Accepted Manuscript Retro-Esophageal Brachiocephalic Artery Assessed by MRI: A Case Report and Literature Review Sharmila Udupa, MD, CM John F. Smythe, MD, FRCPC Derek T. Wong, MD. FRCPC PII:
S0828-282X(14)01400-7
DOI:
10.1016/j.cjca.2014.09.016
Reference:
CJCA 1406
To appear in:
Canadian Journal of Cardiology
Received Date: 4 August 2014 Revised Date:
4 September 2014
Accepted Date: 5 September 2014
Please cite this article as: Udupa S, Smythe JF, Wong DT, Retro-Esophageal Brachiocephalic Artery Assessed by MRI: A Case Report and Literature Review, Canadian Journal of Cardiology (2014), doi: 10.1016/j.cjca.2014.09.016. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Udupa 1
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Retro-Esophageal Brachiocephalic Artery Assessed by MRI: A Case Report and Literature Review Short Title: Retro-Esophageal Brachiocephalic Artery – Literature Review
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Sharmila Udupa MD,CM1, John F Smythe MD, FRCPC2, Derek T Wong MD. FRCPC1
1
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Division of Cardiology, Department of Pediatrics, University of Ottawa, Children’s Hospital of Eastern Ontario, Ottawa, Canada.
2
Divison of Cardiology, Department of Pediatrics, Queen’s University, Kingston General Hospital, Kingston, Canada.
Corresponding Author:
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Word Count: 1686
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Sharmila Udupa, MD,CM Division of Cardiology, Department of Pediatrics Children’s Hospital of Eastern Ontario 401 Smyth Road Ottawa, Ontario Canada K1H 8L1 E-mail: [email protected] Telephone: (613) 737-7600 ext 2390 Fax: (613) 738-4835
ACCEPTED MANUSCRIPT Udupa 2 Brief Summary
A right aortic arch with a retro-esophageal brachiocephalic artery is a very rare type of
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vascular ring. We present a case of one such vascular anomaly diagnosed by cardiac magnetic resonance imaging (MRI), with a review of all cases to date. Cardiac MRI can be used as a primary diagnostic modality for anatomic assessment of the vascular ring,
SC
as well as the hemodynamics of associated cardiac malformations in the pre-operative
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EP
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setting.
ACCEPTED MANUSCRIPT Udupa 3 Abstract
A right aortic arch with a retro-esophageal brachiocephalic artery is a very rare type of
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vascular ring. A case report with a review of published cases to date are presented. Twelve publications from 1968 to 2014 describe a retro-esophageal brachiocephalic artery in a total of thirteen patients. The mean age at diagnosis was 8.7 ± 16 years.
SC
Four of the thirteen patients were male. Nearly half of the patients were symptomatic, with dysphagia or respiratory difficulties. Ten patients (77%) had associated congenital
M AN U
heart defects. Of the thirteen patients with a retro-esophageal brachiocephalic artery, twelve had a right aortic arch, and only one patient had a left aortic arch associated with complex congenital heart disease.
Investigations used in the diagnosis of the vascular ring include angiography,
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esophagram, echocardiogram, and computed tomography. Only two cases confirmed the diagnosis with magnetic resonance imaging but this was in the setting of complex congenital heart disease.
EP
In conclusion, a right aortic arch with a retro-esophageal left brachiocephalic artery is an extremely rare form of vascular ring, often seen in association with other forms of
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congenital heart disease. Cardiac MRI can be used as a primary diagnostic modality for both the assessment of the vascular ring anatomy and the hemodynamics of associated cardiac malformations in the pre-operative setting.
ACCEPTED MANUSCRIPT Udupa 4 Introduction
In general, vascular rings are a rare cardiac anomaly, however a right aortic arch with a
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left retro-esophageal brachiocephalic artery is one of the rarest subtypes. Only a few cases have been described in the literature, with minimal documentation of their age, mode of presentation and association with other forms of congenital heart disease. We
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resonance imaging, with a review of all cases to date.
SC
present a case of one such vascular anomaly diagnosed by cardiac magnetic
Case
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A six-month old boy was referred to our center with a diagnosis of a perimembranous ventricular septal defect (VSD) and unclear aortic arch anatomy. He had initially been assessed for a murmur in a peripheral center while hospitalized for a respiratory tract
EP
illness.
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Upon presentation to our center, there was no history of chronic respiratory or gastrointestinal difficulties such as stridor, dysphagia or gastroesophageal reflux. Physical examination revealed a normal blood pressure in all four limbs with no evidence of an arm-leg gradient. Auscultation demonstrated a grade 3/6 pansystolic murmur. Electrocardiogram revealed sinus rhythm and biventricular hypertrophy. Echocardiography confirmed a moderate perimembranous VSD with evidence of left-
ACCEPTED MANUSCRIPT Udupa 5 sided volume loading. There was evidence of right coronary cusp prolapse into the VSD, without aortic insufficiency. Echocardiography at our institution failed to clearly delineate the aortic arch anatomy, prompting further evaluation with cardiac magnetic
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resonance imaging (MRI).
