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Ann Thorac Surg 1995;60:561-569
© 1995 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Atrial Appendages and Venoatrial Connections in Hearts From Patients With Visceral Heterotaxy

Hideki Uemura, MD, Siew Yen Ho, PhD, William A. Devine, BSc, Lucienne L. Kilpatrick, BSc, Robert H. Anderson, MD

National Heart & Lung Institute, London, England, and Children's Hospital of Pittsburgh, Pittsburgh, Pennsylvania

Accepted for publication April 19, 1995.


   Abstract
Top
 Footnotes
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background. Venoatrial connections are important when choosing surgical options for patients with visceral heterotaxy. The precise morphology of the atriums, however, is often obfuscated by the term ``visceral heterotaxy.'' This morphologic study aims to clarify the features of significance to the cardiac surgeon.

Methods. We investigated 183 hearts from patients known from postmortem inspection to have so-called visceral heterotaxy. The connections of the systemic and pulmonary veins to the atriums, and the detailed morphology of the atriums, were examined in each case.

Results. Pectinate muscles extended bilaterally to the crux in 125 hearts determined to have isomeric morphologically right appendages. The other 58 hearts all exhibited bilaterally smooth-walled vestibules, and were diagnosed as having isomeric left appendages. Bilateral superior caval veins were frequent in both groups. The inferior caval vein was right- or left-sided with equal frequency in both groups, but was interrupted only in hearts with isomeric left appendages. The pulmonary veins connected in extraatrial fashion in 48% of cases with isomeric right appendages, whereas, most commonly, pulmonary veins were connected bilaterally to the atriums in those with isomeric left appendages (60%).

Conclusions. Both the morphology of the atrial appendages and the venoatrial connections need to be distinguished to establish precise diagnoses in patients with so-called visceral heterotaxy (``splenic syndromes'').


   Introduction
Top
 Footnotes
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Surgical treatments, either through anatomic biventricular repairs [1, 2] or right heart bypass procedures [3, 4], are increasing in patients with visceral heterotaxy. If optimal outcomes are to be achieved in either the short or the long term, it is crucial to establish precisely the patterns of venoatrial connections. These connections can obviously influence the choice of surgical strategy, as well as determining the potential for obstruction subsequent to surgical reconstruction [4–6]. It has also been suggested that venous connections can be used in all hearts to determine atrial arrangement (``situs''), and that earlier observations that indicated that the atrial appendages were isomeric in these hearts are no more than a useful mnemonic [7, 8]. With these disagreements in mind, we have studied a large series of hearts from patients known to have visceral heterotaxy, concentrating on the morphology of the atrial chambers and the patterns of venoatrial connection, to elucidate the anatomic features of particular surgical significance.


   Material and Methods
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
We used the principles of sequential segmental analysis [9–11] to study 183 hearts from patients known from postmortem inspection to have visceral heterotaxy (``splenic syndromes''). Of the hearts, 46 came from the National Heart & Lung Institute in London, England; 75 from the Children's Hospital of Pittsburgh, Pittsburgh, Pennsylvania; 43 from the National Cardiovascular Center in Osaka, Japan; and 19 from the Royal Children's Hospital in Liverpool, England. The systemic and pulmonary veins, and the fashions of their connections to the atrial chambers, were examined together with details of the internal and external features of the atrial appendages, relating the latter features to the arrangement seen in the normal heart [12]. The presence of a prominent terminal crest, along with a triangular appendage having a broad junction with the venous component, are well-recognized features of the normal morphologically right atrium. Another important feature, however, is the extent of the prominent pectinate muscles within the appendage relative to the muscular vestibule of the tricuspid valve (Fig 1AGo). In the normal left atrium, the muscular vestibule of the mitral valve is always confluent with the smooth aspect of the pulmonary venous component (Fig 1BGo), with no pectinate muscles interposing. This is in addition to the better recognized diagnostic features for the morphologically left appendages of absence of the terminal crest and presence of a narrow junction between the tubular appendages and the rest of the atrium.



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  		Fig 1. . Pectinate muscles unequivocally extend to the post-eustachian sinus in the normal right atrium (A), while the normal mitral vestibule is confluent with the venous component of the normal left atrium, there being no intervening pectinate muscles (B). Bilateral presence (C) or absence (D) of pectinate muscles at the crux of the heart proved to be an unequivocal landmark for distinction of isomeric arrangements of the appendages in all hearts studied in our series.

