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Europace Advance Access published online on August 28, 2007

Europace, doi:10.1093/europace/eum175
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© The European Society of Cardiology 2007. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Anatomic relations of the Marshall vein: importance for catheterization of the coronary sinus in ablation procedures

Ítalo Martins de Oliveira1,* {dagger}, Maurício Ibrahim Scanavacca1,2, Aristides Tadeu Correia1,2, Eduardo Argentino Sosa1,2 and Vera Demarchi Aiello1,2

1 Heart Institute (InCor), University of São Paulo School of Medicine, São Paulo, Brazil; 2 Av. Dr. Enéas de Carvalho Aguiar, 44, Clinicas, São Paulo CEP 05403-000, São Paulo, Brazil

Manuscript submitted 27 October 2006. Accepted after revision 14 July 2007.

* Corresponding author. Tel: +55 11 3069 5252; fax: +55 11 3069 5279. E-mail address: italomartins{at}terra.com.br. Address for correspondence: Instituto do Coração HC FMUSP, Laboratório de Anatomia Patológica, Av. Dr. Enéas Carvalho Aguiar 44, 05403-000, São Paulo, Brazil


    Abstract
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
 References
 
Aims: Our objective was to study the anatomic relations of the human left atrial oblique vein (Marshall vein), particularly of its ostium opening into the coronary sinus, in order to guide ablation procedures related to that vein.

Methods and results: The study was carried out in 23 heart-specimens (mean weight 446 ± 204 g) of individuals whose mean ages were 43 ± 21 years, 20 males. The coronary sinus was opened longitudinally, exposing the ostium of the tributary veins; the Vieussens valve was looked for, as well as its relationship to the left atrial oblique vein. The diameters of the left atrial oblique vein and the coronary sinus ostia were measured and the distance between them was determined. The left atrial oblique vein could be identified in 20 (87%) of the hearts, while the Vieussens valve was present in 17 (74%) of the specimens (in 16 of which the left atrial oblique vein was identified). In such condition, the vein was adjacent to the Vieussens valve and proximally positioned relative to the coronary sinus ostium in most of them (14/16 cases). The mean diameters of the left atrial oblique vein and of the coronary sinus ostia were, respectively, 1.23 ± 0.38 and 8.22 ± 1.88 mm. The mean distance between both ostia was 30.9 ± 10.2 mm.

Conclusion: When present, the left atrial oblique vein can be easily recognized, adjacent to the Vieussens valve. The mean distance between the coronary sinus opening and left atrial oblique vein ostium was around 30 mm, independently of the heart weight and the presence of cardiomegaly.

Key Words: Marshall ligament, Left atrial oblique vein, Atrial fibrillation


    Introduction
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
 References
 
The remnants of the left superior caval vein or Marshall ligament,1Go a fold of the visceral pericardium containing muscular, vascular, and nervous structures, were recently recognized as a possible origin of electrical ectopic activity which deflagrates atrial fibrillation.2Go Once the Marshall ligament participation in the atrial fibrillation mechanism is demonstrated, its ablation may avoid recurrences.2Go However, one of the necessary conditions for such a demonstration is its identification during the atrial fibrillation ablation procedure.

The left atrial oblique vein, also known as the Marshall vein, is an embryonic remnant of the left superior caval vein which is enclosed within the Marshall ligament. Its identification during ablation procedures through catheter is a specific marker of the ligament anatomic position.2Go

Haissaguerre et al.3Go–5Go suggested that the pulmonary veins are the main site of origin of ectopic foci which deflagrate atrial fibrillation in human beings. The ablation of muscular bands inside the pulmonary veins with radiofrequency or its empiric isolation controls paroxysmal atrial fibrillation in 70% of the patients.6Go However, 20–30% of the patients show recurrent atrial fibrillation, probably originating out of the pulmonary veins. Hwang et al.7Go characterized the left atrial oblique vein in humans and documented the occurrence of ectopic activity originating from the Marshall ligament deflagrating atrial fibrillation after adrenergic stimulation. Wei-Shiang Lin et al. also observed double-electrical potential in the left atrial oblique vein in patients with paroxysmal atrial fibrillation. They conclude that the double-potential characteristics suggest that in sinusal rhythm, the first potential originates from the myocardium and the second one from the muscular band inside the Marshall ligament.2Go During atrial fibrillation deflagration, the activation inversion of such potentials was observed at its beginning, suggesting the left atrial oblique vein as the origin of the atrial fibrillation in those patients.