An outpatient cardiac MRI under general anesthetic revealed a right aortic arch with an
SC
aberrant left retro-esophageal brachiocephalic artery (Figure 1). The first branch arising from the right aortic arch was the right internal carotid artery, followed by the right
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subclavian artery. The last branch off the descending aorta was the left brachiocephalic artery which gave rise to the left internal carotid and subclavian arteries and had a retroesophageal course. In addition, the proximal base of the brachiocephalic artery appeared prominent, reminiscent of a diverticulum of Kommerrell. This finding
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supported the notion that the arterial duct originated from the brachiocephalic artery and coursed towards the pulmonary trunk, thereby completing the vascular ring. There was no evidence of tracheal compression. MRI also confirmed the hemodynamic
EP
significance of the VSD, with a Qp:Qs ratio of 2.9:1 by phase contrast imaging.
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Surgery was performed electively, and the aortic arch anatomy was confirmed at the time of surgery – a right aortic arch with a retro-esophageal left brachiocephalic artery and a left-sided arterial ligament connecting the left subclavian artery to the left pulmonary artery, effectively completing the vascular ring. The VSD was closed and the arterial ligament was divided without complications.
ACCEPTED MANUSCRIPT Udupa 6
Literature Survey
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There have been a total of twelve publications from 1968 to 2014 describing a retroesophageal brachiocephalic artery in a total of thirteen patients (Table 1). The mean age of diagnosis was 8.7 ± 16 years (median 1 year, range 0.002 – 61 years). Four of
SC
the thirteen (30%) cases were male.
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Nearly half of patients (46%) were symptomatic, with dysphagia or respiratory difficulties attributable to the vascular ring. Symptomatic individuals had an average age of presentation of 15.8 ± 20.7 years (median 9 years, range 0.1 – 61 years). Some of these patients had associated congenital heart disease, however, it was felt that their
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primary symptoms at presentation were due to the vascular ring.
Ten of the thirteen patients (77%) had associated congenital heart defects ranging from
EP
isolated VSD in two (15%), common arterial trunk in two (15%), Tetralogy of Fallot in one (7.5%), aortopulmonary window in one (7.5%), valvular aortic stenosis in one
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(7.5%) and hypoplastic left heart complex in one (7.5%). The average age of presentation for those with associated congenital heart disease was 3.5 ± 6.2 years (median 0.375 years, range 0.002 – 19 years).
Of the thirteen patients with a retro-esophageal brachiocephalic artery, twelve had a right aortic arch, and only one patient had a left aortic arch in the setting of complex
ACCEPTED MANUSCRIPT Udupa 7 congenital heart disease. The strong association of right aortic arch and a retroesophageal brachiocephalic artery gives credence to the belief that its pathogenesis may be related to abnormalities in outflow tract formation. In addition, the incidence of
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associated congenital conotruncal lesions (30% of patients with Tetralogy of Fallot, common arterial trunk, or aortopulmonary window) with a retro-esophageal
brachiocephalic artery in our review helps to further support this hypothesis. Only four
SC
of thirteen cases in the literature were isolated vascular rings, highlighting the
when presented with such a lesion.
M AN U
importance of a thorough cardiac assessment to rule out other congenital heart defects
Surgical intervention, consisting of ductal division, was linked to cases in which symptoms were present or where complex cardiac disease co-existed. Only three out of
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thirteen cases document no surgical intervention, likely due to the lack of associated
Discussion
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symptoms.
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The development of various forms of vascular rings can be best understood through the hypothetical pluripotent double aortic arch model proposed by Jesse Edwards in 1948 (Figure 2) (1). This hypothetical model consists of a double aortic arch with an arterial duct on either side and the various head and neck vessels arising from their respective arches. Embryologically, this model is based on the paired arteries seen within the five pharyngeal arches that originate from the aortic sac and travel posteriorly to join with
ACCEPTED MANUSCRIPT Udupa 8 the dorsal aorta (2). The various configurations of aortic arch anatomy can be explained through persistence or regression of the various portions of this primitive aortic arch substrate. The reader is directed to excellent reviews of cardiac embryology for further
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detailed explanations. (2-5).
The formation of a right aortic arch with an aberrant left retro-esophageal
SC
brachiocephalic artery is postulated to occur due to an interruption in the anterior portion of the left branch of the aortic sac, proximal to the origin of the left common carotid
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artery (1). The right aortic arch is formed by persistence of the right branch of the aortic sac, the right aortic arch, and the right dorsal aorta. The left dorsal aorta persists and connects to the distal portion of the left aortic arch, forming the retro-esophageal brachiocephalic artery. Completion of the vascular ring occurs when a left sided arterial
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duct or arterial ligament connects the aberrant left retro-esophageal brachiocephalic artery to a pulmonary artery. This type of vascular ring is a rare entity, with very few other cases described in the literature. A recent review of vascular rings at a single
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institution listed an incidence of 3% of patients with this specific type of vascular ring (6).
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Past reports have documented the use of angiography to diagnose a right aortic arch with aberrant left retro-esophageal brachiocephalic artery. Other diagnostic investigations include esophagram, echocardiogram, and until recently, computed tomography. Only two cases confirmed the diagnosis with MRI but this was in the setting of complex congenital heart disease. Following the use of MRI in confirming their
ACCEPTED MANUSCRIPT Udupa 9 diagnosis, Moes et al concluded that MRI was their preferred tool for assessing vascular rings (7).