 

   Results
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
External and Internal Features of Atrial Chambers
In all the hearts from patients with visceral heterotaxy, the arrangement of the pectinate muscles relative to the vestibules proved to be an absolute guide for distinction of morphologically right and morphologically left atrial appendages. Thus, presence of pectinate muscles extending bilaterally around the muscular atrioventricular vestibules permitted us to diagnose 125 cases as showing isomerism of the morphologically right appendages (Fig 1CGo). In contrast, in the remaining 58 hearts diagnosed as showing isomerism of the morphologically left appendages, no specimen demonstrated bilateral extensions of pectinate muscles around the posterior muscular atrioventricular vestibules (Fig 1DGo). Although minimal extensions toward the lateral sides of the atrioventricular junctions were found unilaterally or bilaterally in 21% of this latter group of hearts, continuity was always seen between the vestibule of the atrioventricular junction and the smooth-walled venous component of the atrium, this area not being interrupted by the presence of pectinate muscles. In addition to the feature of the extent of the pectinate muscles, the presence bilaterally of the anticipated external features of either the morphologically right or the left appendage was a good distinguishing feature, but by no means a perfect one (Table 1Go). Thus, atypically shaped appendages or intermediate patterns in the shape of the junctions between the appendages and the venous components were found unilaterally or bilaterally in some of the hearts from both groups (Fig 2Go). The presence or absence of a terminal crest was similarly not a constant feature for either group.


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  		Table 1. . Features of Atrial Appendages When Judged in Relation to the Disposition of the Pectinate Muscle
 


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  		Fig 2. . Atypically shaped appendages, or an intermediate nature of the junction between the appendage and the rest of atrial component, was seen in some of our specimens.

 
Systemic Venoatrial Connections
The superior caval vein is normally connected to the atrial roof with the terminal crest interposed between the smooth-walled venoatrial connection and the pectinated appendage [12]. Of 186 connections between the superior caval veins and the atria in hearts with isomeric right appendages (Table 2Go): this characteristic relation was found in 179 (96%), the terminal crest being absent in the rest of the cases. In contrast, of 79 instances in which the superior caval vein connected to the atrial roof in the setting of isomeric left appendages, this anticipated pattern was seen in only 7 (9%). In the other 72, the venoatrial connection was distant from the junction of the appendage with the rest of the atrial musculature. In 1 particular heart with isomeric right appendages, a solitary left-sided superior caval vein had no connections to the atrial chamber, but drained via the left-sided azygos system into the inferior caval vein. Another atypical case with isomeric left appendages showed continuation of a solitary left-sided superior caval vein to the coronary sinus.


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  		Table 2. . Patterns of Superior Caval Vein Drainage
 
The inferior caval vein, in the normal heart, has a characteristic pattern of drainage to the right atrium adjacent to the orifice for the coronary sinus, and is additionally related to both the eustachian valve and the terminal crest [12]. The coronary sinus, defined as a circumflex venous channel running in the atrioventricular groove and either receiving the oblique vein of Marshall or containing the venous valve of Vieussens [13], could be identified in 24 of the hearts with isomeric left appendages (41%). In 3 of these, the course of the sinus along the atrioventricular groove was partially unroofed. In the remaining 34 cases with isomeric left appendages, and in all 125 hearts with isomeric right appendages, the coronary sinus as defined above was entirely lacking. The Eustachian valve, or its remnant, was present in only 23 (18%) and 6 (10%) of the hearts with isomeric right and left appendages, respectively. The orifice of the inferior caval vein in all hearts with isomeric right appendages was separated from the smooth vestibule of the atrioventricular junction by the extensive arrangement of the pectinate muscles. In those with isomeric left appendages, the inferior caval vein was connected directly to the atrium in only 14 cases (Table 3Go). In 1 of them, dual inferior caval veins were present, the left-sided vein being connected to the right-sided atrium, whereas the right-sided vein was interrupted and drained via the right-sided azygos vein. The relationship of the orifices of the coronary sinus and the inferior caval vein were as seen in the normal heart (or its mirror image) in 8 specimens, although all of these lacked an Eustachian valve or its remnant. In the other 6, the wall of the inferior caval vein was in direct continuity with the smooth-walled vestibule of the atrioventricular junction, no extensions of pectinate muscles interposing.


