Rom J Leg Med 17 (2) 101 - 110 (2009)
© 2009 Romanian Society of Legal Medicine
Morphofunctional considerations on the atrioventricular node
arterial vascularization
Mugurel C. Rusu*1, Dumitru Ferechide2, George Cristian Curcă3, Dan Dermengiu3
Received: 2.02.2009/ Accepted: 3.05.2009
_____________________________________________________________________
Abstract: The atrioventricular node (AVN) is the relay station for electrical impulses passing from the atria
to the ventricles. The arterial resources of the AVN are functionally relevant and may be interfered by various
surgical procedures which deal with the cardiac valves. Our study aim to bring detailed evidences on the arterial
supply of the AVN. We dissected and microdissected 50 human adult hearts without any known history or evident
cardiac pathology, in order to evidence the arterial suppliers of the AVN; subepicardial dissections were continued in
the interatrial septum (the triangle of Koch). We were able to define 5 morphological types (each with distinctive
subtypes) of the atrioventricular node artery (AVNA) emerged at crux cordis: type I (22%, AVNA from the U-turn of
the right coronary artery (RCA), the left retroventricular artery (RVA) absent), type II (18%, AVNA from PIVA, left
RVA present), type III (34%, AVNA from the left RVA, PIVA from the RCA), type IV (AVNA from the bifurcation
of the RCA into the PIVA and the left RVA – trifurcated RCA) and type V (AVNA from the circumflex artery). In
18% of specimens we found duplicated AVNA. In 22% of specimens, the AVN area was additionally supplied by the
descending septal artery (right descending superior artery) originating from the sinoatrial artery, on the right side of
the aorta. The origin of the AVNA, which is variable, and the accessory resources, such as the descending septal
artery, can explain the possible individual occurrences of the cardiac rhythm alterations determined by coronary
ischemia. Our AVNA types are all related to the atrioventricular and aortic valves and thus liable to damage during
specific surgical procedures, interfering with the respective valves. Duplicated AVNAs must be kept in mind during
the selective atrioventricular nodal artery catheterizations and AVNA must be evaluated angiographically prior to the
interventions. Our study demonstrates that classical dissections combined with microdissections can still offer
valuable informations for a pathologist assigning not only the mechanisms but also the morphological conditions of
the cardiac arrest. A seek and search investigation is launched in every sudden cardiac death: the forensic pathologist
make a good team with the anatomist retrieving very useful etiological data.
Key words: coronary artery; conduction system; right atrium
S
udden cardiac death is an important issue not only clinically but also from the
forensic perspective mainly because most jurisdictions demand for a full detailed
autopsy. Revealing the cardiac etiology is even more complicate. Initiating factors may
superimpose premorbid conditions such as cardiac anomalies, blood reduction flow
conditions, etc., triggering cardiac arrest. In reaching conclusions a forensic pathologist must
________________________
*) Corresponding author; University of Medicine and Pharmacy “Carol Davila” 8, Bd. Eroilor
Sanitari, RO-76241, Bucharest, Romania, Phone: +40722363705 E-mail: anatomon@gmail.com
1) Discipline of Anatomy and Embryology, Faculty of Dental Medicine, University of Medicine and
Pharmacy Carol Davila, Bucharest, Romania; 2) Chair of Physiology, Faculty of Medicine,
University of Medicine and Pharmacy Carol Davila, Bucharest, Romania; 3) National Institute of
Legal Medicine “Mina Minovici”, Sos. Vitan Birzesti 9, Sector 4, 042122 – Bucharest, E-mail:
cgcurca@yahoo.com
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Morphofunctional considerations on the atrioventricular node arterial vascularization
correlate and discriminate between terminal events and pathological findings [6]. A sudden
cardiac arrest must have an acute etiopathogenetic mechanism and the forensic pathologist should
seek acute morphological changes [7]. Therefore our study was conducted to demonstrate that
classical dissections combined with microdissections can still offer valuable informations for a
pathologist assigning not only the mechanisms but also the morphological conditions of the
cardiac arrest.