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Cardiac MRI has recently been described as the new gold standard for evaluation of vascular rings (6), with significant benefit of vascular and extra-cardiac anatomical delineation. Cardiac MRI allows for detailed anatomic imaging of the aortic arch with
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high spatial resolution. In addition, it allows for multi-planar reconstruction and creation of a 3-dimensional picture (Video 1) permitting clear visualization of the impact of the
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vascular ring on adjacent structures. Furthermore, cardiac MRI does not use ionizing radiation (unlike cardiac catheterization or CT) and is not limited by acoustic windows. In our case, echocardiography was unable to resolve the aortic arch anatomy. All other case reports have only utilized cardiac MRI for a purely anatomic diagnosis, thereby not
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fully benefitting from its potential. Given that this anomaly is often associated with other forms of congenital heart disease, MRI can also provide hemodynamic data and precise anatomical assessment of associated lesions, imperative in surgical management of
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these patients. In our case, cardiac MRI determined pulmonary-to-systemic blood flow
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ratio, illustrating the hemodynamic significance of the VSD and necessity for its closure.
Conclusion
A retro-esophageal left brachiocephalic artery with right aortic arch is an extremely rare form of vascular ring, with very few cases reported in the literature. This variant of a
ACCEPTED MANUSCRIPT Udupa 10 vascular ring is often seen in association with other forms of congenital heart disease, specifically those related to abnormalities of the outflow tracts. Our case illustrates how cardiac MRI can be used as a primary diagnostic modality for both the assessment of
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vascular ring anatomy and the hemodynamics of associated cardiac malformations in the pre-operative setting.
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Acknowledgements
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None.
Funding Sources None.
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Disclosures
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None.
ACCEPTED MANUSCRIPT Udupa 11 Reference List (1) EDWARDS JE. Anomalies of the derivatives of the aortic arch system. Med Clin North Am 1948 July;32:925-49.
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(2) Anderson RH, Webb S, Brown NA, Lamers W, Moorman A. Development of the heart: (3) formation of the ventricular outflow tracts, arterial valves, and intrapericardial arterial trunks. Heart 2003 September;89(9):1110-8. (3) Anderson RH, Brown NA, Mohun TJ, Moorman AF. Insights from cardiac development relevant to congenital defects and adult clinical anatomy. J Cardiovasc Transl Res 2013 April;6(2):107-17.
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(4) Anderson RH, Webb S, Brown NA, Lamers W, Moorman A. Development of the heart: (2) Septation of the atriums and ventricles. Heart 2003 August;89(8):949-58.
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(5) Moorman A, Webb S, Brown NA, Lamers W, Anderson RH. Development of the heart: (1) formation of the cardiac chambers and arterial trunks. Heart 2003 July;89(7):806-14. (6) Humphrey C, Duncan K, Fletcher S. Decade of experience with vascular rings at a single institution. Pediatrics 2006 May;117(5):e903-e908. (7) Moes CA, Mawson JB, MacDonald C, Smallhorn J. Right aortic arch with retroesophageal left aberrant innominate artery. Pediatr Cardiol 1996 November;17(6):402-6.
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(8) Grollman JH, Jr., Bedynek JL, Henderson HS, Hall RJ. Right aortic arch with an aberrant retroesophageal innominate artery: angiographic diagnosis. Radiology 1968 April;90(4):782-3. (9) Garti IJ, Aygen MM. Right aortic arch with aberrant left innominate artery. Pediatr Radiol 1979 February 26;8(1):48-50.
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(10) Rajaram PC, Hussain AT, Lakshmikanthan C, Vaidyanathan D, Subramanian N, Vasudevan S. Type D double aortic arch. Double aortic arch with interruption of its left component proximal to the site of origin of left common carotid artery. Angiology 1983 September;34(9):597-603.
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(11) Schlesinger AE, Leiter BE, Connors SK. Computed tomography diagnosis of right aortic arch with an aberrant left innominate artery. J Comput Tomogr 1984 January;8(1):81-7. (12) Maurus KE, Firmin RK, Leanage R. A rare anomaly of the aortic arch complex. Int J Cardiol 1988 July;20(1):149-51. (13) Nakajima Y, Satomi G, Kawamura T, Nishibatake M, Nakazawa M, Takao A. Right aortic arch with aberrant retroesophageal innominate artery: a report of 2 cases and review of the literature. Int J Cardiol 1993 March;38(3):247-51. (14) Ishizaka T, Allen SW, Strouse PJ, Ohye RG. Postductal origin of the left carotid, left subclavian, and aberrant retroesophageal right innominate arteries in truncus arteriosus with interrupted aortic arch. Pediatr Cardiol 2003 November;24(6):581-4. (15) Sett SS, Mawson JB, Sandor GG. Repair in infancy of right aortic arch with aberrant left brachiocephalic artery in the setting of a variant of the hypoplastic left heart syndrome. Cardiol Young 2004 August;14(4):441-3.
