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Original Report |
1 Department of Medical Imaging and General Examination, National Taiwan
University Hospital, Taipei, Taiwan.
2 Department of Diagnostic Radiology, Shin Kong Wu Ho-Su Memorial Hospital,
Taipei, Taiwan, and Fu Jen Catholic University School of Medicine, Taipei,
Taiwan.
3 Department of Surgery, National Taiwan University Hospital, Taipei,
Taiwan.
4 Department of Pediatrics, National Taiwan University Hospital, Taipei,
Taiwan.
Received December 23, 2003;
accepted after revision July 1, 2004.
Address correspondence to H-Y Chen
(m004710{at}ms.skh.org.tw).
Abstract
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CONCLUSION. With advancements in central line procedures and corrective cardiac surgery, and the widespread use of noninvasive imaging techniques, the clinical importance of identification of the anomalous brachiocephalic vein is shown.
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Three major hypotheses attempt to account for the formation of an anomalous brachiocephalic vein. Adachi [6] has suggested double precardinal anastomoses, with regression of the upper resulting in an anomalous brachiocephalic vein. Minami et al. [7] consider that an anomalous brachiocephalic vein is formed secondarily as an alternative channel in patients when the normal course of the left brachiocephalic vein is obstructed. Kim et al. [8] have postulated that a precardinal anastomosis can be formed in any pathway where space is available after development of the aortic arch. The exact embryogenesis of this anomaly remains unknown, however.
In this article, we present the largest study, to our knowledge, of anomalous brachiocephalic vein CT findings with a sample of 30 patients. The patients were diagnosed at the time of workup for congenital heart disease before surgical correction and were treated during the preceding 8 years at our institution. After analysis of this evidence, we reconsidered the possible embryogenesis of the anomalous brachiocephalic vein. The potential clinical implications of this anomaly are also summarized.
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CT Protocol
All subjects underwent CT (ultrafast CT, C-150L, GE Healthcare), with ECG
gating, with all images acquired at the end-diastolic phase of the cardiac
cycle; slice thickness was 3 mm. CT scanned the lung and cardiac apices
without gaps. Table increment was 2 mm for infants to ensure slice overlap and
smooth continuity. The reconstructed matrix in one cross section was 512
x 512. The actual total imaging time, excluding positioning of the
patients, was less than 2 min. The calculated total radiation dose was
approximately 5-7 mSv [9].
Nonionic iodinated contrast medium (2-3 mL/kg; Ultravist 370 [iopromide],
Schering) was delivered by power injector with a variable flow rate (range,
0.4 mL/sec for neonates to 3 mL/sec for older children). Image acquisition was
delayed 20-25 sec from the start of contrast injection. Patients younger than
5 years were routinely sedated with chloral hydrate, 50 mg/kg, before imaging.
The small children usually sleep well because we routinely examine them in the
early morning, having asked their family to play with them until midnight the
evening before the study to reduce their scheduled sleep.
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Underlying cardiac problems in our sample, in descending order of prevalence, were tetralogy of Fallot (TOF; n = 23, 77%), right atrial isomerism (RAI; n = 4, 13%), atrial septal defect (ASD; n = 1, 3%), ventricular septal defect (VSD; n = 1, 3%), and double outlet of right ventricle (DORV; n = 1, 3%). In line with a previous report [2-4], a large proportion of our patients with an anomalous brachiocephalic vein had TOF; however, ours is the first study to show an association between this anomaly and RAI.
Associated Arch and Pulmonary Anomalies
Aortic arch anomalies were present in 22 patients (73%), with 21 of these
on the right side and one double aortic arch. The remaining eight subjects had
isolated left aortic arches. TOF with an anomalous brachiocephalic vein was
more prevalent with right arch (19/23; 83%). One right-sided arch was also
noted in our four RAI patients. Both our ASD and VSD patients involved a right
aortic arch. However, in the same study period, there were 275 and 1,507
patients without anomalous brachiocephalic veins who had right or left aortic
arches, respectively. Presence of a right-sided aortic arch was significantly
more common in patients with an anomalous brachiocephalic vein than in those
without (p < 0.0001).
Pulmonary trunk atresia was the most severe form of right ventricular outflow tract obstruction, appearing in nearly half (10/23; 43%) of our TOF patients and in half (2/4; 50%) of our RAI patients. Our TOF, RAI, and DORV patients who did not have pulmonary trunk atresia had infundibular pulmonary stenosis. In other words, 100% of our TOF, RAI, and DORV subjects had varying degrees of right ventricular outlet obstruction. The right ventricular outflow tract and central pulmonary artery in our ASD and VSD patients were grossly normal anatomically. During the same study period, however, there were 505 and 1,277 patients without anomalous brachiocephalic veins with or without (respectively) pulmonary atresia or stenosis. Pulmonary atresia or stenosis was significantly more common in patients with an anomalous brachiocephalic vein than in those without (p < 0.0001).
Patterns of Anomalous Brachiocephalic Veins
Pattern definitions are as described by Takada et al.
