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Study of the development of the atrioventricular conduction system as a consequence of observing an extra atrioventricular node in the normal heart of a human fetus.

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THE ANATOMICAL RECORD 230:73-85 (1991)
Study of the Development of the Atrioventricular
Conduction System as a Consequence of
Observing an Extra Atrioventricular Node in the
Normal Heart of a Human Fetus
J.M. DOMfiNECH-MATEU, A. ARN6-PALAU, AND A. MARTfNEZ-POZO
Faculty of Medicine, Department of Anatomy, Autonomous University of Barcelona, 08193
Bellaterra, Spain
ABSTRACT
We have observed a n extra atrioventricular node in the normal
heart of a human fetus. It is located in the septa1 wall of the right atrium, subendocardially, and just where Todaro’s tendon leaves this wall to go toward the
inferior vena cava valve. In its trajectory, this tendon gives way to a remarkable
prominence in the cavity of the right atrium: the sinus band. In order to explain
the embryogenesis of this extra atrioventricular node, we have studied the normal
development of the atrioventricular specific system and have concluded that the
atrioventricular node is formed from a growth and displacement toward the atrium
of the primitive atrioventricular specific material, which originates from the myocardium of the posterior wall of the atrioventricular canal. Likewise, during its
development, the atrioventricular node keeps in close proximity with the Todaro’s
tendon. In our view, this accounts for the embryogenesis of the extra atrioventricular node, since a fragment of the atrioventricular node can remain cranial to
Todaro’s tendon and be displaced by i t in a craniodorsal direction. This fragment
would then lead to the formation of a n extra atrioventricular node like the one
present in the heart of the fetus we have examined.
Many reports have described the macroscopic and
microscopic anatomy of the conducting atrioventricular tissue, but there is still controversy regarding its
embryologic origin. The present study of a n extra atrioventricular node in a human fetus with a normal heart
has allowed us to describe its structure and its morphogenesis and, as a consequence, to reconsider the development of the specific atrioventricular tissue.
The existence of aberrant elements of the specific
atrioventricular tissue in the human heart (Kistin,
1949; Truex et al., 1958) and animal heart (Shaner,
1929; Nie, 1983) has been reported mostly associated to
severe alterations of the atrioventricular canal (Truex
and Bishof, 1958; Anderson e t al., 1974; Baissus et al.,
1975). Abnormal specific atrioventricular structures
have also been described in the hearts of young adults
who have suffered sudden death (Walgreen and Winblad, 1937; James, 1968; James and Marshall, 1976;
James, 1985; Marino and Kane, 1985;Bharati and Lev,
1986). Nevertheless, we believe that given its localization, its structure and its own arterial supply, the extra
atrioventricular node herein described cannot be homologated to the abnormal structures above mentioned.
The aim of this work is twofold: the description of the
extra atrioventricular node and the analysis of its morphogenesis. This detailed study of the development of
the specific atrioventricular tissue has enabled us to
establish a new hypothesis on the genesis of the extra
atrioventricular node. Therefore, it is our contention
0 1991 WILEY-LISS, INC
that Todaro’s tendon in its course toward the inferior
vena cava valve, isolates a nodal fragment in craniodorsal direction which will then lead to the formation
of a n extra atrioventricular node.
MATERIAL AND METHODS
Fifty embryos and human fetuses from the Bellaterra collection (Domenech-Mateu) have been used in
the present study. Age, section, and staining characteristics are shown in Table 1. A tridimensional reconstruction from the atrial and atrioventricular areas of
the heart of the LP fetus is carried out using the
method of Born (1883), at X70 final magnification.
RESULTS
Description of the LP Fetus Heart
The heart of this specimen is normal: situs solitus,
atrioventricular concordance, and well-ordered morphology of the pulmonary infundibulum, as well as of
the aortic vestibule. The atrioventricular orifices, a s
well a s their valves, are normal; the septum primum
(Fig. 1)and septum secundum show good development;
the foramen secundum is present, and the foramen
ovale begins to form.
Received March 19, 1990; accepted October 15, 1990.