ACCEPTED MANUSCRIPT Udupa 12 (16) Rios-Mendez RE, rauz-Martinez ME. [Chronic wheezing child and type "D" double aortic arch: case report]. Arch Argent Pediatr 2008 December;106(6):548-51. (17) Fellmer PT, Bohner H, Wolf A, Roher HD, Goretzki PE. A left nonrecurrent inferior laryngeal nerve in a patient with right-sided aorta, truncus arteriosus communis, and an aberrant left innominate artery. Thyroid 2008 June;18(6):647-9.
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(18) Kondrachuk O, Yalynska T, Yemets I. Right aortic arch with retroesophageal brachiocephalic artery. Cardiol Young 2009 June;19(3):292-3.
ACCEPTED MANUSCRIPT
Udupa 13 Table 1: Summary of literature involving patients with a retro-esophageal brachiocephalic artery Year
n
Age
Symptoms
Modality for Diagnosis
Grollman et al.(8;8)
1968
1
19 yrs
Dyspnea on exertion
Esophagram and Arteriogram
Right
Garti et al.(9)
1979
1
9 yrs
Dysphagia and recurrent URTI
Esophagram and Arteriogram
Right
Rajaram et al. (10)
1983
1
5 yrs
Recurrent URTI
Angiogram
Right
Schlesinger et al (11)
1984
1
61 yrs
CT
Right
Maurus et al (12)
1988
1
6 mos
None incidental on CXR Heart failure
Angiogram
Nakajima et al (13)
1993
2
1 yr
1
5 wks
Ishizaka et al. (14)
2003
1
1 day
Cyanosis
Sett et al. (15)
2004
1
5 wks
Cyanosis and failure to thrive
Rios-Mendez et al. (16)
2008
1
8 yrs
Dyspnea and dysphagia
Fellmer et al. (17)
2008
1
1 day
Cyanosis
Kondrachuk et al. (18)
2009
1
3 mo
Dysphagia and dyspnea
Valvular aortic stenosis
None
None
PDA and bilateral pulmonary artery stenosis
Arterial Ligament Division PDA ligation
VSD and PDA
Right
Tetralogy of Fallot
PDA Ligation, and VSD closure Tetralogy of Fallot repair
Right
VSD
None
Angiogram
Right
ASD, PSD, aortopulmonary window and PDA
Complete repair
Echocardiogram and MRI
Left
Common Arterial Trunk (type II), single coronary artery, aortic arch interruption
Complete repair
CT
Right
Severe mitral stenosis, large VSD, bicuspid aortic valve, arch hypoplasia, left superior vena cava
Norwood procedure
Esophagram and Arteriogram
Right
None
PDA ligation
Angiogram
Right
Common Arterial Trunk (Type I)
Complete repair
CT
Right
PDA
PDA ligation
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Right
Angiogram and MRI
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1996
Intervention
None
Angiogram
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Moes et al (7)
Associated CHD
None
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9 yr
None incidental on CXR None incidental on investigation for murmur Stridor and URTI
Aortic Arch Sidedness
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Authors
Legend: CT: computer assisted tomography, CXR: chest radiograph, MRI: magnetic resonance imaging, VSD: ventricular septal defect, PDA: patent arterial duct, ASD: atrial septal defect, URTI: upper respiratory tract infection
ACCEPTED MANUSCRIPT Udupa 14 Figure 1 Legend 3D volume rendered magnetic resonance angiogram of a right aortic arch with an aberrant left retroesophageal brachiocephalic artery. Note the prominent base of the brachiocephalic artery,
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reminiscent of a diverticulum of Kommerrell, indicating that the arterial duct originated from the brachiocephalic artery to connect to the pulmonary trunk, thereby completing the vascular ring. The dotted line represents the location of the arterial ligament.
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AAO: Ascending aorta; REBA: retro-esophageal brachiocephalic artery; PT: pulmonary trunk; DOA:
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descending aorta.
Figure 2 Legend
A. The hypothetical model for the double aortic arch proposed by JE Edwards. LAA: left aortic arch; LCCA: left common carotid artery; LPA: left pulmonary artery; LSA: left subclavian artery; PT:
RSA: right subclavian artery.
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pulmonary trunk; RAA: right aortic arch; RCCA: right common carotid; RPA: right pulmonary artery;
B. Formation of a right aortic arch with an aberrant left retro-esophageal brachiocephalic artery is
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postulated to occur due to an interruption in the anterior portion of the left branch of the aortic sac, proximal to the origin of the left common carotid artery. The right aortic arch is formed by persistence
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of the right branch of the aortic sac, the right aortic arch, and the right dorsal aorta. The left dorsal aorta persists and connects to the distal portion of the left aortic arch, forming the brachiocephalic artery. Completion of the vascular ring occurs when a left sided arterial duct or arterial ligament connects the aberrant left retro-esophageal brachiocephalic artery to a pulmonary artery. The red lines indicate areas of regression. [Reprinted from Paediatric Cardiology, 3rd Edition, Anderson RH, Baker EJ, Penny DJ, Redington AN, Rigby ML, Wernovsky G [eds], “Vascular Rings, Pulmonary Arterial Sling, and Related Conditions”, Yoo S-J and Bradley TJ, pp967-989, with permission from Elsevier; originally modified from Edwards
ACCEPTED MANUSCRIPT Udupa 15 JE: Anomalies of the derivatives of the aortic arch system. Med Clin N Am 1948;32:925–948; and Edwards JE: Vascular rings and slings. in Moller JH, Neal AN [eds]: Fetal, Neonatal, and Infant
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Cardiac disease. Norwalk, CT: Appleton & Lange, 1990, pp 745–754.].