The atrioventricular node (AVN) acts as an electrical relay station for electrical impulses,
passing from the atria to the ventricles [11].
The origin of blood supply to the conduction system is highly relevant to clinical and
surgical procedures [2]. In severe conduction disturbances, patients tend to have specific coronary
lesion distribution, involving either the anterior interventricular artery (AIVA) branches or a
combination of this with significant right coronary artery (RCA) disease, compromising supply to
sinoatrial or AV nodes [26]. The location of narrowings in the AIVA and RCA as the arteries
supplying the conduction system was classified according to Mosseri et al. in 4 types: in type II
pathological coronary anatomy involves the septal branches of the AIVA, in type III it
compromises the blood supply to the sinoatrial or the atrioventricular node but not that one of the
AIVA septal branches while type IV represents a combination of types II and III [13, 26]. As a
major risk factor, the atherosclerotic or thrombotic obstruction of the sinoatrial node artery may
induce severe heart rhythm disturbances or even sudden cardiac death [15]. Identification of the
anatomical variants of the arterial blood supply to the SA and AV nodes may help in overcoming
potential difficulties when treating arrhythmias and in mitral valve surgery [16], while the
presence of coronary artery disease should be sought in every patient over 45 who presents with
severe conduction disturbance [26].
Removal of the heart and careful examination of the major extramural arteries and veins
is mandatory in every thorough autopsy conducted in sudden cardiac death. Intramural coronary
arteries, such as sinus node and atrioventricular node atrial branches should be, as possible,
search and examined: beneficial information may be gathered despite time consuming
appearence. Examination of the conduction system may be further on necessary when the
etiology still remains uncertain or a specific pathology is established (WPW sd., etc.). The best
undertaken action is therefore to remove three tissue blocks containing the SA node, the AV node
and the AV bundles, respectively [19].
The atrioventricular node artery
The AVNA arises at crux cordis [16] and continues towards the triangle of Koch, close to
the orifice of the coronary sinus, the endocardial surface of the right atrium, the middle cardiac
vein, and the specialized conduction tissues in most hearts [17]. The AVNA and/or the AV
conduction tissues arteries can be at risk of damage when ablative procedures are carried out at
the base of the triangle of Koch. Suppliers of the AVN may be the RCA, the CxA or both [18].
Kügel’s artery and the DSA (RDSA) were discovered to supply 40% of AVN and 70% of the
hearts [2].
Angelini pointed out that only two coronary atrial arteries are generally recognized with
the specific expression of “atrial branch”: SNA and AVNA. Of the two, multiple branches, only
one is frequently (but inconsistently) recognized in literature with a specific name, but no real
definition: the Kügel’s artery. The same author emphasized that the generally understood
attribute of any so-called Kugel’s artery is that it connects an anterior coronary artery located
around the aortic root (the LCA, the CxA or the RCA) to a posterior arterial branch (the RCA or
the CxA) in the coronary groove [4].
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The descending septal artery (right descending superior artery)
The blood supply to the upper ventricular septum in the region of the conduction system
is more abundant than literature suggests. A significant arterial contribution to the upper
ventricular septum from the proximal segment of the RCA, or one of its early branches, was
found in 77% of the hearts studied by Taylor, who named these contributors as „descending
septal arteries (DSA)”. In 68% of the hearts, the DSAs supplied the region of the proximal
conduction system [22]. The DSA was later called „Right Descending Superior Artery (RDSA)”
by Abuin [1, 2], who evaluated its distribution as being at the level of the bundle of His and the
area within the triangle of Koch, including the AVN [2].
Kügel's artery, DSA (RDSA) and SNA, were discovered as being affected by the surgical
procedures performed [1].
Our study aimed to bring detailed evidence regarding the arterial suppliers of the
atrioventricular node in humans and to evaluate the atrioventricular node artery morphological
patterns. We also took into account the considerations of Abuin and Nieponice, who claimed that
classical dissection techniques proved useless in the efforts of following the atrial vessels to the
nodal target, which deterred many anatomists from the attempt [2], and intended to demonstrate
that classical disssections combined with microdissections can still offer valuable informations.