Due to the relevance of studies suggesting a relationship between the Marshall ligament and the paroxysmal atrial fibrillation, a complete morphologic description has become essential to guide the approach to that structure.

This research aims at studying the left atrial oblique vein anatomic relations in human hearts, describing its position related to the coronary sinus ostium and its course in the left atrial posterior wall.


    Methods
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
 References
 
The study was accomplished in 23 human heart-specimens, 11 of which (group I), from patients died due to heart diseases and submitted to necropsies at the Laboratory of Pathology of the Heart Institute (InCor), University of São Paulo School of Medicine. The second group (group II) included 12 hearts from Anatomic Museum of the Heart Institute (InCor) from patients who were submitted to necropsies at the Medical Examiner of the City (Serviço de Verificação de Óbitos da Capital—São Paulo—SVOCSP) and died form non-cardiac diseases. The present study complies with the Declaration of Helsinki and was authorized by the Scientific Commission of Heart Institute (InCor).

The hearts in the first group (group I) were all from male patients. Their age ranged from 34 to 87 years (62 ± 15) and the heart weight varied from 480 to 820 g (632 ± 126). In the second group, patients ages ranged from 18 to 46 years (26 ± 8), and there were three females and nine males. The heart weights varied from 183 to 370 g (274 ± 48) (Table 1).


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Table 1 Patients age, gender, heart weight, and main disease

 
After fixation of the specimens in formalin, the coronary sinus ostium was identified. A longitudinal section of its free wall was performed, exposing the ostium of the tributary veins. The Vieussens valve was looked for, as well as the left atrial oblique vein ostium (Figure 1). When the left atrial oblique vein ostium was identified, a metal guide was inserted and its progression through the left atrium wall was followed; the path was then established. The following measures were accomplished: the distance between the coronary sinus and the left atrial oblique vein ostia (CSO–LaOv-O), the distance between the Vieussens valve and the left atrial oblique vein ostium (VV–LaOv-O), and the distance between the Vieussens valve and coronary sinus ostium (VV–CSO), all obtained with a pachymeter. The left atrial oblique vein ostium diameter (LaOv-D) and the coronary sinus ostium diameter (CSO-D) were measured with probes (1.0–15.0 mm).


Figure 1
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Figure 1 Opened coronary sinus, displaying the Vieussens valve (VV) and the ostium of the left atrial oblique vein (LaOv).

 
All continuous variables are expressed as mean ± SD and proportions are expressed as proportion ± confidence interval. Comparisons of data among different groups were performed using unpaired Student's t-test, and correlation between continuous variables was tested with Pearson's correlation coefficient. A P-value <0.05 was considered statistically significant.


    Results
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
 References
 
The left atrial oblique vein was identified in 20 (87% ± 13%CI) hearts. The mean diameters of the left atrial oblique vein ostium were 1.56 ± 0.42 (group I) and 1.0 ± 0.0 (group II), P < 0.01. The mean diameters of the coronary sinus ostium were 9.45 ± 1.97 (group I) and 7.08 ± 0.79 (group II), P < 0.05. These values are expressed in Table 2.


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Table 2 Mean diameters of the left atrial oblique vein ostium and coronary sinus ostium

 
The Vieussens valve was present in 17 (74% ± 17.8% CI) of the hearts, in 16 of which the left atrial oblique vein was identified. In such a condition, the left atrial oblique vein ostium was adjacent to the Vieussens valve (mean VV–LaOv-O 1.98 ± 1.88 mm) and between the valve and coronary sinus ostium. In only two hearts (13%), the Vieussens valve was located away from the left atrial oblique vein ostium, with a mean distance to the coronary sinus orifice of 17.5 mm). All Vieussens valves studied were composed of one cusp (Figure 2).


Figure 2
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Figure 2 The negative values correspond to the cases presenting the left atrial oblique vein ostium distal to the Vieussens valve.

 
The left atrial oblique vein projected obliquely to the lateral and posterior aspect of the left atrium, running towards the left inferior pulmonary vein and reaching the superior pulmonary veno-atrial junction (Figures 3 and 4). Anatomically, it is the atrial tributary that joins the great cardiac vein at the point where latter becomes the coronary sinus.