Video Legend
3D volume rendered magnetic resonance angiogram of a right aortic arch with an aberrant left retro-
SC
esophageal brachiocephalic artery. The prominent base of the brachiocephalic artery, reminiscent of a diverticulum of Kommerrell, indicates that the arterial duct originated from the brachiocephalic artery
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to connect to the pulmonary trunk.
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EP
TE D
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SC
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ACCEPTED MANUSCRIPT
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ACCEPTED MANUSCRIPT
S0828-282X(14)01400-7
DOI:
10.1016/j.cjca.2014.09.016
Reference:
CJCA 1406
To appear in:
Canadian Journal of Cardiology
Received Date: 4 August 2014 Revised Date:
4 September 2014
Accepted Date: 5 September 2014
Please cite this article as: Udupa S, Smythe JF, Wong DT, Retro-Esophageal Brachiocephalic Artery Assessed by MRI: A Case Report and Literature Review, Canadian Journal of Cardiology (2014), doi: 10.1016/j.cjca.2014.09.016. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Udupa 1
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Retro-Esophageal Brachiocephalic Artery Assessed by MRI: A Case Report and Literature Review Short Title: Retro-Esophageal Brachiocephalic Artery – Literature Review
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Sharmila Udupa MD,CM1, John F Smythe MD, FRCPC2, Derek T Wong MD. FRCPC1
1
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Division of Cardiology, Department of Pediatrics, University of Ottawa, Children’s Hospital of Eastern Ontario, Ottawa, Canada.
2
Divison of Cardiology, Department of Pediatrics, Queen’s University, Kingston General Hospital, Kingston, Canada.
Corresponding Author:
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Word Count: 1686
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Sharmila Udupa, MD,CM Division of Cardiology, Department of Pediatrics Children’s Hospital of Eastern Ontario 401 Smyth Road Ottawa, Ontario Canada K1H 8L1 E-mail: [email protected] Telephone: (613) 737-7600 ext 2390 Fax: (613) 738-4835
ACCEPTED MANUSCRIPT Udupa 2 Brief Summary
A right aortic arch with a retro-esophageal brachiocephalic artery is a very rare type of
RI PT
vascular ring. We present a case of one such vascular anomaly diagnosed by cardiac magnetic resonance imaging (MRI), with a review of all cases to date. Cardiac MRI can be used as a primary diagnostic modality for anatomic assessment of the vascular ring,
SC
as well as the hemodynamics of associated cardiac malformations in the pre-operative
AC C
EP
TE D
M AN U
setting.
ACCEPTED MANUSCRIPT Udupa 3 Abstract
A right aortic arch with a retro-esophageal brachiocephalic artery is a very rare type of
RI PT
vascular ring. A case report with a review of published cases to date are presented. Twelve publications from 1968 to 2014 describe a retro-esophageal brachiocephalic artery in a total of thirteen patients. The mean age at diagnosis was 8.7 ± 16 years.
SC
Four of the thirteen patients were male. Nearly half of the patients were symptomatic, with dysphagia or respiratory difficulties. Ten patients (77%) had associated congenital
M AN U
heart defects. Of the thirteen patients with a retro-esophageal brachiocephalic artery, twelve had a right aortic arch, and only one patient had a left aortic arch associated with complex congenital heart disease.
Investigations used in the diagnosis of the vascular ring include angiography,
TE D
esophagram, echocardiogram, and computed tomography. Only two cases confirmed the diagnosis with magnetic resonance imaging but this was in the setting of complex congenital heart disease.
EP
In conclusion, a right aortic arch with a retro-esophageal left brachiocephalic artery is an extremely rare form of vascular ring, often seen in association with other forms of
AC C
congenital heart disease. Cardiac MRI can be used as a primary diagnostic modality for both the assessment of the vascular ring anatomy and the hemodynamics of associated cardiac malformations in the pre-operative setting.
ACCEPTED MANUSCRIPT Udupa 4 Introduction
In general, vascular rings are a rare cardiac anomaly, however a right aortic arch with a
RI PT
left retro-esophageal brachiocephalic artery is one of the rarest subtypes. Only a few cases have been described in the literature, with minimal documentation of their age, mode of presentation and association with other forms of congenital heart disease. We
M AN U
resonance imaging, with a review of all cases to date.
SC
present a case of one such vascular anomaly diagnosed by cardiac magnetic
Case
TE D
A six-month old boy was referred to our center with a diagnosis of a perimembranous ventricular septal defect (VSD) and unclear aortic arch anatomy. He had initially been assessed for a murmur in a peripheral center while hospitalized for a respiratory tract
EP
illness.