Materials and methods
We performed the present study by dissecting 50 human adult hearts, in compliance with
the acting ethical rules of our institution. Complete subepicardial dissections of the coronary
arteries were performed. In those specimens, with the sinoatrial artery emerged from the right
coronary artery, the presence of the descending septal artery was observed and, if present, that
artery was dissected/microdissected in the posterior wall of the right atrium. The arteries at the
level of the crux cordis, on the diaphragmatic surface of the heart, were also identified, and the
atrioventricular node arteries were dissected within the triangle of Koch, after
removing/reflecting the anterior wall of the right atrium. The topography at the level of the
triangle of Koch was evaluated in accordance to the description of Yanagawa and Nakajima
(2009), who described its base as being formed by the opening of the coronary sinus, the apex
resinding at the AV septum (right atrial region of the membranous septum), the two sides
bordered by the septal leaflet of the tricuspid valve and the tendon of Todaro; according to these
authors, AVN is connected to AVB under the fibrous ring [25].
We defined as dominant coronary arteries those arteries sending the posterior
interventricular artery, PIVA. The coronary arteries also sending the opposite retroventricular
artery and not only the PIVA, we defined as hyperdominant coronary arteries.
Results
The dissections of AVNA at the level of the crux cordis leaded us to define 5 different
morphological patterns (AVNA types I - V), as follows:
- type I, with AVNA emerged from the U-shaped turn of the RCA-to-PIVA arteries, in
hearts with right coronary dominance (PIVA continuing the RCA); we found this
pattern in 11 specimens (22%) with 2 subtypes: Ia – single AVNA (9 specimens, 18%)
and Ib – duplicated AVNA (2 specimens, 4%):
o in a specimen type Ia the ANAV left the U-turn of the RCA in a common trunk
with the first two PSA (fig. 1);
o in a specimen type Ib from the U-turn of the RCA was leaving, distally to the
duplicated AVNA, a right postero-lateral branch (fig. 2), for the left ventricle;
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-
-
-
-
Morphofunctional considerations on the atrioventricular node arterial vascularization
type II, with AVNA emerged from the origin of PIVA, in hearts with right coronary
hyperdominance (PIVA and left RVA given at crux cordis by the RCA), was
encountered in 9 specimens (18%), also with two subtypes: IIa – unique AVNA (8
specimens, 16%)(fig. 3) and IIb – duplicated AVNA (1 specimen, 2%);
type III, with AVNA emerged from the origin of the left RVA at crux cordis, in hearts
with right coronary hyperdominance, in 17 specimens (34%); single AVNA (subtype
IIIa) was present in 12 cases (24%), while duplicate AVNA (subtype IIIb) was present
in 5 specimens (10%) (fig. 4); a single specimen type IIIb presented the distal AVNA
continued at the level of the membranous septum to supply the AVB (fig. 4);
type IV (trifurcation of the RCA) – AVNA leaving the V-shaped angle of the RCA
terminal bifurcation into the PIVA and the left RVA (4 specimens, 8%) as a unique
artery (1 heart) or in common trunk with the first (1 specimen, 2%), or with the first
two PSA (2 specimens, 4%) (fig. 5);
type V, with the AVNA emerging from the CxA, in 9 specimens (18%) with left
coronary dominance and hyperdominance, having the following subtypes:
o Va: single AVNA leaving the CxA in hearts with left coronary dominance (5
specimens, 10%);
o Vb: duplicated AVNA leaving the CxA in a single specimen (2%) with left
coronary dominance; the distal AVNA in that case left the U-turn of the CxA
in a common trunk which also supplied two PSA (fig. 6);
o Vc: single AVNA leaving the CxA in the presence of a right RVA (left
coronary hyperdominance), in 3 specimens (6%).