Figure 3
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Figure 3 Lateral-left-posterior aspect of the heart showing the dissected left atrial oblique vein (LaOv, arrow), displaying its oblique course, beginning near the inferior left pulmonary vein.

 


Figure 4
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Figure 4 Left-posterior aspect of the heart showing the dissected left atrial oblique vein (arrows), reaching the opened coronary sinus.

 
The mean distance between the ostia of the left atrial oblique vein and coronary sinus was 30.9 ± 10.2 mm (group I 26.2 ± 13.02 mm and group II 34.0 ± 6.71 mm; P = 0.15). As we tested the possible correlation between the distance of the coronary sinus orifice to the left atrial oblique vein ostium and the heart weight or the diameter of the coronary sinus orifice, no statistical significance was found with very low correlation coefficients (r = 0.141 and r = 0.063, respectively). As we tested the possible correlation between the heart weight and the diameter of the coronary sinus ostium, the correlation analysis was of r = 0.648; P < 0.005 (Figures 2,5,6 and 7).


Figure 5
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Figure 5 Correlation analysis: r = 0.141; P non-significant.

 


Figure 6
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Figure 6 Correlation analysis: r = 0.063; P non-significant.

 


Figure 7
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Figure 7 Correlation analysis: r = 0.648, P < 0.005.

 

    Discussion
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
 References
 
In 1850, Marshall1Go described a ligament which takes his name. It consists of fibrous and muscular bands, nervous and small blood vessels involved in pericardial fat. Chaffanjon et al.8Go described that a vestigial pericardial fold involves the Marshall Vein (Marshalls fold), close to left pulmonary venous recess. Following this structure, the left atrial oblique vein runs obliquely on the posterior surface of the left atrium and towards the left superior pulmonary vein, draining the posterior wall of the left atrium. The left atrial oblique vein is the atrial tributary that joins the great cardiac vein at the point where latter becomes the coronary sinus.9Go Marshall also described it as a vestigial tissue of the embryonary venous sinus and of the left common cardinal vein.

In the present study, it was possible to identify this vein with a frequency of 87%. It was also possible to define its ostium dimensions as well as its proximity in relation to the pulmonary veins. Melo et al.14Go identified the left atrial oblique vein in only 8 (26%) out of the 30 patients studied by coronary venous angiography.

The left atrial oblique vein drains adjacent to the Vieussens valve, present as a membranous remnant with indefinite functional value. In the present study, all valves were composed of a single cusp, while Silver and Rowley15Go described a 55–74% frequency of two-cusped valves. Maros et al.13Go in an anatomical study, observed that in 20% of the hearts, the left atrial oblique vein ostium was obliterated and that the Vieussens valve was present in the great majority of them (78%). Silver et al. observed that in 19 of 50 human hearts (79%), the Vieussens valve was present.

Sherlag10Go proposed the presence of cardiac specific muscle inside the Marshall ligament in canine hearts. The presence of muscular bands forming multiple and complex connexions with the adjacent atrial myocardium and the coronary sinus musculature was demonstrated. They are well isolated by adipose tissue and also innervated by sympathetic nervous fibers,11Go in this context suggesting the presence of a structure which is susceptible to the re-entry mechanism. Also in canine hearts, the Marshall ligament is sensitive to catecholamines, and this may be the substrate for the development of atrial adrenergic tachyarrhythmias.12Go

The presence of the Vieussens valve is an important anatomical reference for the left atrial oblique vein ostium, facilitating its identification. During catheterization of the coronary sinus, such feature can be perceived by the blocking of the catheter passage through this structure. Nevertheless, we should keep in mind that in 13% of our cases, the left atrial oblique vein ostium was located distally in relation to the Vieussens valve, which may explain difficulties in the vein catheterization in some patients.

Silver and Rowley described a significant difference in the coronary sinus volume between hearts with weights superior and inferior to 400 g, however, they failed to demonstrate a significant difference in the coronary sinus ostium diameter.

Based on the lack of correlation between the distance of the left atrial oblique vein ostium to the opening of the coronary sinus and the heart weight, we may expect in average to find the left atrial oblique vein ostium at ~30 mm from the coronary sinus ostium, independent of the heart weight or the presence of cardiomegaly. This finding can prove to be a very useful information in the catheterization laboratory, during ablation procedures.


    Conclusion
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
 References
 
The left atrial oblique vein is present in most of the human hearts and is easily identifiable as the first atrial vein reaching the coronary sinus lumen at ~30 mm from the coronary sinus ostium, independently of the heart weight or the presence of cardiomegaly.