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  		Table 3. . Patterns of Inferior Caval Vein Drainage
 
Hepatic drainage via isolated and independent channels was seen more frequently in hearts with isomeric left than in those with isomeric right appendages (p < 0.01 by {chi}2 test) (Table 4Go). This feature bore no relationship to presence or absence of interruption of the inferior caval vein. In 1 heart with isomeric left appendages, a component of hepatic venous drainage drained through the coronary sinus, with the rest joining the atrium via the inferior caval vein.


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  		Table 4. . Patterns of Hepatic Vein Drainage
 
Pulmonary Venous Connections
The drainage of the pulmonary veins was more complicated in the group of hearts with isomeric right than in those with isomeric left appendages (Table 5Go). Among 52 hearts with isomeric right appendages in which all pulmonary veins had direct connections to the atrium, 4 cases showed an unusual pattern in which a centrally located confluence drained through fenestrations into both the right-sided and the left-sided atrial chambers. Such a confluence, forming, as it were, a common pulmonary venous chamber, was also found connecting unilaterally to one or other atrium at or near its roof in 45 instances. The pulmonary venous confluence thus formed lacked any myocardial structures within its wall. Thus, the parietal musculature, which is usually interposed between the right and left pulmonary venous connections to the atrium as a typical feature in the normal heart (Fig 3AGo), was lacking in all but 3 of the group of hearts with isomeric right appendages, the wall of the confluence being composed only of fibrous tissue (Fig 3BGo). A pulmonary venous confluence distinct from but draining to the atrium was not found in any heart with isomeric left appendages. Rather, the veins joined the atrial musculature, either unilaterally or bilaterally, in the fashion anticipated for the normal heart (Fig 3CGo).


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  		Table 5. . Patterns of Drainage of Pulmonary Veins
 


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  		Fig 3. . The arrangement of the pulmonary venous connections in the normal heart includes the universal presence of atrial musculature between the junctions of the right and left pulmonary veins to the left atrium (A, B). This feature was almost always absent in our hearts with isomeric right appendages, even when all the pulmonary veins were connected to the atrial wall (C). In contrast, such parietal musculature was present in those with isomeric left appendages having bilateral connections of the pulmonary veins, the right and left pulmonary venoatrial junctions being widely separated (D).

 
Overall Pattern of Venous Drainage
A relatively normal or a mirror-imaged pattern of venous drainage, with all the systemic veins connected with one atrium and all the pulmonary veins to the other atrium, was seen in only 13 hearts with isomeric right appendages (11%) and in 8 of those with isomeric left appendages (14%) (Table 6Go).


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  		Table 6. . Overall Pattern of Venous Drainage
 
Splenic Status
Autopsy records were available concerning splenic status in 123 of the patients studied (68%). In the hearts shown, on the basis of the extent of pectinate muscles, to have isomerism of morphologically right appendages, the spleen was absent in the majority (65 of 82 cases; 79%). A solitary spleen was present in 14 cases (17%), being right-sided in 7, left-sided in 6, and in the midline in 1. Multiple spleens were found in 3 cases (4%). In those with isomeric left appendages, multiple spleens were detected in 36 cases (88%). A solitary spleen was found in 3 (7%), being right-sided in 2 and left-sided in 1, but splenic tissue was absent in the remaining 2 (5%).

Pulmonary Morphology
Information could be obtained concerning the bronchial tree in 111 cases with isomeric right and in 53 with isomeric left appendages. Of these, 1 case with isomerism of right atrial appendages exhibited aplasia of the right lung, along with agenesis of the right bronchus. Another 2 cases, 1 with isomeric right and the other with isomeric left appendages, had an abnormality of the bronchus to the left upper lobe. Excluding these 3, bilaterally short and eparterial bronchi were present in the majority of those with isomerism of the morphologically right appendages (in 97, 89%), but in none of those with isomeric left appendages. Bilaterally long and hyparterial bronchi were seen in almost all the patients with isomerism of morphologically left atrial appendages (in 51 cases; 98%), and were not detected in the setting of isomerism of the right atrial appendages. In 9 cases with isomeric right atrial appendages (8%), and in 1 case with isomeric left appendages (2%), the bronchial pattern was usual, whereas in the remaining 3 patients with isomeric right appendages the pattern was mirror imaged.