AC C
Upon presentation to our center, there was no history of chronic respiratory or gastrointestinal difficulties such as stridor, dysphagia or gastroesophageal reflux. Physical examination revealed a normal blood pressure in all four limbs with no evidence of an arm-leg gradient. Auscultation demonstrated a grade 3/6 pansystolic murmur. Electrocardiogram revealed sinus rhythm and biventricular hypertrophy. Echocardiography confirmed a moderate perimembranous VSD with evidence of left-
ACCEPTED MANUSCRIPT Udupa 5 sided volume loading. There was evidence of right coronary cusp prolapse into the VSD, without aortic insufficiency. Echocardiography at our institution failed to clearly delineate the aortic arch anatomy, prompting further evaluation with cardiac magnetic
RI PT
resonance imaging (MRI).
An outpatient cardiac MRI under general anesthetic revealed a right aortic arch with an
SC
aberrant left retro-esophageal brachiocephalic artery (Figure 1). The first branch arising from the right aortic arch was the right internal carotid artery, followed by the right
M AN U
subclavian artery. The last branch off the descending aorta was the left brachiocephalic artery which gave rise to the left internal carotid and subclavian arteries and had a retroesophageal course. In addition, the proximal base of the brachiocephalic artery appeared prominent, reminiscent of a diverticulum of Kommerrell. This finding
TE D
supported the notion that the arterial duct originated from the brachiocephalic artery and coursed towards the pulmonary trunk, thereby completing the vascular ring. There was no evidence of tracheal compression. MRI also confirmed the hemodynamic
EP
significance of the VSD, with a Qp:Qs ratio of 2.9:1 by phase contrast imaging.
AC C
Surgery was performed electively, and the aortic arch anatomy was confirmed at the time of surgery – a right aortic arch with a retro-esophageal left brachiocephalic artery and a left-sided arterial ligament connecting the left subclavian artery to the left pulmonary artery, effectively completing the vascular ring. The VSD was closed and the arterial ligament was divided without complications.
ACCEPTED MANUSCRIPT Udupa 6
Literature Survey
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There have been a total of twelve publications from 1968 to 2014 describing a retroesophageal brachiocephalic artery in a total of thirteen patients (Table 1). The mean age of diagnosis was 8.7 ± 16 years (median 1 year, range 0.002 – 61 years). Four of
SC
the thirteen (30%) cases were male.
M AN U
Nearly half of patients (46%) were symptomatic, with dysphagia or respiratory difficulties attributable to the vascular ring. Symptomatic individuals had an average age of presentation of 15.8 ± 20.7 years (median 9 years, range 0.1 – 61 years). Some of these patients had associated congenital heart disease, however, it was felt that their
TE D
primary symptoms at presentation were due to the vascular ring.
Ten of the thirteen patients (77%) had associated congenital heart defects ranging from
EP
isolated VSD in two (15%), common arterial trunk in two (15%), Tetralogy of Fallot in one (7.5%), aortopulmonary window in one (7.5%), valvular aortic stenosis in one
AC C
(7.5%) and hypoplastic left heart complex in one (7.5%). The average age of presentation for those with associated congenital heart disease was 3.5 ± 6.2 years (median 0.375 years, range 0.002 – 19 years).
Of the thirteen patients with a retro-esophageal brachiocephalic artery, twelve had a right aortic arch, and only one patient had a left aortic arch in the setting of complex
ACCEPTED MANUSCRIPT Udupa 7 congenital heart disease. The strong association of right aortic arch and a retroesophageal brachiocephalic artery gives credence to the belief that its pathogenesis may be related to abnormalities in outflow tract formation. In addition, the incidence of
RI PT
associated congenital conotruncal lesions (30% of patients with Tetralogy of Fallot, common arterial trunk, or aortopulmonary window) with a retro-esophageal
brachiocephalic artery in our review helps to further support this hypothesis. Only four
SC
of thirteen cases in the literature were isolated vascular rings, highlighting the
when presented with such a lesion.
M AN U
importance of a thorough cardiac assessment to rule out other congenital heart defects
Surgical intervention, consisting of ductal division, was linked to cases in which symptoms were present or where complex cardiac disease co-existed. Only three out of
TE D
thirteen cases document no surgical intervention, likely due to the lack of associated
Discussion
EP
symptoms.
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The development of various forms of vascular rings can be best understood through the hypothetical pluripotent double aortic arch model proposed by Jesse Edwards in 1948 (Figure 2) (1). This hypothetical model consists of a double aortic arch with an arterial duct on either side and the various head and neck vessels arising from their respective arches. Embryologically, this model is based on the paired arteries seen within the five pharyngeal arches that originate from the aortic sac and travel posteriorly to join with
ACCEPTED MANUSCRIPT Udupa 8 the dorsal aorta (2). The various configurations of aortic arch anatomy can be explained through persistence or regression of the various portions of this primitive aortic arch substrate. The reader is directed to excellent reviews of cardiac embryology for further
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detailed explanations. (2-5).
The formation of a right aortic arch with an aberrant left retro-esophageal
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brachiocephalic artery is postulated to occur due to an interruption in the anterior portion of the left branch of the aortic sac, proximal to the origin of the left common carotid
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artery (1). The right aortic arch is formed by persistence of the right branch of the aortic sac, the right aortic arch, and the right dorsal aorta. The left dorsal aorta persists and connects to the distal portion of the left aortic arch, forming the retro-esophageal brachiocephalic artery. Completion of the vascular ring occurs when a left sided arterial
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duct or arterial ligament connects the aberrant left retro-esophageal brachiocephalic artery to a pulmonary artery. This type of vascular ring is a rare entity, with very few other cases described in the literature. A recent review of vascular rings at a single
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institution listed an incidence of 3% of patients with this specific type of vascular ring (6).
