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Embryology of Some Congenital Cardiac Anomalies

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Embryology of Some Congenital Cardiac Anomalies Thorax: first published as 10.1136/thx.20.2.158 on 1 March 1965. Downloaded from Thorax (1965), 20, 158. Embryology of some congenital cardiac anomalies E. W. T. MORRIS From St. Thomas's Hospital Medical School, London The purpose of this paper is to propose explana- reptiles seems open to doubt since the living tions for the nature of some commonly occurring orders of these two classes are, for the most part, congenital cardiac anomalies in terms of human highly specialized and therefore less likely to embryology. The basic difficulty in any such resemble their early common ancestor in the attempt is that, in the course of the development structure and form of their organs. of the human heart, there are two stages. During The steps in ontogeny only repeat phylogeny the first, the embryological process results in the in a very general way. For example, in its early formation of a four-chambered heart separated stages the mammalian heart resembles the fish by an interatrial and interventricular septum into heart in that each chamber is undivided, and the a right and left part; during the second, the organ blood is impelled by it into a single ventral aorta so formed grows in size, and changes occur in the and thence into paired aortic arch arteries. At form and proportions of its component parts to a later stage, the common chambers become achieve those of the definitive heart. As Grant divided into a right and a left, a step that occurs (1962) points out, little is known about the second in phylogeny when pulmonary respiration is stage. In congenital heart disease, since the heart established. has to function continuously so long as it is alive, At the most these stages may resemble earlycopyright. errors of form occurring in the first period are steps in the embryology of the presumed ancestor likely to influence changes occurring in the second. and not the definitive heart of such a precursor. These latter may be such as to render difficult the There seems little justification now for describing elucidation of those errors of formation in the congenital abnormalities of the heart in terms of first stage which is the object of this paper. an atavism to the form of heart found in a http://thorax.bmj.com/ The views put forward are based on the dissec- modern reptile. Moreover, these explanations tion of 25 infant hearts which showed such were mainly given at a time when the account abnormalities (see Table). This study was under- of the development of the mammalian heart taken because views still current on the aetiology showed many gaps. Now that these have been of some forms of congenital heart disease are largely filled in to give an almost complete picture thought to be erroneous. The earlier ones (Keith, it is worth while to try to explain examples of 1902, 1905) were propounded, in the light of some congenital abnormalities in terms of failure theories then current, that ontogeny repeated either of initiation or completion of some step phylogeny, and the abnormalities were conse- or steps known to occur in the normal heart. on September 25, 2021 by guest. Protected quently seen as arrests of development at a stage When this has been done some abnormalities when the evolving heart resembled some phylo- will remain which are inexplicable in terms of genetic precursor of man, such as a reptile. These simple arrest: in these, some stage has not views have been elaborated (Spitzer, 1923) and proceeded normally. In attempting to unravel are included in recent clinical books (Brown, what has happened, it is legitimate to try to 1950; Taussig, 1960) and seem widely held despite confine the explanation to a presumed diversion recent papers (Kramer, 1942; Foxon, 1955) which of a step known to occur normally. Equally, in cast doubts on them. accordance with Ocean's dictum 'essentia non sunt There is a central difficulty inherent in any multiplicanda praeter necessitatem', it is undesir- attempt to explain abnormalities on the assump- able to introduce into the explanation a stage not tion that they represent a deviation to the form known to occur in normal human embryology. of a phylogenetic ancestor: no one knows, or is An assumption of this sort is made by some ever likely to know, what the hearts of the writers (Lev and Saphir, 1945) when they amphibian and reptilian ancestors of man were postulate that, in the development of an abnormal like. The assumption that they would have heart, the bulbar septum is derived from ridges resembled the hearts of modern amphibians or which normally occur in the developing heart of 158 Thorax: first published as 10.1136/thx.20.2.158 on 1 March 1965. Downloaded from Embryology of some congenital cardiac anomalies 159 " + + vI "fl ~ ~__ + ++ + N'i + + + + -l + + eo. + + IXlo + o1 ++ + + + We + + m1 ++ + + cn :I + + as2e1 + Y# I " ++ ++ + + - I + + o z - + copyright. z- , ,I z r + + + ;h I ± I Ea 0< -t1 o z + + http://thorax.bmj.com/ + + 02 .X + + + + 1; 9LO ++ + + + .5 "!