© 2005 The European Society of Cardiology. Published by Elsevier Ltd. All rights reserved.
Anatomy of the inferior interatrial route in humans
aAlmazov Research Institute of Cardiology 15, Parkhomenko St., 194156 St. Petersburg, Russia; bPavlov State Medical University 6/8, Lev Tolstoy St., 197002 St. Petersburg, Russia; cDepartment of Cardiology, Lund University Hospital SE 221 85, Lund, Sweden
Manuscript submitted 13 January 2005. Revision received 28 July 2005. Accepted after revision 3 May 2005.
*Corresponding author. Tel.: +46 46 17 24 35; fax: +46 46 15 78 57. E-mail address: pyotr.platonov{at}kard.lu.se (P.G. Platonov).
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Abstract |
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AIMS: To explore the morphology of the proximal coronary sinus (CS) and the surrounding tissues in order to identify possible routes for interatrial conduction.
METHOD: Specimens containing interatrial septum and proximal CS were taken from 21 necropsied hearts and sliced into 10-µm thick parallel histological sections in 1-mm steps starting from the valve plane, up to the atrial roof (40–80 sections per heart). The sections were stained with van Gieson's stain.
RESULTS: Media in the proximal CS consists of smooth muscle cells that do not form a continuous layer. CS was not surrounded by striated atrial myocardium in 10 specimens in which posterior CS wall was covered by epicardial fat only. In seven specimens, striated muscle bundles of up to 2-mm width connected the myocardium surrounding the CS with the left atrium. Regardless of their presence, variable posterior and/or anterior interatrial muscular connections were identified in all specimens.
CONCLUSION: Variability of the striated atrial myocardium surrounding proximal CS may affect interatrial conduction. Striated muscular fascicles connecting the proximal CS with the left atrium are not obligatory cardiac structures and may be considered as supplementary to the larger interatrial connections outside the CS.
Key Words: atrial anatomy, interatrial conduction, atrial fibrillation, coronary sinus
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Introduction |
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Interest in the detailed anatomy of interatrial connections is driven by the growing appreciation of the role of interatrial conduction defects in development of atrial fibrillation [1,
2] and the recent breakthroughs in development of sophisticated and precise endocardial mapping technologies. Introduction of the electro-anatomical mapping and the non-contact mapping systems in clinical practice during the last five years has opened possibilities of identification and high-precision ablation of cardiac structures involved in the pathogenesis of arrhythmias.
The role of conduction delay in the postero-inferior interatrial connections has recently become appreciated [3,4]. The coronary sinus (CS) and the muscular layers that surround it are a part of the inferior interatrial conduction route in humans. Limited clinical studies in humans suggest that the inferior route could be more important for interatrial conduction during sinus rhythm than Bachmann's bundle [5] which has traditionally been considered as the major interatrial conduction route.
Available anatomical studies are limited in a number of heart specimens used for analyses of inferior interatrial connections and show great variability of their structure and location [6,7]. The aim of our study was to explore the morphology of the proximal coronary sinus and the surrounding tissues in order to identify possible routes that could be used for conduction of electrical activation between the right and the left atrium.
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Methods |
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Material from autopsies performed during the period 1998–2003 in St. Petersburg, Russia, was used for the study. The material included 17 specimens obtained during clinically motivated autopsies of patients who died in hospital from acute myocardial infarction and four specimens from subjects who died unexpectedly without any known diseases. In total, hearts from 21 subjects (mean age 65±13 years, 15 females) were studied. The local ethics committee approved the study. The study complies with the Declaration of Helsinki.
Excision of interatrial septum specimens and their serial sections were performed in accordance with the autopsy protocol and techniques described earlier [7]. The specimens included interatrial septum, adjacent portions of atrial walls and proximal portion of the CS with its mouth opening into the right atrium. Serial 10-µm thick sections of the interatrial septum were performed in 1-mm steps from the valve plane up to the atrial roof. They were stained with van Gieson's stain and examined using light microscopy.
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Coronary sinus wall
The coronary sinus wall consists of three distinct layers: intima, media and adventitia. In our material, the media of the proximal CS consisted of single or grouped smooth muscle cells that were arranged in 1–5 layers; they were surrounded by connective-tissue fibres but never formed a continuous uninterrupted layer. In one specimen, smooth muscle cells could not be identified in the media of the posterior wall of the proximal CS.