Fig. 1 Dissection of the arteries at the crux cordis.
1.RCA; 2.common posterior septal trunk; 3.PIVA;
4.ANAV; 5.first PSA; 6.second PSA; 7.right
ventricle.
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Fig. 2 Dissection of the posterior wall of the right atrium.
1. fossa ovalis; 2.medial cusp of the tricuspid valve;
3.opening of the coronary sinus; 4.duplicate atrioventricular
node artery, emerged at crux cordis from the U turn of the
RCA to PIVA (right coronary dominance); 5.sinoatrial
artery, emerged from the initial segment of the RCA and
sending off a descending septal artery (arrowheads) that
distribute in the area of the triangle of Koch; 6.RCA.
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Vol. XVII, nr. 2, 2009
Fig. 3 Dissection of the arteries at the level
of the posterior right atrial wall, by an
antero-lateral approach, for the anatomical
evaluation of the AVNA. 1.aorta; 2.right
SNA; 3.RCA; 4.anterior cusp of the TV,
detached and partially reflected; 5.septal
cusp of the TV; 6.PIVA; 7.limbus fossae
ovalis; 8.oval fossa; 9.small artery for the
limbus fossae ovalis; 10.right fibrous
trigone, at the tip of the triangle of Koch;
11.AVNA, emerged in a short common
trunk from the left RVA with a posterior
septal branch and a small right posterolateral
branch (for the left ventricular myocardium);
12.left RVA. The small arrows indicate an
artery emerged from the right fibrous trigone
and coursing on the right side of the
membranous septum, in the area
corresponding to the AVB.
Fig. 4 Dissection of the arteries of the cardiac septa, at the level of the right atrium and superior part of the right
ventricle. 1.aorta; 2.anterior parietal branch of the RA, emerged from the SNA; 3.anterior parietal branches of
the RA, emerged from the DSA(RDSA); 4.branch of the oval fossa limbus; 5.branch of the interatrial septum,
projected on the tendon of Todaro and coursing towards the valve of Eustachio; 6.left RVA; 7.primary common
trunk of the AVNA and PSA (further sending the main AVNA– asterisk and the first right PSA – small arrows;
the later sends from its loop accessory branches of the AVN – two asterisks); 8.left PSA; 9.RCA; 10.PIVA;
11.septal cusp of the TV; 12.anterior cusp of the TV; 13.SNA; 14.RCA; 15.right branch to conus arteriosus,
with common ostial origin with the RCA; 16.DSA (RDSA); 17.parietal branches of the right ventricle;
18.AIVA; 19.RSSA, emerged from the origin of the RCA.
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Morphofunctional considerations on the atrioventricular node arterial vascularization
The AVNA’s emerged at crux cordis
deepened to course endocardially, successively at
the level of the cavo-tricuspid isthmus, medially to
the sub-thebesian isthmus and next at the level of
the septal isthmus, to reach the base of the triangle
of Koch.
The duplicated AVNA’s we encountered
were either arising from a single common trunk or
had different close origins from the coronary
system, according to the types we defined above.
We defined these duplicated AVNA’s as proximal,
the one closer to the eustachian valve, and distal,
the one closer to the TV. Invariably, the distal one
sent off the first PSA at about the level of the
septal isthmus.
In 11 hearts (22%) we also found the
presence of the descending septal artery (right
descending superior artery) emerged from the
initial segment of the sinoatrial artery; all these
hearts were AVNA types I-IV (fig. 1, 3).
Fig. 5 Dissection of the arteries at crux cordis,
right coronary dominance. 1.RCA; 2.PIVA;
3.first two PSA; 4.AVNA; 5.left RVA; 6.right
ventricle; 7.left ventricle.
Fig. 6 Dissection of a duplicate atrioventricular node artery supplied by the CxA; left coronary dominance.