74
J.M. DOMENECH-MATEU E T AL
TABLE 1. Features of the specimens used
CR length
(mm)
Embryos
PLA
MAR
MARS
RI.l
ss.l
PU.5
BI.4
PLA.14
HB
DU
DF. 1
DU.20
PO
DU.10
DU.5
FU.22
BI.7
GI.7
GI.l
DU.9
RE.l
FU.20
FU.10
BI.5
DU.8
GC
RI.2
ss.2
GI.10
PLA.3
FU.18
FU.ll
FU.12
GI.2
DF.4
DF.2
PLA.9
FU.6
SAM
Fetuses
D0.4
ED.l
FRA.4
PLA.5
PLA.7
AL.2
D0.5
DF.3
LP
C.155
JS.1
4
4
4
6
6
6
6.8
8
8
8.5
10
10
10
10
10.3
11.5
12
12
13
15
15
16
16.5
17
18
18
19
19
19
21
22
24
24
25
26
27
27.5
28
30
Carnegie
stage
Age
(days)
Plane of
section'
12
12
12
13
13
13
14
15
15
15
16
16
16
16
16
17
17
17
17
18
18
18
18
19
19
19
20
20
20
20
20
21
21
22
22
23
23
23
23
26
26
26
28
28
28
32
33
33
33
37
37
37
37
37
41
41
41
41
44
44
44
44
48
48
48
51
51
51
51
52
54
54
54
54
57
57
57
57
(weeks)
32
39
50
54
60
64
68
70
130
155
160
8?h
9
9
10Yz
10%
11
11
11
16
17%
18
Thickness
of section
(w)
Staining
technique'
T
T
T
T
T
T
T
T
T
T
F
T
T
T
T
F
T
T
T
T
T
T
F
T
T
T
T
T
F
T
T
T
F
T
T
T
T
T
T
20
10
10
10
10
10
10
10
10
8
10
10
7
10
8
10
10
10
10
10
10
10
10
10
10
10
10
10
10
10
10
10
10
10
10
10
10
10
10
H-E
H-E
H-E
H-E
H-E
H-E
H-E
H-E
H-E
H-E
H-E
H-E
H-E
H-E
H-E
H-E
H-E
H-E
H-E
H-E
H-E
H-E
H-E
H-E
B
H-E
H-E
H-E
H-E
H-E
H-E
H-E
H-E
H-E/MTR
H-E
B
B
H-E
B
T
T
T
F-0
F-0
T
F
F-0
T
T
T
10
10
10
10
10
10
10
10
10
15
15
H-E (azan)
B
H-E
H-E/MTR
H-E/MTR
B
H-E (azan)
H-E/MTR
H-E/MTR/G
H-E/MTWG
H-E/MTR/G
'Abbreviations: T transversal
F frontal
F-0 frontalioblique
H-E hematoxylin-eosin
MTR Masson's trichrome
B Bielschowsky
G Goldner
In the left atrium, the outlet of five pulmonary veins
can be appreciated: three from the right and two from
the left. The coronary sinus has a great diameter and it
is lateral to the left atrium. It follows the left atrium
along its left and inferior portions. In the last part of its
course, i t keeps a close relationship with the posterior
EXTRA ATRIOVENTRICULAR NODE: EMBRYOGENESIS
75
aspect of the left atrium, beneath the right and the left
inferior pulmonary veins, and next to the posterior aspect of the left atrioventricular orifice.
The right atrium, of great volume, shows in its inferior part the orifice of the inferior vena cava, and ventral and medial to it we find the ostium of the coronary
sinus. In both orifices we observe their corresponding
valves: Eustachian valve and Thebesian valve (Fig. 2).
The main point of interest of the right atrium is found
in its internal or septal wall. At that point, the sinus
band produces a great prominence which goes from the
membranous septum to the inferior vena cava valve,
looking like a crest protruding in the interior of the
atrial cavity (Fig. 1).In its distal portion, this crest
forms the cranial limit of the coronary sinus outlet.