We observed valves in the lumen of the proximal CS in 12 of 21 specimens. The number of valves varied from 1 to 5. The size and shape of the valves varied from short rudimentary folds of the CS intima to large 5-mm long valves containing elastic and collagen fibre with inclusion of single smooth muscle cells.
Myocardial sleeves surrounding the proximal coronary sinus
Striated atrial myocardium extending from the right atrium covered the proximal portion of the coronary sinus in 20 of 21 specimens. The myocardium was arranged in two perpendicularly oriented layers. As a rule, the internal layer was longitudinal while the outer layer was circular. However, these findings were not homogeneous. Six specimens demonstrated mixed pattern where in certain segments of proximal CS it was either difficult visually to separate the internal and external layers or the circular muscle fibres dominated in the outer layer and vice versa.
In 10 specimens, the inferior CS wall was covered by epicardial fat only without any striated atrial myocardium inferior to the CS adventitia (Fig. 1). In one specimen, no striated myocardium could be identified in either superior or inferior wall of the CS and the proximal CS was completely surrounded by the epicardial fat in the cross-section of the interatrial septum.
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Muscular connections between the coronary sinus and the left atrium
We were able to visualize the fascicles of parallel muscular fibres up to 2-mm width without fibrous capsule that travelled through the epicardial fat from the CS wall to the left atrial myocardium (Fig. 2). The fascicles were extensions of the right atrial myocardial sleeves and matched the description provided by Chauvin et al. [8]
. These were seen in 6 of 21 of our specimens.
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Interatrial bundles outside the CS
Interatrial muscular bridges in the postero-inferior septal area were present in 15 of 21 specimens. Their exact location, number of bundles per specimen and width were highly variable (Table 1). The maximal width of bundles observed in our material was 21 mm. That was a muscular band bridging the inferior interatrial groove between the intercaval bundle on the right side and the interpulmonary bundle on the left.
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Epicardial fat surrounding the muscular bundles, as a rule, contained organized encapsulated neural fibres and ganglia in the vicinity of the bundles (Fig. 3). In six hearts, no distinct muscular bundle was seen outside the CS region.
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Discussion |
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The anatomy of the human atria is a field of medicine that has not been considered very dynamic since the beginning of the twentieth century when the major components of the atrial conduction system were described [9,
10]. Nevertheless, a series of recent publications provided a deeper insight into the structure and location of muscular bundles, which could conduct activation between the atria. In addition to the superior interatrial route represented by Bachmann's bundle, which despite its morphological variability [6,7], is still considered the major pathway for interatrial conduction [11], several other connections were described on the inferior atrial surface. The importance of these connections representing so-called inferior interatrial route has only recently become appreciated.
Understanding the role of the inferior route in interatrial conduction in humans
Though the first epicardial map of atrial activation during sinus rhythm in patients with Wolff–Parkinson–White syndrome was published by Boineau et al. in 1988 [12], it was not until the late 1990s that the ability of the inferior interatrial connections to conduct activation was confirmed by endocardial atrial mapping in humans. Electroanatomical mapping allowed investigators to verify that the area in the vicinity of CS ostium was the site of earliest septal breakthrough during left atrial pacing [13]. Later, the same technique applied to left atrial mapping through the patent foramen ovale provided evidence that both superior and inferior interatrial routes conduct activation from the right to the left atrium during sinus rhythm [11,14].
In an experiment on pigs performed by Schwartzman et al. [15], ablation of the septal regions corresponding to the location of the inferior interatrial bundles in the vicinity of the fossa ovalis and the CS ostium was required for a complete interatrial block in addition to the extensive ablation lesion along the crista terminalis.
Two years later, Markides et al. published the first description of the preferential activation patterns in the human left atrium using the non-contact mapping system [5]. By observing the earliest activation breakthrough in the postero-septal region in the majority (63%) of their 19 patients they have shown for the first time that inferior connections are at least as important as Bachmann's bundle in right-to-left interatrial conduction during sinus rhythm. Observations of the variability in structure and location of Bachmann's bundle published by our and other groups [6,7] may provide an anatomical background for such conclusions. Analysis of biatrial endocardial septal activation and electrophysiological characteristics of conduction over interatrial connections recently performed by Lemery et al. [16] has verified the function of the inferior and superior interatrial routes and their contribution to interatrial conduction in sinus rhythm and during atrial pacing.
