Table Of ContentSitzungsberichte der Heidelberger Akademie der Wissenschaften
Mathematisch-naturwissenschaftliche Klasse
Jahrgang 1990, 2. Abhandlung
G. Conte F. Giannessi M. Cornali
Hemodynamics and the
Development
of Certain Malformations
of the Great Arteries
B. Chuaqui
Comment
With 13 Figures
Vorgelegt in der Sitzung vom 18. November 1989
von Wilhelm Doerr
Springer-Verlag Berlin Heidelberg New York
London Paris Tokyo Hong Kong
Prof. Dr. Giuseppe Conte
Francesco Giannessi
Istituto di Anatomia Umana Normale, Facolta di Medicina
e Chirurgia dell'Universita degli Studi di Pisa
Via Roma 55, 56126 Pisa, Italy
Mario Cornali
Cardiovascular Radiology, Hospital of Massa, 54100 Massa, Italy
Benedicto Chuaqui
Pontificia Universidad Cat6lica de Chile
Departamento de Anatomia Patol6gica
Casilla 114-D, Santiago, Chile
ISBN-13: 978-3-540-52362-8 e-ISBN-13: 978-3-642-46699-1
DOl: 10.1007/978-3-642-46699-1
LC card number: 12-8903
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Acknowledgement
This work was supported by the Italian Ministry
of Education. The authors wish to thank
Mr. Vincenzo Reale for his expert secretarial assistance
in the preparation of this manuscript.
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Contents
G. CONTE, F. GIANNESSI, M. CORNALl
Hemodynamics and the Development of Certain Malformations of the
Great Arteries ................................................... 9
B. CHUAQUI
Comment....................................................... 36
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Hemodynamics and the Development of Certain Malformations of the
Great Arteries
G. Conte, F. Giannessi, M. Cornali
Summary
The Authors hypothesize variations in the course of the bloodstreams in the
ventricular outflow tract and consequent changes in distribution to the 6th and
4th branchial arterial arches; these are thought to be the result of primary in
tracardiac or extracardiac events. The Authors have also studied the changes in
the way the endocardial septal ridges are arranged in the ventricular outflow tract.
They have thus theoretically identified 13 probable hemodynamic patterns, 1 in
the normal and 12 in the abnormal developing heart: in developing "complete
transposition" and in "corrected transposition", in developing interruption of the
aortic arch and in the development of other morphologically unidentified vascu
lar anomalies. The Authors have studied various hypotheses previously advanced
by other research-workers and have compared these with their own theoretical
patterns.
Introduction
The influence of the bloodstreams on the normal and abnormal development
of the heart is a controversial matter (RYCHTER 1962; JAFFEE 1970, 1978;
GOERTTLER 1955, 1956, 1970a; HEINE 1975; DE LA CRUZ et al. 1977; GESSNER
1978; MOORE and HUTCHINS 1978; PEXIEDER 1978a; ORTS LLORCA et al. 1980;
VAN PRAAGH et al. 1980; CLARK 1984; YOSHIDA et al. 1983; RUCKMAN 1985;
MANASEK et al. 1986; STEWARf et al. 1986).
Various conflicting hypotheses have been put forward as to the dysmor
phogenesis of the ventricular outflow tract but no evidence has been found to
support these hypotheses (for an exhaustive review of this question, see: SPITZER
1923; PERNKOPF and WIRTINGER1935; DOERR 1939, 1943, 1950, 1952, 1955a,
1955b, 1987; SHANER 1962; DE LA CRUZ and DA ROCHA 1956; GOERTTLER
1958, 1970b; BARfHEL 1960; BANKL 1972; CHUAQUI and BERSCH 1972, 1973;
ANDERSON et al. 1974; GOOR and LILLEHEI 1975; PEXIEDER 1978a; BERSCH
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10 G. Conte et al.
and DOERR 1976; CHUAQUI 1979; VAN MIEROP and PATTERSON 1980; VAN
PRAAGH et al. 1980; DOR and CORONE 1981, 1985; STEDING and SEIDL 1981).
THOMPSON and FITZHARRIS (1985) and THOMPSON et al. (1987) underline
the contradictions and uncertainties of the various experimental results concern
ing truncal septation. THOMPSON and FITZHARRIS (1985) summarize as follows:
"Most of the descriptive evidence in support of the classical «fusion without rota
tion» model of TS can also be interpreted as supporting alternative explanations
involving retraction and rotation of tissue along the outflow. ... The apparent
rotation and descent of the valve sites relative to the rest of the outflow tract is
probably more real than illusory. Despite clear differences between the two prin
cipal models discussed above, experimental demonstrations of relative tissue
movements during Ts remain ambiguous" (p. 177).
In agreement with the findings of LANGER (1894), WATHERSTON (1918),
CHANG (1932), Los (1969, 1978), CONTE and ARRIGONI (1967), McBRIDE et al.