Histologically, we can distinguish the extra atrioventricular node (Fig. 3a-c) in the junction of the interatrial septum with the sinus band, where we find
the tendon of Todaro (Fig. 3a). The extra atrioventricular node is rounded, with a maximum diameter of 450
pm, and it is formed almost totally by nodal fibres. In
its central position lies its artery (Fig. 3c), which has
its origin in the artery of the atrioventricular node
(Fig. 4). This nodal artery stems from the circumflex
branch of the left coronary artery at the posterior atrioventricular sulcus. It courses in a posteroanterior direction relating to the floor of the coronary sinus and it
is tightly applied to the mitral valve attachment in
order to reach the atrioventricular node (Fig. 4).
It is precisely within the node that it supplies the
artery for the extra node, which ascends by the interatrial septum and reaches the extra node by its inferior
aspect. From its entrance the artery is completely surrounded by nodal fibres (Fig. 3c).
The atrioventricular node has a subendocardial location in front of the coronary sinus orifice and above the
insertion of the tricuspid septal cusp, in the triangle of
Koch. Its histology and development is normal and its
arterial vascularization stems from the artery of the
atrioventricular node which, as already mentioned, is a
branch of the circumflex artery. Therefore, the arterial
supply of the atrioventricular node is tributary to the
left coronary artery system. The atrioventricular node
continues with the His bundle first, in the midst of the
central fibrous body and later in the base of the membranous septum.
The extra atrioventricular node does not continue
with any fascicular structure. However, we observe
muscular fibres from the interatrial septum reaching,
by its superior part, the extra atrioventricular node
(Fig. 3b). In order to explain the embryogenesis of the
extra atrioventricular node we have studied the normal development of the atrioventricular node in the
human embryonic and fetal periods.
identified as specific tissue. We have not seen such a
tissue either in the left horn of the sinus venosus or in
the posterior wall of the primitive or common atrium.
In embryos of 6-mm CR length, with well-defined atrioventricular cushions, we have not appreciated the primordium of the specific atrioventricular tissue either.
But we do recognize it in 10-mm CR length embryos, in
which the rudiments of the specific atrioventricular tissue are already detectable.
Stage 16 (from 8-1 1-mm CR length). Along this stage,
the specific atrioventricular tissue can be distinguished as a compact cellular mass under the inferior
endocardial cushion (Fig. 5a) and in relationship to the
posterior part of the atrioventricular canal, from which
it has extended in a dorsoventral direction, following
the base of the inferior endocardial cushion. This cellular mass is in contact with the subendocardial layer
of the ventriculus through a cellular tract (Fig. 5b).
Stage 18 (13-17-mm CR length). During this stage,
the conducting atrioventricular tissue is found in the
atrioventricular junction. Its dorsal part, appearing as
a plexus, corresponds to the atrioventricular node. Its
location is subendocardial in the area of the septal wall
of the atrium, between the base of the sinus venosus
right valve, and the primordium of the tricuspid septal
cusp (Fig. 6a). Ventrally, however, the tissue is more
compact, and corresponds to the His' bundle; it is located caudally to the sinus venosus right valve but at a
greater distance of it, between the tricuspid and mitral
valves primordia (Fig. 6b). Finally, we observe it underneath the inferior endocardial cushion, in its concavity between its right and left tubercles. The tissue,
in all its extension, is surrounded by mesenchyma,
which allows us to differentiate it clearly from the
neighboring myocardial tissue (Fig. 6a,b).
Stage 20 (18-22-mm CR length). We find the atrioventricular node, during this stage, in a subendocardial
position in the septal wall of the right atrium, just in
the area between the septum secundum and the tricus-
Embryonic Period
Human embryos: stages 12-15 (4-8-mm CR length)
M
MS
NA
PB
RA
RV
RVV
SB
SP
T
The youngest embryo of our collection included in
the present work is the PLA, of 4-mm CR length. The
heart shows the truncus, the bulbus cordis, the ventriculus primitivus, the atrium primitivum, and the sinus
venosus to be well differentiated. In regard to its structure, we have failed to observe in the Gosterior wall of
the atrioventricular canal any cell group that, by its
cytological and locational characteristics, could be
ABBREVIATIONS
A
A0V
AV
BB
C
CF
cs
EAN
EV
HB
IC
IVC
LA
LH
LV
Tr
TV
v
aorta
aortic vestibule
atrioventricular node
branching bundle
conus
central fibrous body
coronary sinus
extra atrioventricular node
Eustachian valve
His bundle
inferior endocardial cushion
inferior vena cava
left atrium
left horn of sinus venosus
left ventricle
mitral (anterior cusp)
membranous septum
nodal artery (extra atrioventricular node)
penetrating bundle
right atrium
right ventricle
right venous valve
sinus band
septum primum
tricuspid (septal cusp)
tendon of Todaro
Thebesian valve
ventriculus
Figs. 1,2
EXTRA ATRIOVENTRICULAR NODE: EMBRYOGENESIS
77
Fig. 3. Transverse section of the LP fetus (130-mm CR length). a:
The extra atrioventricular node (arrow) is situated subendocardially
at the intersection of the interatrial septum and the sinus band. (H-E
stain.) x 25. b: Part of the previous section showing the structure and
position of the extra atrioventricular node. (H-E stain.) x 250. c: Enlargement of the extra atrioventricular node. Note the presence of the
nodal artery. (H-E stain.) x 630.