High-precision measurements of conduction velocities across the CS ostium recently performed by our group using the CARTO-system has confirmed that patients with paroxysmal atrial fibrillation have slower conduction via the inferior interatrial route [17]. This finding has further reinforced the earlier reported observations [3,4] that strategically located conduction disturbance in the posterior-inferior septal region could be an important predisposing factor to atrial fibrillation.
Components of the inferior route
Several structurally different "non-Bachmann" pathways could potentially provide a basis for interatrial conduction:
- Muscular bundles bridging the inferior interatrial groove at different levels outside CS has recently been described in detail [7,18,19]. Though different in number, size and shape, their position on the inferior atrial surface is in agreement with the activation patterns revealed by endocardial mapping studies [5,14].
- Muscular sleeves extending from the right atrium, forming a muscular cuff around the proximal coronary sinus [19] appeared to be a common finding in our study present in 96% of the specimens. Interestingly, in half of the studied hearts (48%) no atrial musculature extended on the inferior wall of the CS. In these specimens, only the muscular sleeves located between the CS and the inferior left atrial wall could potentially participate in interatrial conduction. This type of connection could provide a route connecting the inferior right atrium with the inferior septal region of the left atrial wall.
- Striated myocardial fascicles between the muscular cuff around the proximal CS and myocardium of the inferior left atrial wall can be considered as extensions of myocardial sleeves originating from the right atrial wall described above. Similar connections described by Chauvin et al. [8] as consistent but variable myocardial structures were identified only in 29% of the specimens in our study. The relatively narrow section of the interatrial septum investigated in our study could explain this discrepancy. Such fascicles can possibly connect the right atrium with more lateral regions of the inferior left atrial wall and, therefore, might not be seen in our serial sections. Whether those thin fascicles were present in a specimen or not, larger interatrial bundles were always found outside the CS region. Those fascicles and the earlier discussed myocardial sleeves form discrete connections between the CS and the left atrial wall which could explain the ability of dissociate electrical activation of the CS from the left atrium [20,21].
- Coronary sinus wall. Our observation of single or grouped smooth-muscle cells not forming a continuous layer in the media of the CS wall does not support clinical significance of electrical conduction through the CS wall per se.
The observation of neural ganglia in the epicardial fat pad in the inferior interatrial groove in the vicinity of the muscular bundles connecting the atria may represent a part of the autonomic neural system, which could potentially affect propagation of electrical impulses over the interatrial bundles. Earlier experimental studies report that in the canine heart three epicardial fat pads containing vagal innervation ganglia are strategically located above the regions containing interatrial connections, i.e. between the inferior vena cava and left atrium, between the right pulmonary vein and atrial junction and between the aorta and the superior vena cava [22,23]. Vagal denervation of the atria experimentally achieved by radiofrequency ablation of these fat pads has been shown to affect selectively atrial electrophysiological properties without affecting the ventricles [24]. Though it remains to be tested in humans, this offers an attractive explanation of the fact that in some patients dynamic interatrial conduction delay associated with initiation of atrial fibrillation may have a vagally mediated origin.
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Conclusion |
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While reporting slightly different observations in regard to the exact location and the structure of the interatrial connections, all studies demonstrate their extremely high variability [6
–8]. The view on the interatrial conductive routes as a combination of primary prominent Bachmann's bundle and the auxiliary inferior connections is transforming into a continuum of variable interatrial connections located both superiorly and inferiorly. Such anatomical variability supported by clinical [5] observations suggests the existence of superior-dominant interatrial conduction with Bachmann's bundle being one major route and the inferior-dominant interatrial connections with inferior connections being another. Whether or not such anatomical variations contribute to the predisposition to certain arrhythmias still remains unclear. However, several clinical studies have reported that conduction delay in the inferior septal region of the right atrium and the proximal CS are linked to the development of atrial fibrillation [2,3,25]. |
Acknowledgements |
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The authors thank Dr Siew Yen Ho, Department of Paediatrics, National Heart Lung Institute, London, UK and Prof. S. Bertil Olsson, Department of Cardiology, Lund University, Sweden, for their valuable advice during the preparation of the manuscript. The study was supported by research grants from the Swedish Heart-Lung Foundation and the Franke and Margaretha Bergqvist Foundation.
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