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Past reports have documented the use of angiography to diagnose a right aortic arch with aberrant left retro-esophageal brachiocephalic artery. Other diagnostic investigations include esophagram, echocardiogram, and until recently, computed tomography. Only two cases confirmed the diagnosis with MRI but this was in the setting of complex congenital heart disease. Following the use of MRI in confirming their
ACCEPTED MANUSCRIPT Udupa 9 diagnosis, Moes et al concluded that MRI was their preferred tool for assessing vascular rings (7).
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Cardiac MRI has recently been described as the new gold standard for evaluation of vascular rings (6), with significant benefit of vascular and extra-cardiac anatomical delineation. Cardiac MRI allows for detailed anatomic imaging of the aortic arch with
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high spatial resolution. In addition, it allows for multi-planar reconstruction and creation of a 3-dimensional picture (Video 1) permitting clear visualization of the impact of the
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vascular ring on adjacent structures. Furthermore, cardiac MRI does not use ionizing radiation (unlike cardiac catheterization or CT) and is not limited by acoustic windows. In our case, echocardiography was unable to resolve the aortic arch anatomy. All other case reports have only utilized cardiac MRI for a purely anatomic diagnosis, thereby not
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fully benefitting from its potential. Given that this anomaly is often associated with other forms of congenital heart disease, MRI can also provide hemodynamic data and precise anatomical assessment of associated lesions, imperative in surgical management of
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these patients. In our case, cardiac MRI determined pulmonary-to-systemic blood flow
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ratio, illustrating the hemodynamic significance of the VSD and necessity for its closure.
Conclusion
A retro-esophageal left brachiocephalic artery with right aortic arch is an extremely rare form of vascular ring, with very few cases reported in the literature. This variant of a
ACCEPTED MANUSCRIPT Udupa 10 vascular ring is often seen in association with other forms of congenital heart disease, specifically those related to abnormalities of the outflow tracts. Our case illustrates how cardiac MRI can be used as a primary diagnostic modality for both the assessment of
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vascular ring anatomy and the hemodynamics of associated cardiac malformations in the pre-operative setting.
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Acknowledgements
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None.
Funding Sources None.
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Disclosures
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None.
ACCEPTED MANUSCRIPT Udupa 11 Reference List (1) EDWARDS JE. Anomalies of the derivatives of the aortic arch system. Med Clin North Am 1948 July;32:925-49.
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(2) Anderson RH, Webb S, Brown NA, Lamers W, Moorman A. Development of the heart: (3) formation of the ventricular outflow tracts, arterial valves, and intrapericardial arterial trunks. Heart 2003 September;89(9):1110-8. (3) Anderson RH, Brown NA, Mohun TJ, Moorman AF. Insights from cardiac development relevant to congenital defects and adult clinical anatomy. J Cardiovasc Transl Res 2013 April;6(2):107-17.
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(4) Anderson RH, Webb S, Brown NA, Lamers W, Moorman A. Development of the heart: (2) Septation of the atriums and ventricles. Heart 2003 August;89(8):949-58.
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(5) Moorman A, Webb S, Brown NA, Lamers W, Anderson RH. Development of the heart: (1) formation of the cardiac chambers and arterial trunks. Heart 2003 July;89(7):806-14. (6) Humphrey C, Duncan K, Fletcher S. Decade of experience with vascular rings at a single institution. Pediatrics 2006 May;117(5):e903-e908. (7) Moes CA, Mawson JB, MacDonald C, Smallhorn J. Right aortic arch with retroesophageal left aberrant innominate artery. Pediatr Cardiol 1996 November;17(6):402-6.
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(8) Grollman JH, Jr., Bedynek JL, Henderson HS, Hall RJ. Right aortic arch with an aberrant retroesophageal innominate artery: angiographic diagnosis. Radiology 1968 April;90(4):782-3. (9) Garti IJ, Aygen MM. Right aortic arch with aberrant left innominate artery. Pediatr Radiol 1979 February 26;8(1):48-50.
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(10) Rajaram PC, Hussain AT, Lakshmikanthan C, Vaidyanathan D, Subramanian N, Vasudevan S. Type D double aortic arch. Double aortic arch with interruption of its left component proximal to the site of origin of left common carotid artery. Angiology 1983 September;34(9):597-603.
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(11) Schlesinger AE, Leiter BE, Connors SK. Computed tomography diagnosis of right aortic arch with an aberrant left innominate artery. J Comput Tomogr 1984 January;8(1):81-7. (12) Maurus KE, Firmin RK, Leanage R. A rare anomaly of the aortic arch complex. Int J Cardiol 1988 July;20(1):149-51. (13) Nakajima Y, Satomi G, Kawamura T, Nishibatake M, Nakazawa M, Takao A. Right aortic arch with aberrant retroesophageal innominate artery: a report of 2 cases and review of the literature. Int J Cardiol 1993 March;38(3):247-51. (14) Ishizaka T, Allen SW, Strouse PJ, Ohye RG. Postductal origin of the left carotid, left subclavian, and aberrant retroesophageal right innominate arteries in truncus arteriosus with interrupted aortic arch. Pediatr Cardiol 2003 November;24(6):581-4. (15) Sett SS, Mawson JB, Sandor GG. Repair in infancy of right aortic arch with aberrant left brachiocephalic artery in the setting of a variant of the hypoplastic left heart syndrome. Cardiol Young 2004 August;14(4):441-3.