pid primordium. The basal zone of the right venous
valve coincides, approximately, with the central part of
the cranial aspect of the nodal tissue. Ventrally and
caudally, i t becomes more compact and i t has a truncal
appearance a s it forms the primordium of the His’ bundle which, in its lowest part, is close to the crest of the
septum inferius. We also readily discern the left bundle
branch directing itself, subendocardially, to the septal
wall of the left ventricle.
Stage 21 (22-24-mm CR length). Along this stage, the
atrioventricular node shows in its superior aspect a
series of prominences that confer it a toothed aspect
(Fig. 7a). They are a n indication of the progression of
the nodal tissue towards the subendocardium of the
septal wall of the right atrium. The loose texture of this
area permits its “diffuse” growth; at the same time, it
Fig. 1. Internal view of the reconstruction of the heart of the LP
fetus (130-mm CR length). x 70. Observe that the sinus band is the
fold running from the anterior part of the inferior vena cava valve to
the membranous septum in the right atrium. The tendon of Todaro is
the major element in this band.
Fig. 2. A more dorsal plane of the same reconstruction. Here the
opening of the inferior vena cava, as well as the coronary sinus with
its corresponding valves, is clearly seen.
78
J.M. DOMENECH-MATEU ET AL.
Fig. 4. Drawing of the LP fetus heart viewed from above and lateral to the left atrium. The trajectory
of the circumflex artery and the origin of the nodal artery can be observed. 1, circumflex artery; 2,
atrioventricular nodal artery; 3, branch for the extra A-V node.
accounts for the netted morphology observed in the definitive atrioventricular node structure: a network
formed as the nodal fibres interweave with a collagen
framework. In addition, we appreciate the primordium
of the tendon of Todaro from its origin in the membranous septum next to the aortic vestibule, as a cellular
tract going toward the attachment of the right valve of
the sinus venosus, keeping a close relationship with the
superior and medial aspect of the atrioventricular node
(Fig. 7b). We find this configuration, clearly seen in
Figure 7b, essential in order to support our hypothesis
of the embryogenesis of the extra atrioventricular node
presented in the discussion of this paper.
Stage 22 (23-28-mmCR length). During this stage,
the tricuspid septal cusp shows a remarkable develop-
ment. The primordia of the coronary sinus valve and of
the inferior vena cava originate from the inferior portion of the right valve of the sinus venosus. The base of
the venous right valve in its continuation with the endocardium that covers the septal wall of the atrium
marks the atrioventricular node area, which lies,
subendocardially, cranial with respect to the attachment of the tricuspid septal cusp and at the base of the
septum secundum. At this stage, the specific atrioventricular tissue corresponding to the node shows a more
diffuse shape in comparison with the His’ bundle truncal structure.
Stage 23 (27-31-mmCR length). The morphology of
the specific tissue during this stage is represented by
the atrioventricular node, which keeps its loose dispo-
EXTRA ATRIOVENTRICULAR NODE: EMBRYOGENESIS
79
Fig. 5. Frontal sections of the DF.l embryo (10-mm CR length). a: The primordium of the specific
atrioventricular tissue (arrows) is situated under the inferior endocardia1 cushion. W E stain.) x 40. b
Detail of the previous figure. Note a cellular tract running from the cellular mass of the specific atrioventricular tissue to the subendocardial layer of the ventriculus. (H-E stain.) x 250.
sition, a s observed in the advanced embryonic period,
while maintaining identical position (Fig. 8a). It is located subendocardially between the superior limit of
the tricuspid septa1 cusp primordium and the base of
the septum secundum. Between them we can distinguish the attachment of the sinus venosus right valve.