1.proximal AVNA, emerged from the CxA trunk; 2.CxA; 3.PIVA; 4.anterior cusp of the tricuspid valve;
5.inferior cusp of the tricuspid valve; 6.medial cusp of the tricuspid valve; 7.right ventricle; 8.common arterial
trunk emerged from the CxA-to-PIVA angle, further sending off a distal AVNA (12), the first posterior septal
branch (9) and a parietal branch (10); 11.RCA.
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These DSAs (RDSAs) initially coursed in the atrioventricular (coronary) groove on the
right side of aorta to enter the interatrial septum near its junction with the membranous
interventricular septum.
-
The distributed DSA (RDSA):
parietal branches of the right ventricle, in the vicinity of the anterior cusp of the TV;
branches of the interatrial septum, coursing laterally, at the level and above the limbus
fossa ovalis;
a descending branch that reached the apex of the triangle of Koch, distributing in the
AVN area.
Discussion
On the origin of the AVNA from the coronary system, we are in accordance with
Pejković et al (2008), who stated that the origin of the AV node artery is dependent on
coronary arterial dominance [16]; there are authors who found the AVNA leaving the left
coronary artery in 10% of their specimens [10, 16], while we found such origin of AVNA in
18% of those cases. In our specimens, we did not encounter a dual supply of AVNA, from codominant right and left coronary arteries, although such dual supply is described in literature
[12].
Our study demonstrated that the usual description on the origin of AVNA, from the Uturn into the base of the posterior interatrial septum made by the artery (either right or left
coronary) crossing the crux of the heart [21] is quite general; the AVNA may be considered
as arising from that arterial U-turn only in situations of coronary dominance (types I, Va and
Vb in our study), but not those of coronary hyperdominance (the other types we defined),
when a retroventricular artery (RVA) continues the sender, either RCA or CxA and may serve
as origin for AVNA.
Arid et al (2000) also evidenced similar to us, the possible origin AVNA from the
retroventricular artery and not only from the RCA or the CxA; however in their study were
not evidenced duplicated AVNA’s. Arid et al identified in 60,86% the AVNA arising from
the left RVA (it corresponds to our type IV that we encountered in 8%) and had singular cases
(4,34% each) of AVNA emerged from the CxA (corresponds to our type V identified in 18%)
and from the CxA division into the right RVA and the PIVA (we didn’t get at dissection such
morphology). Arid et al also found, in 33,33% of the specimens with “right coronary
dominance” (there was made no distinction with the hyperdominance), the AVNA leaving
“from the terminal part of the right coronary a., as well as the left retroventricular a. and the
posterior interventricular a. thus forming a sort of trifurcation” – in our study we defined as
trifurcated only the arteries (RCA’s, type IV) with adjacent origins of the PIVA, left RVA and
AVNA and if the AVNA emerged from the initial part of the RVA or the PIVA we
considered that artery as origin (types II and III) and didn’t take the RCA branching pattern as
trifurcation. Moreover, Arid et al didn’t found any specimen with the AVNA leaving the Uturn of the RCA, with left RVA absent [5].
Tanaka et al (1998) reported a case with a posterior SNA and an accessory AVNA
arising by a common origin from the CxA, on the diaphragmatic surface of the heart [21].
These authors considered the AVNA emerged at the crux cordis as “principal atrioventricular
node artery”, while defining the “accessory atrioventricular node artery” as corresponding to
Taylor’s DSA (1980) and to Abuin’s RDSA (1998) [1, 2, 22]. In our study, we preferred to
use the terms DSA (RDSA), which we considered more appropriated, due to the fact that the
respective artery is not uniquely distributed to the AVN so as to be called accessory AVNA.
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Tanaka et al evaluated their accessory AVNA (DSA or RDSA) as being quite similar
to the initial portion of Kügel’s anastomotic artery, but this evaluation must be discussed. The
“arteria anastomotica auricularis magna” was described by Kügel in 1928 and documented
in 100 hearts by Nerantzis et al (2004).
