventricular outlet, and as aconsequence the architecture of the ventricu-lar septum shows a convexity towards the left.Haemodynamic, histological, and morphomet-ric studies have previously revealed hyper-trophic changes in both ventricles intetralogy.2'25 It could be that the right ventric-ular middle layer is acquired postnatally as anadaptive change to the ventricular load, butthe finding of a middle layer in the specimenfrom our youngest patient, a neonate, and alsoin the oldest patient, who was 59, suggests thatthe myocardial architecture is a further charac-teristic of the abnormal cardiac development.Clinical studies have shown persistentdepressed function of the right ventricle insome cases, even subsequent to surgicalrepair.2$28 In these, increased myocardialfibrosis has been proposed as an importantfactor in restricting myocardial compli-ance.2629 The abnormal myoarchitecture mustbe considered a potential additional factor. Ithas been demonstrated that rearrangement inorientation of muscle fibres, and changes ininterstitial connective tissue matrix, can influ-ence both the electrical and mechanical func-tion of the heart.30 31 Our previous studies32showed that a middle layer was lacking fromthe right ventricle of normal hearts in humanspecimens ranging in age from fetuses of 13weeks' gestation to adults aged 90. We neednow, therefore, to explore the clinical signifi-cance of these anatomical findings. Our bias isthat in tetralogy the abnormal ventriculararchitecture already present at birth representsan adaptative change in formation of themyocardial fibres, but we do not yet know atwhich developmental stage the middle layer isformed.

LIMITATIONS OF THE STUDYGood necropsy examples of Fallot's tetralogy,especially those from subjects who have nothad previous surgical interventions, arebecoming increasingly scarce. For this study,we selected specimens from our collection thatwere basically intact; this will further limit thenumbers that will be available for study in thefuture. For this reason, we have includedhearts which, at first glance, are grossly differ-ent in their morphology but, nonetheless, sat-isfy the accepted criteria for description astetralogy of Fallot. We did not study manyhearts, none the less, all show the same basicdifferences in from normal myoarchitecture.We cannot increase the numbers because suchan approach would mean destroying all ourspecimens with tetralogy, leaving a wide gap inthe teaching value of our collection. Rather,we hope our findings will generate interest inthis method of investigation among other mor-phologists, especially in centres that have col-lections of necropsied hearts that wereestablished before the early days of cardiacsurgery.

It is also pertinent that we did not attemptto quantify the changes in orientation of thefibres. Our technique is based on gross dissec-tion, which eventually leaves little of the speci-men. For meaningful assessment of the

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angular changes, histological sections throughthe full thickness of the ventricular walls arepreferable,9 and this also is a fruitfill area forfuture study.

During this investigation D S-Q was supported by grantDGICYT (PR95-057) from the Spanish government. SYHand RHA are supported by the British Heart Foundation.

1 Harvey W. An anatomical disquisition on the motion of theheart and blood in animals (1628). In: Willis FA, KeysTE, eds. Cardiac Classics. London: Henry Kimpton.1941:19-79.

2 Pettigrew JB. On the arrangement of the muscular fibres inthe ventricles of the vertebrate heart, with physiologicalremarks. Philos Trans R Soc Lond 1865;154:445-500.

3 Krehl L. Kenntniss der Fullung und Entleerung desHerzens. Abhandl Math Phys Kl Koniglichen Saechs GesWiss 1891;29:341-62.

4 Mall FP. On the muscular architecture of the ventricles ofthe human heart. AmJ7Anat 1911;11:211-66.

5 Robb JS, Robb RC. The normal heart, anatomy and physi-ology of the structural units. Am Heart 7 1942;23:455-67.

6 Grant PP. Notes on the muscular architecture of the leftventricle. Circulationl965;32:301-8.

7 Streeter DD. Gross morphology and fiber geometry of theheart. In: Beme RM, Sperelakis N, Geiger SR, eds.Handbook of physiology, the cardiovascular system.Baltimore: Williams and Wilkins. 1979:61-112.

8 Torrent-Guasp F. La estructura macroscopica del miocardioventricular. Rev Esp Cardiol 1980;33:265-87.

9 Greenbaum RA, Ho SY, Gibson DG, Becker AF,Anderson RH. Left ventricular fibre architecture in man.Br Heartj3 1981;54:248-63.

10 Fernandez-Teran MA, Hurle JM. Myocardial fiber archi-tecture of the human heart ventricles. Anat Rec 1982;204:137-47.

11 McLean MR, Prothero J. Coordinated three-dimensionalreconstruction from serial sections at macroscopic andmicroscopic levels of resolution: the human heart. AnatRec 1987;219:434-9.