(1981), FANANAPAZIR and KAUFMAN (1988) and VUILLEMIN and PEXIEDER
(1989), we found (CONTE and GRIECO 1980b) that in the hearts of rabbit em
broys the endocardial spiral septal ridges extend from the ventricular extremity to
the aortic sac in the outflow tract of the ventricles. These ridges would appear
to be moulded by the intracardiac blood as a negative mould of the streams
(BREMER 1932; ROMHANYI 1952; GOERTTLER 1955, 1970a; BARTHEL 1960; JAF
FEE 1965, 1967; LEYHANE 1969).
According to BREMER (1932), JAFFEE (1965, 1967) and LEYHANE (1969), the
bloodstreams run in the outflow tract of the ventricles with a spiral course from
right to left: the left stream goes into the 4th and the right stream into the 6th
branchial arterial arches. But, according to YOSHIDA et al. (1983), the
bloodstreams do not follow a spiral course and the blood of the right om
phalomesenteric vein flows into the left branchial arterial arches while the blood
of the left omphalomesenteric vein flows into the right branchial arterial arches.
Recently, we saw in a rabbit embryo heart (CONTE and GIANNESSI 1987) that
the outflow tract of the right ventricle joins together with the 4th branchial
arterial arches and the outflow tract of the left ventricle joins together with the
6th branchial arterial arches; the endocardial septal ridges are developed rec
tilinearly, becoming A-3 and B-1. Relating the morphology of the anomalous sep
tal ridges A-3 and B-1 to the course of the bloodstreams in the ventricular outflow
tract, as described by JAFFEE (1965, 1967), LEYHANE (1969) and YOSHIDA et al.
(1983), we hypothesize variations in the hemodynamics that should provide a bet
ter understanding of both normal and maldeveloped formalgenesis of the septum
of the ventricular outflow tract.
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Hemodynamics and the Development of Certain Malformations 11
Hypothesis on the Variations of the Bloodstreams Concerning the 6th and the
4th Branchial Arterial Arches
We have calculated, theoretically, every possible change which might occur in
the course of the bloodstreams concerning the 6th and the 4th, right and left,
branchial arterial arches. We have also examined the lay-out of the endocardial
septal ridges, as if they really were moulded by the bloodstreams in the ventricular
outflow tract. In this way, we have also identified, hypothetically, the for
malgenesis of certain corresponding malformations of the Great Arteries.
Terminology
The area of the embryonic heart from the bulbus to the aortic sac will be refer
red to as the outflow tract of the ventricles. The endocardial spiral septal ridges that
develop normally into the ventricular outflow tract are the septal ridges A-1 and
B-3, the forerunners of the septum of the outflow tract of the ventricles (CONTE
and GRIECO 1984). The proximal parts A and B (LANGER 1894; TANDLER 1913)
of the septal ridges A-1 and B-3 are the dextrodorsal and sinistroventral conus
swellings referred to by VAN MIEROP et al. (1963). The distal parts 1 and 3
(LANGER 1894; TANDLER 1913) of the septal ridges A-1 and B-3 are the dextro
dorsal and sinistro-ventral truncus ridges described by KRAMER (1942), and the
sinistroinferior and dextrosuperior truncus swellings referred to by VAN MIEROP et
al. (1963). The dorsal ridge 2 (pulmonary) and the ventral ridge 4 (aortic) described
by LANGER (1894) and TANDLER (1913) are the intercalated valve swellings refer
red to by KRAMER (1942) and VAN MIEROP et al. (1963).
Results
We shall begin with the normal bloodstreams and with the endocardial septal
ridges that they mould; after which, we shall examine the other hemodynamic
patterns.
Case 1. The bloodstreams twist normally from right to left. The right
bloodstream flows into the 6th branchial arterial arches and the left bloodstream
flows into the 4th branchial arterial arches; the septal ridges are moulded, twisted
from right to left, to become A-1 and B-3. The outflow tract of the right ventricle
connects up with the Pulmonary Circulation and becomes the Pulmonary Artery,
and the outflow tract of the left ventricle connects up with the Systemic Circula
tion and becomes the Aorta. The Great Arteries develop normally, in agreement
with BARTHEL'S figures 26 and 157a (1960), and with GOERTTLER'S description
(1963): "Die Verschmelzung der einander gegeniiberliegenden Polster und Leisten
(A-1 mit B-3) bei 12 mm groBen Keimen sowie deren Vereinigung mit dem
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12 G. Conte et al.
Trunkusseptum fiihrt nach der schon lange bestehenden funktionellen zur mor
phologischen Itennung der Ausstromteile" (p. 67). [The merging of the cushions
and ridges situated diametrically opposite each other (A-1 con B-3) in embryos
12 mm in length, as well as the fusion of these with the truncus septum, mor
phologically divide the outflow tract that was already functionally divided.]
Case 2. The bloodstreams are straight. The right bloodstream remains right
anterior and flows into the 4th branchial arterial arches, the left bloodstream re
mains left-posterior and flows into the 6th branchial arterial arches; the septal
ridges develop rectilinearly to become A-3 and B-1. The outflow tract of the right
ventricle connects up with the Systemic Circulation, becoming the Aorta, and the
outflow tract of the left ventricle connects up with the Pulmonary Circulation,
becoming the Pulmonary Artery. The great arteries are in "Complete Transposi
tion", in agreement with GoERITLER'S figure 6 (1956), with BARI'HEL'S figures
157d and 169 (1960) and figures 1 and 2 in CONTE and GIANNESSI (1987).