The left atrial oblique vein ostium is related to the Vieussens valve, being proximal relative to the coronary sinus ostium in more than 80% of the cases.

Conflict of interest: none declared.


    Footnotes
 
{dagger} During the development of this study, I M Oliveira was a visiting medical student at the Laboratory of Pathology of the Heart Institute (InCor), University of São Paulo. Back


    References
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
 References
 
[1] Marshall J. On the development of the great anterior veins in man and mammalia: including an account of certain remnants of fetal structure found in the adult, a comparative view of these great veins in the different mammalia, and an analysis of their occasional peculiarities in the human subject. Philos Trans R Soc Lond (1850) 140:133–69.[CrossRef]

[2] Lin WS, Prakash VS, Tai CT, Hsieh MH, Tsai CF, Yu WC, et al. Pulmonary vein morphology in patients with paroxysmal atrial fibrillation initiated by ectopic atrial beats originating from the pulmonary veins. Implication for catheter ablation. Circulation (2000) 101:1274–81.[Abstract/Free Full Text]

[3] Haissaguerre M, Jais P, Shah DC, Garrigue S, Takahashi A, Lavergne T, et al. Electrophysiological end point for catheter ablation of atrial fibrillation initiated from multiple pulmonary venous foci. Circulation (2000) 101:1409–17.[Abstract/Free Full Text]

[4] Haissaguerre M, Jais P, Shah DC, Takahashi A, Hocini M, Quiniou G, et al. Spontaneous initiation of atrial fibrillation by ectopic beats originating in the pulmonary veins. N Engl J Med (1998) 339:659–66.[Abstract/Free Full Text]

[5] Haissaguerre M, Jais P, Shah DC, Gencel L, Pradeau V, Garrigues S, et al. Right and left atrial radiofrequency catheter therapy of paroxysmal atrial fibrillation. J Cardiovasc Electrophysiol (1996) 7:1132–44.[Web of Science][Medline]

[6] Hocini M, Ho SY, Kawara T, Linnenbank AC, Potse M, Shah D, et al. Electrical conduction in canine pulmonary veins: electrophysiological and anatomic correlation. Circulation (2002) 105:2442–8.[Abstract/Free Full Text]

[7] Hwang C, Wu TJ, Doshi RN, Peter CT, Chen PS. Vein of Marshall cannulation for the analysis of electrical activity in patients with focal atrial fibrillation. Circulation (2000) 101:1503–5.[Abstract/Free Full Text]

[8] Chaffanjon Ph, Brichon PY, Faure C, Favre JJ. Pericardial reflection around the venous aspect of the heart. Surg Radiol Anat (1997) 19:17–21.[Web of Science][Medline]

[9] Gilard M, Mansourati J, Etienne Y, Larlet J, Troung B, Boschat J, et al. Angiographic anatomy of the coronary sinus and its tributaries. Pacing Clin Electrophysiol (1998) 21:2280–4.[CrossRef][Medline]

[10] Sherlag BJ. The re-entry concept as the basis for clinical arrhythmias. Arch Inst Cardiol Mex (1991) 61:5465–73.

[11] Dave TK, Angela CL, Chun H, Ling-Tao F, Hyrar SK, Peng-Sheng C, et al. The ligament of Marshall: a structural analysis in human hearts with implications for atrial arrhythmias. J Am Coll Cardiol (2000) 36:1324–7.[Abstract/Free Full Text]

[12] Doshi RN, Wu TJ, Yashima M, Kim YH, Ong JJ, Cao JM, et al. Relation between ligament of Marshall and adrenergic atrial tachyarrhythmia. Circulation (1999) 100:876–83.[Abstract/Free Full Text]

[13] Maros TN, Rácz L, Plugor S, Maros TG. Contributions to the morphology of the human coronary sinus. Anat Anz (1983) 154:133–44.[Web of Science][Medline]

[14] Melo WDS, Prudêncio LAR, Kusnir CE, Pereira ALN, Marques V, Vieira MC, et al. Anatomia Angiográfica do Sistema Venoso Coronário. Aplicações em Eletrofisiologia Clínica. Arq Bras Cardiol (1998) 70:409–13.[Medline]

[15] Silver MA, Rowley NE. The functional anatomy of the human coronary sinus. Am Heart J (1988) May:1980–4.


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