[5]. Most of our cases were
pattern b, which incorporated anomalous brachiocephalic veins crossing the
midline beneath the aortic arch, above the pulmonary artery, and in front of a
patent ductal arteriosus or ligamentum arteriosus. A number of reports have
detailed the salient features of CT images for this pattern
[5,
7,
8,
10-12].
Ten anomalous brachiocephalic vein subpatterns were recognized on the basis of
the relationship between the anomalous brachiocephalic vein and adjacent
vessel anomalies (Fig. 1). In
our study, these patterns were classified into left and right arch groups,
with the first subscript of the pattern name being a capital "L"
or "R." One female TOF patient with a double aortic arch was
classified as right arch because of its dominance, with the descending aorta
also located on the same side. Another arch anomaly involved a right ascending
aorta, with a left descending thoracic aorta occurring in one sinus
venosus-type ASD patient. This patient also had a right-sided arch but with an
unusual retroesophageal segment crossing the midline. Pattern bR,
the occurrence of an anomalous brachiocephalic vein in a right-sided arch, was
most prevalent (n = 16), accounting for 53% of our patients. Of
these, one was RAI, with the remainder being TOF (n = 15). The second
and third subscripts are abbreviations indicating other coexistent vessel
anomalies. Pattern bL bsvc and pattern bL lsvc (pattern
b in left-sided arch with bilateral and left-sided, respectively, superior
venae cavae) occurred only in RAI patients. The ASD patient was pattern
bR retro asc (pattern b with right-sided arch, retroesophageal
segment, and an aberrant left subclavian artery). The VSD patient was pattern
bR asc (pattern b with right-sided arch and an aberrant left
subclavian artery). The DORV patient was pattern bL (pattern b with
left-sided arch).
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One novel pattern was identified in this study, pattern a + b R asc. This was a hybrid of pattern a and pattern b with a right-sided arch and an aberrant left subclavian vein. Sharing the partial characters of both, pattern a + b R asc indicates the presence of a cephalocaudal connection between the upper and lower transverse channels [2-4, 11] of the bilateral anterior cardinal veins during fetal development, which to our knowledge has never before been reported (Fig. 2). Another anatomic structure was pattern cR (pattern c with right-sided aortic arch), with CT clearly showing the spatial relationship, the anomalous brachiocephalic vein crossing the midline behind the patent ductus arteriosus hump (Figs. 3A, and 3B). This characteristic has also never been reported by CT images to our knowledge.
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Association with Persistent Left Superior Vena Cava
An anomalous brachiocephalic vein was not associated with persistent left
superior vena cava in any of our situs solitus patients. This finding has also
been described without further explanation in another study
[11]. However, analysis of our
other situs solitus patients with no anomalous brachiocephalic vein in the
same period of the study showed that 20% (58/290) of TOF patients had a
persistent left superior vena cava. Furthermore, the presence of a persistent
left superior vena cava in the absence of an anomalous brachiocephalic vein
also occurred in 31% (21/67), 11% (12/107), and 7% (8/113) of our other DORV,
VSD, and ASD patients, respectively (Table
1). The presence of a persistent left superior vena cava was
significantly less common in situs solitus patients who had an anomalous
brachiocephalic vein than in those who did not (p < 0.05 comparing
TOF, DORV, VSD, and ASD subgroups). Our four RAI patients were not included in
the analysis because venous channels with visceral heterotaxy cannot be
reasonably compared with normal lateralization.
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Embryogenesis
The exact cause of an anomalous brachiocephalic vein remains unknown.
Previous reports have proposed the presence of two transverse channels
initially in the early embryo, one located superiorly and the other
inferiorly. Subsequently, the lower regresses and the upper becomes the normal
left brachiocephalic vein. The anomalous brachiocephalic vein is therefore
thought to reflect survival of the lower transverse anastomotic channel
[2-4,
11]. However, in the novel
pattern a + b R asc, a connection appears to exist between the two
channels. We suggest the presence of one venous plexus, with more than two
transverse channels extant before the eighth week of fetal development
[5]. This venous plexus should
have connections oriented along the cephalocaudal axis and various
ventral-dorsal planes (Fig.
4).
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Some researchers have postulated that this venous plexus may develop whenever reduced spatial hindrance is present because of the abnormal elongation of the aortic arch and an elevated [8] or right-sided [11] aortic arch. It may develop in varying degrees of right ventricular outflow tract underdevelopment, such as pulmonary trunk atresia [14]. We support this hypothesis because of the significantly greater numbers of right arch anomalies or underdevelopment of the central pulmonary artery, or both, in our sample.