Case 3. The bloodstreams twist from left to right. The right bloodstream flows
into the 6th branchial arterial arches and the left bloodstream flows into the 4th
branchial arterial arches; the septal ridges are moulded to become A-1 and B-3
but they are twisted from left to right. In this case, the outflow tract of the right
ventricle connects up with the Pulmonary Circulation and becomes the
Pulmonary Artery, the outflow tract of the left ventricle connects up with the
Systemic Circulation, becoming the Aorta. The Great Arteries are in "Corrected
Itansposition", in agreement with GOERTTLER'S figure 5 (1956) and with BAR
THEL'S figures 175 and 176 (1960).
Case 4. The right bloodstream flows into the 6th right branchial arterial arch,
while the left bloodstream flows into the 6th left branchial arterial arch and into
the 4th branchial arterial arches; the septal ridges are moulded to become A-1 and
B-2. The outflow tract of the left ventricle connects up with the Systemic Circula
tion and the left Pulmonary Circulation, while the outflow tract of the right ven
tricle connects up with the right Pulmonary Circulation alone. Therefore, the left
pulmonary artery branch starts in the ascending Aorta (lYPe I in GOOR and
LILLEHEI 1975), in agreement with MORGAN'S figure 4 (1972).
Case 5. The right bloodstream flows into the 4th branchial arterial arches and
into the 6th left branchial arterial arch, while the left bloodstream flows into the
6th right branchial arterial arch; the septal ridges are moulded to become A-2 and
B-1. The outflow tract of the right ventricle connects up with the Systemic Cir
culation, becoming the Aorta, and with the left Pulmonary Circulation. The
outflow tract of the left ventricle connects up with the right Pulmonary Circula
tion, becoming the right pulmonary artery branch. The Great Arteries are in
Transposition but the left pulmonary artery branch originates from the right Ven
tricular outflow tract.
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Hemodynamics and the Development of Certain Malformations 13
Case 6. The right bloodstream flows into the 6th left branchial arterial arch,
while the left bloodstream flows into the 6th right branchial arterial arch and into
the 4th branchial arterial arches; the septal ridges are moulded to become A-2 and
B-3. The outflow tract of the left ventricle connects up with the Systemic Circula
tion and the right Pulmonary Circulation; the outflow tract of the right ventricle
connects up with the left Pulmonary Circulation. The right pulmonary artery
branch originates in the ascending Aorta (Type I in GOOR and LrLLEHEI 1975).
These findings agree with figure 24.7 in EDWARDS et al. (1965), with figure 6 A
in Seidl and Steding (1981).
Case 7. The right bloodstream flows into the 4th branchial arterial arches and
into the 6th right branchial arterial arch, while the left bloodstream flows into the
6th left branchial arterial arch; the septal ridges are moulded to become A-3 and
B-2. The outflow tract of the right ventricle connects up with the Systemic Cir
culation, becoming the Aorta, and with the right Pulmonary Circulation; the
outflow tract of the left ventricle connects up with the left Pulmonary Circula
tion, becoming the left pulmonary artery branch. The Great Arteries are in
Transposition but the right pulmonary artery branch originates in the right ven
tricular outflow tract.
Case 8. The right bloodstream flows into the 6th branchial arterial arches and
into the 4th left branchial arterial arch, while the left bloodstream flows into the
4th right branchial arterial arch; the septal ridges are moulded to become A-1 and
B-4. The outflow tract of the right ventricle connects up with the Pulmonary Cir
culation and with the left Systemic Circulation. The outflow tract of the left ventri
cle connects up with the right Systemic Circulation and forms the innominate
artery. The left common carotid and the left subclavian arteries and, perhaps, the
aortic arch originate in the Pulmonary Artery. These findings agree with figure 5
in CELORIA and PATroN (1959) and with figure 3 (4055, 3613) in MOULAERT
(1976).
Case 9. The right bloodstream flows into the 4th right branchial arterial arch,
while the left bloodstream flows into the 4th left branchial arterial arch and into
the 6th branchial arterial arches; the septal ridges are moulded to become A-4 and
B-1. The outflow tract of the right ventricle connects up with the right Systemic
Circulation and becomes the innominate artery; the outflow tract of the left ven
tricle connects up with the left Systemic Circulation and the Pulmonary Circula
tion: both branches of the Pulmonary Artery originate in the Aorta.
Case 10. The right bloodstream flows into the 6th branchial arterial arches and
into the 4th right branchial arterial arch, while the left bloodstream flows into the
4th left branchial arterial arch; the septal ridges are moulded to become A-4 and
B-3. The outflow tract of the right ventricle connects up with the Pulmonary Cir
culation and the right Systemic Circulation; the outflow tract of the left ventricle
connects up with the left Systemic Circulation. The Great Arteries are in "Cor-
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