Likewise, we detect a cellular growth-the tendon of
Todaro primordium-which, originating in the mem-
branous septum near the aortic vestibule, goes toward
the base of the right valve of the sinus venosus and
keeps a close relationship with the atrioventricular
node cellularity (Fig. 8a).
Ventrally and caudally, the node continues itself
with the His bundle, which is positioned in the center
of what will be the central fibrous body (Fig. 8b) and,
immediately thereafter, finds its way between the base
80
J.M. DOMENECH-MATEU ET AL.
Fig. 6. Transverse sections of the FU.20 embryo (16-mm CR length). a: Note how atrioventricular
tissue appears as a plexus. W E stain). x 63. b The more compact tissue corresponds to the His’ bundle.
W E stain.) x 63.
EXTRA ATRIOVENTRICULAR NODE: EMBRYOGENESIS
81
Fig. 7. a: Transverse section of the FU.ll embryo (24-mm CR length). Observe the toothed aspect of the
cranial part of the atrioventricular node. (H-E stain.) x 63. b: Frontal section of FU.12 embryo (24-mm
CR length). Observe the primordium of Todaro’s tendon, keeping a close relationship with the superior
and medial aspect of the atrioventricular node. (H-E stain.) x 160.
of the membranous septum and the cranial margin of
the septum inferius. We can also keenly observe its
right and left branches.
Fetal Period
DO 4 Fetus (32-mm CR length, 84 weeks).
The development of the valvular structures of the
tricuspid and mitral orifices, along with a better differentiation of the future atrioventricular fibrous annulus, has helped us establish with great precision the
morphology of the conducting atrioventricular tissue.
Subendocardially, in the septa1 wall of the right atrium
and in close relationship with the base of the right
valve of the sinus venosus, we find the atrioventricular
node. The disposition of its cellularity gives i t a loose or
diffuse appearance. Anteriorly, i t continues with the
His bundle, which, in contrast with the node, offers a
compact disposition. Likewise, we can determine very
well its penetrating bundle and its branching or distal
bundle. The latter in its inferior aspect lays over the
cranial margin of the septum inferius. The morphology
of the node and of the His bundle resemble the image of
a barbell used in weight lifting
- (Fig.
- 9). The cranial or
superior part of the barbell corresponds to the atrio-
ventricular node; the caudal part, to the branching
bundle; and the intermediate part, to the penetrating
bundle.
Fetuses (39-60-mm CR length (9-10% weeks). These
fetuses exhibit a morphology nearly identical to that of
the adult heart. The mesenchymal tissue, which in the
embryonic period and a t the beginning of the fetal period constitutes the environment of the nodal primordium, becomes differentiated into connective tissue.
This, along with the incremented cellularity of the
node, produces its compact appearance. We also observe the nodal artery in a n eccentric position in relationship to the node (Fig. 10a). Cranial to the node, we
see Todaro’s tendon (Fig. 10a) coming from the membranous septum towards the right atrium, and reaching the Eustachian valve. The atrioventricular node
continues with the His bundle, which has a compact
appearance and divides itself into the well formed right
and left branches.
During progressive fetal periods (64-160-mm CR
length fetuses, 11-18 weeks) the most evident features
are, on the one hand, the greater distance bet-reen the
tendon of Todaro and the atrioventricular node (Fig.
10b,c) and, on the other, the configuration of the atrioventricular node in a morphologfand structure abso-
82
J.M. DOMENECH-MATEU ET AL.
Fig. 8. Transversal sections of the SAM embryo (30-mm CR length). a: Observe the loose disposition of
the well-developed atrioventricular node as well as the Todaro’s tendon (arrow). b More caudally, the
compact appearance of the His bundle is clearly shown. (Bielschowsky stain.) x 160.
lutely homologous to the atrioventricular node of the
definitive heart (Fig. 10d).
we believe, in agreement with DeHaan’s (1961) theory,
that they constitute a specific population different from
the one that will produce the working myocardial cells.