12 Usson Y, Parazza F, Jouk PS, Michalowicz G. Method forthe study of the three-dimensional orientation of thenuclei of myocardial cells in fetal human heart by means ofconfocal scanning laser microscopy. J Micros 1994;174:101-10.

13 Becker AE, Caruso G. Congenital heart disease: a mor-phologist's view on myocardial dysfunction. In: BeckerAE, Losekoot TG, Marcelletti C, Anderson RH. eds.Paediatric cardiology. Vol 3. London: Churchill Living-stone. 1981:307-23.

14 Sanchez-Quintana D, Hurle JM. Ventricular myocardialarchitecture in marine fishes. Anat Rec 1987;217:263-73.

15 Rosenquist GC, Sweeney U, Stemple DR, ChristiansonSD, Rowe RD. Ventricular septal defect in tetralogy ofFallot. Am _J Cardiol 1973;31:749-54.

16 Becker AE, Connor M, Anderson RH. Tetralogy of Fallot:a morphometric and geometric study. Am J Cardiol1975;35:402-12.

17 Anderson RH, Becker AE, Van Mierop LHS. What shouldwe call the "crista"?. BrHeart3r 1977;39:856-9.

18 Van Praagh R, Van Praagh S, Nebesar RA, Muster AJ,Shina SN, Paul MH. Tetralogy of Fallot. Under-development of the pulmonary infundibulum and itssequelae. Am Jf Cardiol 1970;26:25-33.

19 Lev M, Eckner FAO. The pathologic anatomy of tetralogy ofFallot and its variations. Dis Chest 1964;45:251-61.

20 Anderson RH, Devine W, del Nido P. The surgicalanatomy of tetralogy of Fallot with pulmonary atresiarather than pulmonary stenosis. J Card Surg 1991;6:41-59.

21 Hutchins GM, Bulkley BH, Moore GW, Piasio MA, LohrFT. Shape of the human cardiac ventricles. Am 7 Cardiol1978;41 :646-54.

22 Sanchez-Quintana D, Garcia-Martinez V, Hurle JM.Myocardial fiber architecture in the human heart.Anatomical demonstration of modifications in the nor-mal pattern of ventricular fiber architecture in a mal-formed adult specimen. Acta Anat 1990;138:352-8.

23 Matsuda H, Hirose H, Nakano S, Kishimoto H, Kato H,Kobayashi J, et al. Age-related changes in right and leftventricular function in tetralogy of Fallot. Jpn Circ Res1986;50: 1040-3.

24 Toussaint M, Planche C, Duboc D, Pfister A, Da Lage C,Guerin F. Left ventricular ultrastructure in pulmonarystenosis and in tetralogy of Fallot. Virchows Archiv-APathol Histopathol 1987;411:33-8.

25 Alvarez L, Aranega A, Contreras JA, Lopez-Torres J,Fernandez JE. Morphometric study of right ventricle in32 cases of tetralogy of Fallot. Herz 1988;13:41-8.

26 Jarmakami JM, Nakazawa M, Isabel-Jares J, Marks RA.Right ventricular function in children with tetralogy ofFallot before and after aortic-to-pulmonary shunt.Circulation 1976;53:555-61.

27 Lange PE, Onnasch DEW, Bernhard A, Heintzen PH. Leftand right ventricular adaptation to right ventricular over-load before and after repair of tetralogy of Fallot. Am JTCardiol 1982;50:786-94.

28 Gatzoulis MA, Clark AL, Cullen S, Newman CEH,Redington AN. Right ventricular diastolic function 15 to35 years after repair of tetralogy of Fallot. Circulation1995;91:1775-81.

29 Krymysky LD. Pathologic anatomy of congenital heart dis-ease. Circulation 1965;32:814-27.

30 Weber KT, Sun Y, Tyagi SC, Cleutjens JPM. Collagennetwork of the myocardium: function, structural remod-elling and regulatory mechanisms. Jf Mol Cell Cardiol1994;26:279-92.

31 LeGrice IJ, Smaill BH, Chai LZ, Edgar SG, Gavin JB,Hunter PJ. Laminar structure of the heart: ventricularmyocyte arrangement and connective tissue architecturein the dog. Amj Physiol 1995;38:H571-82.

32 Sanchez-Quintana D, Garcia-Martinez V, Climent V,Hurle JM. Morphological changes in the normal pattern ofventricular myoarchitecture in the developing humanheart. Anat Rec 1995;243:483-95.

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Ventricular myoarchitecture in tetralogy of Fallot · Nine specimens from cases of tetralogy of Fallot and four normal hearts were studied. The specimens with tetralogy of Fallot