In other words, the normal development of the great arteries (shortening of the arch and enlargement of the ascending aorta and pulmonary artery) interrupts and arrests further formation of the preexisting bridging vein in the course of their growth through direct pressure. Normally, the surrounding arterial systems are developed between the fourth and seventh weeks of fetal development, before further growth of this venous plexus from the eighth week. Thereafter, when the aortic arch shortens and the aortic and pulmonary arteries enlarge, their pressure on the inferior dorsal part causes regression, whereas the rest of the venous blood shunts into the superior ventral portion of the venous plexus. This situation facilitates normal development of the brachiocephalic vein [15]. In contrast, reduced shortening of the aortic arch (right-sided or high aortic arch) may compress and prevent the further development of the upper ventral portion of the venous plexus. This situation also results in a widening of the subaortic space [8]. Abnormal development of the pulmonary arteries (pulmonary atresia or pulmonary stenosis) encourages the sparing of the lower dorsal portion, possibly leading to formation of an anomalous brachiocephalic vein.
Persistence of the left common cardinal vein results in a persistent left superior vena cava [16]. Analysis of our data reveals that the latter was significantly less common in patients with an anomalous brachiocephalic vein than in those without. Thus, we suggest that this unusual nonoccurrence of an associated persistent left superior vena cava may be due to early arrest development of the the middle portion of the left common cardinal vein and formation of the ligament of Marshall. This event must be an important dependent factor for creation of the anomalous brachiocephalic vein to afford adequate drainage for the left upper part of the body. In other words, when the middle portion of the left common cardinal vein is obliterated and the usual transverse anastomosis fails to develop because of anatomic space restriction, survival forces creation of an alternative pathway within this venous plexus, eventually resulting in formation of an anomalous brachiocephalic vein [3].
We also determined from CT that the initial course for an anomalous brachiocephalic vein and persistent left superior vena cava is similar before they turn to the contralateral side. We propose that the anatomic development during embryogenesis of the anomalous brachiocephalic vein at its proximal part derives from the distal portion of the left common cardinal vein. This may explain the absence of a persistent left superior vena cava in our patients with an anomalous brachiocephalic vein because these two vessels compete for this segment of their own channel.
In summary, we suggest that three major components are precursors to the formation of an anomalous brachiocephalic vein during fetal development. Initially, a venous plexus forms between the bilateral anterior and common cardinal veins around the primitive aortic arch-pulmonary system that is ready to develop. Second, early arrest of the middle common cardinal vein forces the returned venous blood to run absolutely in a supracardiac direction. Third, the venous return finds the path of least resistance, governed by compression of the surrounding systemic and pulmonary arteries. In an anomalous brachiocephalic vein, the third component inhibits growth of the cephalic ventral portion of the venous plexus, which causes arch anomalies and preservation of the caudal dorsal portion through underdevelopment of the central pulmonary artery.
Clinical Implications
To the radiologist, the descending portion of an anomalous brachiocephalic
vein must be differentiated from a persistent left superior vena cava
[5], an ascending vertical vein
in a total anomalous pulmonary venous connection
[3,
7,
14], and a left partial
anomalous pulmonary venous return. The middle portion needs to be
differentiated from the central pulmonary artery
[3,
7,
14]. The retroaortic crossing
segment of the anomalous brachiocephalic vein may be misinterpreted on
unenhanced CT as an enlarged lymph node
[11], an elevated right
pulmonary artery in patients with hypoplastic or atretic central pulmonary
arteries, or an early branching right upper lobe pulmonary artery on
cross-sectional echocardiography
[2,
4,
5]. Carefully tracing this
vascular channel through sequential images is the key to differentiation.
Although our data were based on ultrafast CT findings, the newly developed
MDCT is more widely available and capable of being used to differentiate these
abnormalities.
For cardiologists performing transvenous pacemaker insertion, and clinicians and anesthesiologists who insert a central venuos pressure line and Port-A-Cath system (Pharmacia, Germany) implantation, the anomalous brachiocephalic vein may cause technical difficulty in a left-arm approach.
If the surgeon has not been informed of the presence of the anomalous brachiocephalic vein before surgery, it might mistakenly be concluded, on initial exploration through a median sternotomy, that the left brachiocephalic vein is absent. In a cardiopulmonary bypass, this would suggest the presence of a persistent left superior vena cava, which carries implications for establishment of adequate alternative venous drainage [5].
When the surgeon has been informed of the presence of the anomalous brachiocephalic vein before surgery, cannulation of the superior vena cava must be performed with extreme care to avoid obstruction of the anomalous vein because it enters the superior vena cava deeper and more caudally than usual [5]. When creating systemic vein-to-pulmonary artery anastomoses, the presence of this anomaly may also complicate exposure of the pulmonary arteries. Finally, an anomalous brachiocephalic vein may obscure the surgical field in the construction of a subclavian-to-pulmonary arterial shunt [3, 17] and the ligation of a patent artery duct [3, 5, 18]. It can also be confused with the pulmonary artery during reconstruction of the right ventricular outlet and angioplasty of bilateral central pulmonary arteries.
With advancements in central line procedures and corrective cardiac surgery, and the prevalence of intrasurgical cardiopulmonary bypass, the role of the anomalous brachiocephalic vein may increase. Moreover, because current noninvasive imaging techniques are widespread and reliable, we suggest that the preoperative diagnosis of this anomaly is important when any cardio-vascular intervention is to be performed.
Acknowledgments
We thank Ritta Huang for her assistance in preparing this manuscript.
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