Information was also available concerning lobation in 109 cases with right isomerism (88%) and 54 with left isomerism (93%). Excluding the case with aplasia of the right lung, three lobes were found bilaterally in 79 cases with isomeric right appendages (73%), and in 2 with isomeric left appendages (4%). There were 40 cases with isomeric left appendages having two lobes on both sides (74%), whereas 2 cases with isomeric right appendages showed a similar pattern (2%). Usual pulmonary lobation was seen in 5 cases in each of the groups (5% and 9%, respectively). Mirror imagery, with a bilobed right-sided lung along with a trilobed left-sided lung, was less common (in 2 and 4 hearts with isomeric right and left appendages; 2% and 7%, respectively). Other unusual patterns of lobation, such as absence of lobation or presence of more than three lobes, were demonstrated in 20 cases with isomeric right appendages (18%) and in 3 with isomeric left appendages (6%).


   Comment
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
In the past, the patients collected within the overall heading of visceral heterotaxy have been analyzed in various fashions. It has been conventional over the years to describe these characteristic groups in terms of asplenia and polysplenia. During this period, however, Van Mierop and colleagues [14, 15], along with Moller and associates [16], had emphasized the tendency in these syndromes toward isomerism of the thoracic organs.

We, too, in earlier investigations, had been struck by the potential isomerism of the atrial appendages. Indeed, from these studies we had concluded that the anatomic features of the appendages could be used with just as much, if not more, efficacy as the state of the spleen to divide the overall group of heterotaxy into the entities of right and left isomerism [9–11,17]. It further seemed that these groupings could not only be distinguished from each other, but could also be recognized as discrete from the patterns of usual atrial arrangement (situs solitus) and mirror-imagery (situs inversus). It was, perhaps, unfortunate, therefore, that we initially chose the words ``atrial isomerism'' to describe these findings rather than ``isomerism of the atrial appendages.'' ``Left atrial isomerism'' could be taken to describe a heart with eight pulmonary veins! This, of course, never exists. At the same time, others have argued that the venoatrial connections can be used to place all hearts within the groups of solitus and inversus [7, 18]. Our previous findings, endorsed by this study, militate against this possibility.

Although it has been held to have no clinical significance [19], this distinction between atrial arrangement determined according either to venous connections or to the morphology of the appendages is surely important for the surgeon. Consider, for example, the situation in which a patient with congenital absence of the spleen has morphologically right atrial appendages present bilaterally, with an intact atrial septum or a small atrial septal defect of the ``oval fossa'' type, but with all four pulmonary veins connected to the right-sided atrium and all the systemic veins connected to the left-sided atrium. Two such hearts were encountered in our material, and 1 is illustrated in Figure 4Go. According to our findings, such patients have isomerism of the morphologically right atrial appendages. With this information to hand, the surgeon, if needing to open the right-sided atrium, will know that all previous histologic studies have shown that sinus nodes will be present bilaterally [14,20–22]. In contrast, if the diagnosis of ``situs inversus'' is made on the basis of venous connections in these cases, and no description is given of the morphology of the appendages, the surgeon might presume that a sinus node is present only on the left side, introducing the potential risk of damage to the unsuspected right-sided sinus node, which is almost certainly present.



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  		Fig 4. . A heart from a patient with visceral heterotaxy in which the left-sided atrium received all the systemic venous drainage (A) and the right-sided atrium received all the pulmonary venous drainage (B). Notwithstanding the presence of isomeric right appendages bilaterally on the basis of the extent of the pectinate muscles, the pattern of venous drainage is that of ``situs inversus.'' This would be confusing if chosen as the criterion for determination of the location of the sinus node, which is almost certainly present bilaterally at the sites shown by the asterisks.

 
Our study shows that such disagreements are unnecessary. The morphology of the appendages as well as the venoatrial connections are important, and both need description. When describing the appendages, however, it was necessary to determine if rules could be established for their unequivocal identification. As had been stressed [7], the shape of the appendage and the nature of its junction to the venous components of the atrium are not infrequently ambiguous in hearts from patients with visceral heterotaxy. Our present study confirmed this finding. Because of this, we sought additional criteria for diagnosis of morphologic rightness and leftness. Having studied a large number of normal hearts, the extent of the pectinate muscles around the atrioventricular junctions emerged as an obvious feature distinguishing the morphologically right from the left appendage. This feature also proved absolute in our hands in distinguishing isomeric right or left appendages in all the hearts from our patients with visceral heterotaxy. When we then studied the overall patterns of venoatrial connections in these hearts, it did not prove possible to divide our group into discrete patterns of usual drainage (solitus) or mirror-imagery (inversus). Rather, according to our observations the arrangement of the atrial appendages as determined on the basis of the extent of the pectinate muscles permits all hearts to be placed in one of four groups, namely those with usual arrangement, mirror-imagery, isomeric right appendages, or isomeric left appendages. It is an easy matter then to describe anomalies of venous connection for each of these groups, particularly those with isomeric appendages in which abnormal venoatrial connections are the rule. In addition to this, recognition of a morphologically right appendage enables the surgeon to predict with confidence the precise location of the sinus node, whereas recognition of isomerism of the left appendages alerts the surgeon to a situation in which the atrial pacemaker is known to be abnormally located [20, 21, 23].