DISCUSSION
However, once the primordium of the specific atrioThere are two unanswered questions in regard to the ventricular tissue can be distinguished not only by its
embryogenesis of the specific atrioventricular tissue. cellularity but also by its topography, its development
The first relates to the origin of the specific cellularity can easily be followed. Our results show that the close
of the nodal tissue and, the second, to the formation of relationship with the posteroinferior endocardial cushthe atrioventricular node, which has been explained as ion, observed in this initial phase, is essential for its
originating (1)from unique material, either from the appropriate development, since to a large extent the
posterior wall of the atrioventricular canal (Keith and structures originated from the cushion will be directly
Mackenzie, 1910; Mall, 1912; Tandler, 1913; Shaner, related with the atrioventricular node in its final posi1929; Sanabria, 1936; Calcagno, 1941; Walls, 1947; tion. Thus the close relationship between the cushion
Duckworth, 1952; Muir, 1954; Navaratnam, 1965 and and the specific atrioventricular tissue leads, in stage
Viragh and Challice, 1982) or from the sinus-muscular
18, to the positioning of the His bundle between the
layer of the left horn of the sinus venosus (Retzer, 1908; primitive tricuspid valve-primordium of the septa1
Patten, 1956; James, 1970); or (2) having a double or- c u s p a n d the primitive mitral valve-primordium of
igin, either atrioventricular and sinusal (Anderson and the anterior cusp. Consequently, the His bundle apTaylor, 1972) or atrioventricular and atrial (Truex et pears to be located in the future central fibrous body
al., 1978). The morphological development of the spe- and has a n apparent growth in cranial direction. We
cific atrioventricular tissue begins in human embryos believe that it is this cranial-atrial-portion of the maof 10-mm CR length (stage 16; 37 days) as a compact terial of the specific tissue, which will entirely produce
cellular group, easily identified, under the posteroinfe- the atrioventricular node. The development of this marior endocardial cushion.
terial takes place in a n area relatively loose (base of
The origin of its cellularity is still being debated, the implantation of the sinus venosus right valve)
although it would appear that it stems from the myo- which permits a “diffuse” growth very different from
cardium of the posterior wall of the atrioventricular that of the His bundle. The latter is always surrounded
canal located subendocardially. Even though it is true by “solidly” configured structures that force it, methat in the initial periods, premorphogenic, of the spe- chanically, to keep a truncal morphology. However, a s
cific atrioventricular tissue (stages 13-15), it is impos- the elements that will form the triangle of Koch besible to detect cells with the ability to form this tissue, come differentiated, the node progressively loses its dif-
EXTRA ATRIOVENTRICULAR NODE: EMBRYOGENESIS
83
Fig. 9. Transverse section of D0.4 fetus (32-mm CR length). Note the barbell shape of the atrioventricular conduction system. The cranial part corresponds to the atrioventricular node, the intermediate
part, to the penetrating bundle, and the caudal part is the branching bundle (of His). (H-E stain.) x 63.
fuse aspect and acquires its definitive morphology: a
dense appearance preceded by a configuration that
mimics a barbell with a cranial portion a s the atrioventricular node, and a caudal one, as the branching
bundle (of His).
In this particular point, we disagree with Anderson
and Taylor (1972) and Truex et al. (1978), who claim
that there exists a double origin of the atrioventricular
node: one from the atrioventricular canal musculature
and another from the atrium (in the human embryo,
Truex et al., 1978, and in the ferret embryo, Marino e t
al., 1979) or sinusal (Anderson and Taylor, 1972). In
our observation, we have not been able to detect any
structure that having the origin in the atrial segment
(posterior wall of the primitive atrium or of the muscular layer of the left horn of the sinus venosus) joins
the specific tissue of atrioventricular origin. To the contrary, the atrioventricular node is, simply, a result of
the growth and migration in cranial direction (atrial)
of the primitive specific atrioventricular material.