+ + I °r;;4 I I-I + I C*** * * * .... on September 25, 2021 by guest. Protected C 0) 00 o . ..o E U k. .2C .~ 0OC Y Co~~~~~~~~~0 ~~~::~~~:: 0 -: 0)0) U 0.. ..00 0 2. 0) Y * )!;' 4 t>tU0c ).. LU U.0~~~~~~~~~~~~~~~~~~~~~~~~~~~~. a ,o .0 C,0 .0 ~~UU0)~~~~~ ~~0 o 0S' : ID oAO o co 0 000 C U~~~~~~r -. Thorax: first published as 10.1136/thx.20.2.158 on 1 March 1965. Downloaded from 160 E. W. T. Morris modern reptiles in order to explain overriding of (ii) the interventricular parts of the pars the aorta and transposition of the great arteries. membranacea septi, (c) the proximal, and (d) the At no stage in the development of the human distal bulbar swellings, and (e) the aortico- heart are there two ventral aortae arising pulmonary septum. independently from the ventricles as there are in Of these, the last to develop is the inter- typical modern reptiles. This is, of course, not to ventricular part of the membranous septum be confused with the fact that double aortic arches (Odgers, 1938). If this fails to develop then the may occur as the result of the persistence of both defect is found under the superior part of the right and left fourth arch arteries, for, when these septal cusp of the tricuspid valve and below the are found, they are connected to the left ventricle crista supraventricularis (Fig. l) and represents by a single ascending aorta. a persistence of the interventricular foramen After some study of and thought about the which normally exists at this stage of develop- specimens, various features and patterns of ment. Such a defect is bounded ventrally and features displayed by them began to emerge. Even inferiorly by the upper border of the muscular in the most complicated abnormalities it was septum, above by the bulbar septum-that is the found possible to suggest embryological explana- complete septum formed from elements (c), (d), tions without invoking any steps now known not to occur in normal development. These observa- tions and the embryological explanation for them Abbreviations used in plates: A W, wall ofaorta; AS V(R), are given below. The terms 'proximal' and 'distal' right septal (coronary) cusp of aortic semilunar valve; relate to the direction of blood flow through the ASV(L), left septal (coronary) cusp of aortic semilunar heart. valve; ASV(N), nonseptal (non-coronary) cusp of aortic semilunar valve; AZV, azygos vein; BS, bulbar septum; CAV(S), superior cusp of common atrioventricular valve; ABNORMALITIES OF THE VENTRICLE AND BULBUS CAV(I), inferior cusp of common atrioventricular valve; CORDIS CS, crista supraventricularis; CVC, common venous chamber; IVC(L), left inferior vena cava; IAS, interatrialcopyright. Reference to embryological texts (Hamilton, septum; MS, muscular part of interventricular septum; Boyd, and Mossman, 1962; Kramer, 1942; PA(L), left pulmonary artery; PA(R), right pulmonary Odgers, 1938) shows that defects in the septation artery; PMS(A), atrioventricular part of pars mcn7- of this part of the heart can result in varying branacea septi; PMS(I), interventricular part of pars degrees of failure either of development or of membranacea septi; PMS(IR), rudimentary interventricu- http://thorax.bmj.com/ union the of the larpart ofpars membranacea septi; PTA, atretic pulmonary of component parts septum. trunk; PTS, stenotic pulmonary trunk; PSV(L), left septal There are five structures or groups of structures cusp of pulmonary semilunar valve; PS V(R), right septal involved in the formation of this septum; from cusp of pulmonary semilunar valve; PSV(N), non-septal proximal to distal, (a) the muscular inter- cusp ofpulmonary semilunar valve; PV, pulmonary veins; ventricular septum, (b) the atrioventricular SVC(L), left superior vena cava, TVS, septal cusp of cushions forming both (i) the atrioventricular, and right atrioventricular valve. on September 25, 2021 by guest. Protected - FIG. 1. Right side of interventricular septum showing position of interven- f- tricular membranous part (x). Dotted line marks site of fused bulbar ridges and rod A marks site ofseptal defect. 1.t .I. Thorax: first published as 10.1136/thx.20.2.158 on 1 March 1965. Downloaded from Embryology of some congenital cardiac anomalies 161 and (e) already described; it is limited dorsally TVS by the atrioventricular part of the membranous septum. This is continuous with the right wall of the aorta in the region below and between the right coronary and non-coronary cusps of the aortic valve, and has the superior part of the septal cusp of the tricuspid valve continuous with it ventrally (Fig. 2). Ms () FIG. 3. Heart 2 showing aorta, septal cusp of tricuspid valve, rudiment of interventricular membranous septum, and muscular septutm; a small piece has been excisedfirom the latter.
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