These distinctions according to appendage morphology have other more functional implications. The pulmonary venous return, for example, can scarcely be anatomically normal when connecting to the atrial chambers in hearts with isomeric right appendages [17]. Thus, in hearts in which the confluence of the pulmonary veins forms a cavity with fibrous walls distinct from the muscular parietal walls of the atrial chambers, the surgeon must decide whether, in the process of surgical treatment, it is possible to obtain unobstructed pulmonary venous return without enlargement of the junction of the fibrous confluence with the muscular atrium. The presence of pectinate muscles extending all around the muscular atrioventricular vestibules of hearts with isomeric right appendages could also pose problems when attempting to repair cases with extracardiac types of anomalous pulmonary venous connection, because it may well prove difficult to create an ideal anastomosis between the extracardiac pulmonary venous confluence and the pectinated atrial wall. In hearts with isomeric left appendages, in contrast, the arrangement of the pulmonary veins and their related atrial musculature tends to be anatomically normal. When viewed in the context of the entire atrial chambers, however, there is a significant distance between bilateral connections of right- and left-sided pulmonary veins. In terms of the surgical approach, such bilateral pulmonary venous drainage must also be recognized as abnormal, because it makes potential suture lines for any intraatrial baffle elongated and complex.

In the minority of cases with isomeric appendages in which one atrial chamber receives all the systemic venous drainage and the other accepts the entire pulmonary venous drainage, atrial septation could readily be achieved as part of biventricular repair (providing, of course, that ventricular morphology is suitable for such a corrective operation). Atrial septation will be much harder in the majority. If required, the orientation of the systemic and the pulmonary venous connections must be determined precisely before the operation. Knowledge of such precise patterns of systemic venous drainage is also a prerequisite for successful initial establishment of cardiopulmonary bypass. We conclude, therefore, that it is necessary to determine both the morphology of the appendages and the venoatrial connections in hearts with visceral heterotaxy. Once identified, the presence of isomeric appendages permits still further inferences to be drawn. Thus, the venous drainage from the heart itself is known to be grossly abnormal in hearts with isomeric atrial appendages [24]. The ventricular structures are similarly abnormal, particularly in hearts with isomeric right appendages, when compared with features in those with usual atrial arrangement [25]. We cannot agree, therefore, with those investigators who state that the patterns of arrangement of the atrial appendages are of no surgical or clinical significance [19].


   Acknowledgments
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
We express special thanks to Dr Audrey Smith and Dr. Chikao Yutani for generously permitting us to study hearts from the collections at the Royal Liverpool Children's Hospital in Liverpool, UK, and at the National Cardiovascular Centre in Osaka, Japan.

During this investigation, Dr Uemura was a Senior Research Fellow at the National Heart & Lung Institute and supported by project grants 93100 and 94079 from the British Heart Foundation. Doctor Ho, Mrs Kilpatrick, and Professor Anderson are also supported by the British Heart Foundation.


   Footnotes
Top
 Footnotes
Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Address reprint requests to Dr Anderson, Department of Paediatrics, National Heart & Lung Institute, Dovehouse St, London SW3 6LY, England.


   References
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

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  6. Kawashima Y. Discussion of Mayer JE Jr, Helgason H, Jonas RA, et al. Extending the limits for modified Fontan procedures. J Thorac Cardiovasc Surg 1986;92:1021–8; and DeLeon SY, Ilbawi MN, Idriss FS, et al. Fontan type operation for complex lesions. Surgical considerations to improve survival. J Thorac Cardiovasc Surg 1986;92:1029–37.[Abstract]
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  18. Van Praagh S, Kreutzer J, Alday L, Van Praagh R. Systemic and pulmonary venous connections in visceral heterotaxy, with emphasis on the diagnosis of the atrial situs: a study of 109 postmortem cases. In: Clark E, Takao A, eds. Developmental cardiology, morphogenesis and function. Mt. Kisco, NY: Futura, 1990:671–721.
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