In 6% of cases, they evidenced several morphologic and topographic distinctive types
of Kügel’s artery (KA), connecting the proximal RCA or CxA, either directly or through the
SNA, with the distal arterial segment [14]. Nerantzis et al identified four different types of
origin and connections of the KA; in the second type, the KA was a right intracoronary
connection of the proximal and distal portions of the RCA, coursing in the interatrial septum
on the right of the coronary sinus orifice. So, it appears to us that only the second type of KA,
described by Nerantzis, can be considered in its initial part as similar to the DSA and the
initial general evaluation of Tanaka must be revised.
We consider that the only relevant difference between the KA leaving the RCA or the
SNA and the DSA (RDSA) is represented by their distal connection at the crux cordis: the
DSA (RDSA) is unconnected distally. No matter the anatomical diagnostic, any of these
arteries are, if present, suppliers of the AVN. Moreover, the RCA, CxA, SNA, KA, DSA
(RDSA) and AVNA may contribute, in various individual morphological pictures, to an
anastomotic network in the lower part of the interatrial septum, mainly in its right side [14],
which complicates the diagnostic of the dissections.
We found in 2% (fig.3, specimen type IIb) an AVB branch, continuing the AVNA.
With this evidence we improve the evidences of Van der Hauwaert et al (1972) who reported
that in none of the 10 hearts they studied did the AVNA reach the common bundle [23] and
correlate with Anderson and Murphy (1983) who reported that the AVNA supplied the AVB
in 64% [3], a percent consistently higher than ours. The respective authors also described that
in 7 from 10 hearts, AVNA invariably made a sharp caudal turn (50 to 90o), left the
conducting tissue, and ramified further in the adjacent myocardium – such caudal turns of the
AVNA we found only in 6 specimens (12%) of types Ia, IIIa and IIIb (the distal AVNA).
We found duplicated AVNA in 9 specimens (18%), of different types. It was hard for
us to document in the anatomical references such duplications. Saremi et al (2008) described
an “accessory atrioventricular nodal artery” arising from the distal RCA was reported in a
single case (0,98%). The “accessory” AVNA of Saremi is different to that one of Tanaka and
refers to a duplication of AVNA at the crux [18].
The noticeable difference of frequencies (18% vs. 0,98%) is probably due to the
hazard of specimens, on one hand, and to the different methods used (dissection vs. CT). Also
Brugada et al (1990), in a report on the chemical ablation of the atrioventricular tissue,
mention the presence, in 2 from 7 patients, of duplicated AVNA’s at the crux [8].
The hearts presenting not only the AVNA, but also the DSA (RDSA) and those hearts
with duplicated AVNAs, appear to us as provided with additional anatomical resources of
perfusion for the AVN, which will be better protected from ischemia. The difference is that an
occlusion of the distal RCA will spare the DSA (RDSA) emerged from the SNA, but may not
spare a duplicated AVNA (the occlusion of the proximal RCA may spare or not the DSA,
depending on the reciprocal relation of the occlusion site and the origin of the SNA). As we
did not find hearts, where the DSA (RDSA) associated with AVNA emerged from the CxA,
we cannot evaluate the former as an alternative supplier of the AVN in such specimens.
Our AVNA types are all related to the atrioventricular and aortic valves and are thus
liable to damage during specific surgical procedures interfering with the respective valves.
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Duplicated AVNA’s must be held in mind during the selective atrioventricular nodal
artery catheterizations [8, 20, 24], being able to determine failures of such procedures. The
AVNA, duplicated or not, must be evaluated angiographically prior to the interventions.
We must keep in mind that a complete investigation must be launched in every sudden
cardiac death, especially in young. In this perspective the forensic pathologist make a good
team with the anatomist, dissection and microdissection techniques still being very useful for
both SA and AV nodes examination. Actually a seek and search is launched and a complex
team will look for the cause of death and etiology: forensic pathologist, anatomist, radiologist,
histopathologist, toxicologist, geneticians [9].
Acknowledgements
Funding resource:
Grant, code 2642, of the National University Research Council (UEFISCSU), Romania.
Abbreviations:
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