Moreover, we have shown that at the end of the embryonic period, stage 23 (57 days), the development of
the atrioventricular node is already completed. This is
a t variance with what has been indicated by some authors (James, 1970; Anderson and Taylor, 1972), who
state that its configuration, similar to the adult, is established during the fetal period (human fetus of 46
mm C.R. length, 9 1/2 weeks) (Anderson and Taylor,
1972) and by others who postulate a sinusal origin
(Retzer, 1908; Patten, 1956; James, 1970) and who consider that the atrioventricular node joins the His bundle, precisely, a t the beginning of the fetal period
(James, 1970).
Furthermore, the structure of the atrioventricular
node at its origin and already during its development,
has less nodal fibres than the sinoatrial node a s previously pointed out by one of us (Domenech-Mateu and
Boya-Vegue, 1975; Domenech-Mateu and Orts-Llorca,
1976) in a study on the development of the sinoatrial
node in the heart of the rat embryo.
With regard to the anatomic differentiation of the
node, we believe that its proximity to the primordium
of the tendon of Todaro is a relevant observation. This
structure, of minor significance in the anatomy of the
adult heart, plays a n essential role in the morphogenesis of the specific atrioventricular tissue, since, in its
origin, it keeps a relation of close vicinity with the
cranial aspect of the atrioventricular node. It is our
contention that this circumstance explains the embryogenesis of the extra atrioventricular node present in
the LP fetus heart described in this paper. A fragment
of the atrioventricular node would remain cranial to
Todaro’s tendon in its initial course, either because i t
introduces itself in the thickness of the atrioventricular node, or because a part of the cell population of the
nodal primordium remains cranial to Todaro’s tendon,
given the very diffuse initial morphology of the atrioventricular node. In any of these circumstances, the
84
J.M. D O M E N E C H - M A T E U ET AL.
Fig. 10
EXTRA ATRIOVENTRICULAR NODE: EMBRYOGENESIS
Fig. 10. a: Frontal-oblique section of the PLA.5 fetus (54-mm CR
length). Observe the compact aspect of the atrioventricular node, with
the nodal artery in an eccentric position. Above the node, note the
tendon of Todaro. (Pollack‘s trichrome stain.) x 40. b-c:Transversal
sections of the C.155 fetus (155-mm CR length). b Observe the origin
of Todaro’s tendon. (Goldner stain.) x 40. c: Appreciate the atrioventricular node and His bundle. Note the greater distance between the
atrioventricular node and Todaro’s tendon. (Goldner stain.) x 40. d
Transversal section of the JS.l (160-mm CR length). Observe the
atrioventricular node and His bundle, homologous with those of the
definitive heart. (Goldner stain.) x 63.
tendon would displace the nodal fragment in cranial
and dorsal direction. This fragment would then become
the extra node, located, exactly, at the crux of the sinus
band (from where it goes toward the valve of the inferior vena cava) with the interatrial septum. Therefore,
we understand that the optimal disposition of Todaro’s
tendon to fragment the atrioventricular node, thereby
forming extra nodes, corresponds to the embryonic period. This, however, would be a remote possibility in
the fetal period because of the greater distance between
the node and Todaro’s tendon.
The extra node that we present herein has several
remarkable features: (1)its arterial irrigation: it comes
from the same branch of the circumflex trunk, which
irrigates the atrioventricular node, further suggesting
and identical origin for both structures; and (2) its location in the interatrial septum and far from the atrioventricular fibrous annulus. This is in contrast to the
fragments of aberrant atrioventricu1a.r tissue described
by others as located in the vicinity of the atrioventricular fibrous annulus or within the central fibrous body
(Truex et al., 1958; James and Marshall, 1976). These
fragments could possibly form accessory atrioventricular connections but never an extra atrioventricular
node. In the case we report, however, the extra node
can be classified as a true nodal structure, not only by
its configuration-abundant
cellularity of nodal fibres-but also by its location and irrigation.
James (1968) suggested that the aberrant specific
atrioventricular structures observed in term fetuses
and in young individuals affected by a sudden death
would progressively disappear due to resorptive degeneration (James and Marshall, 1976). This is not the
case for our specimen. We consider that since the artery of the extra node is very voluminous in relation to
the structure irrigated, it is likely that the extra atrioventricular node, instead of involuting, might become a
structure of great morphological entity with important
implications in the electrophysiological sphere.
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