ACCEPTED MANUSCRIPT Udupa 12 (16) Rios-Mendez RE, rauz-Martinez ME. [Chronic wheezing child and type "D" double aortic arch: case report]. Arch Argent Pediatr 2008 December;106(6):548-51. (17) Fellmer PT, Bohner H, Wolf A, Roher HD, Goretzki PE. A left nonrecurrent inferior laryngeal nerve in a patient with right-sided aorta, truncus arteriosus communis, and an aberrant left innominate artery. Thyroid 2008 June;18(6):647-9.
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(18) Kondrachuk O, Yalynska T, Yemets I. Right aortic arch with retroesophageal brachiocephalic artery. Cardiol Young 2009 June;19(3):292-3.
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Udupa 13 Table 1: Summary of literature involving patients with a retro-esophageal brachiocephalic artery Year
n
Age
Symptoms
Modality for Diagnosis
Grollman et al.(8;8)
1968
1
19 yrs
Dyspnea on exertion
Esophagram and Arteriogram
Right
Garti et al.(9)
1979
1
9 yrs
Dysphagia and recurrent URTI
Esophagram and Arteriogram
Right
Rajaram et al. (10)
1983
1
5 yrs
Recurrent URTI
Angiogram
Right
Schlesinger et al (11)
1984
1
61 yrs
CT
Right
Maurus et al (12)
1988
1
6 mos
None incidental on CXR Heart failure
Angiogram
Nakajima et al (13)
1993
2
1 yr
1
5 wks
Ishizaka et al. (14)
2003
1
1 day
Cyanosis
Sett et al. (15)
2004
1
5 wks
Cyanosis and failure to thrive
Rios-Mendez et al. (16)
2008
1
8 yrs
Dyspnea and dysphagia
Fellmer et al. (17)
2008
1
1 day
Cyanosis
Kondrachuk et al. (18)
2009
1
3 mo
Dysphagia and dyspnea
Valvular aortic stenosis
None
None
PDA and bilateral pulmonary artery stenosis
Arterial Ligament Division PDA ligation
VSD and PDA
Right
Tetralogy of Fallot
PDA Ligation, and VSD closure Tetralogy of Fallot repair
Right
VSD
None
Angiogram
Right
ASD, PSD, aortopulmonary window and PDA
Complete repair
Echocardiogram and MRI
Left
Common Arterial Trunk (type II), single coronary artery, aortic arch interruption
Complete repair
CT
Right
Severe mitral stenosis, large VSD, bicuspid aortic valve, arch hypoplasia, left superior vena cava
Norwood procedure
Esophagram and Arteriogram
Right
None
PDA ligation
Angiogram
Right
Common Arterial Trunk (Type I)
Complete repair
CT
Right
PDA
PDA ligation
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Right
Angiogram and MRI
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1996
Intervention
None
Angiogram
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Moes et al (7)
Associated CHD
None
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9 yr
None incidental on CXR None incidental on investigation for murmur Stridor and URTI
Aortic Arch Sidedness
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Authors
Legend: CT: computer assisted tomography, CXR: chest radiograph, MRI: magnetic resonance imaging, VSD: ventricular septal defect, PDA: patent arterial duct, ASD: atrial septal defect, URTI: upper respiratory tract infection
ACCEPTED MANUSCRIPT Udupa 14 Figure 1 Legend 3D volume rendered magnetic resonance angiogram of a right aortic arch with an aberrant left retroesophageal brachiocephalic artery. Note the prominent base of the brachiocephalic artery,
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reminiscent of a diverticulum of Kommerrell, indicating that the arterial duct originated from the brachiocephalic artery to connect to the pulmonary trunk, thereby completing the vascular ring. The dotted line represents the location of the arterial ligament.
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AAO: Ascending aorta; REBA: retro-esophageal brachiocephalic artery; PT: pulmonary trunk; DOA:
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descending aorta.
Figure 2 Legend
A. The hypothetical model for the double aortic arch proposed by JE Edwards. LAA: left aortic arch; LCCA: left common carotid artery; LPA: left pulmonary artery; LSA: left subclavian artery; PT:
RSA: right subclavian artery.
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pulmonary trunk; RAA: right aortic arch; RCCA: right common carotid; RPA: right pulmonary artery;
B. Formation of a right aortic arch with an aberrant left retro-esophageal brachiocephalic artery is
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postulated to occur due to an interruption in the anterior portion of the left branch of the aortic sac, proximal to the origin of the left common carotid artery. The right aortic arch is formed by persistence
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of the right branch of the aortic sac, the right aortic arch, and the right dorsal aorta. The left dorsal aorta persists and connects to the distal portion of the left aortic arch, forming the brachiocephalic artery. Completion of the vascular ring occurs when a left sided arterial duct or arterial ligament connects the aberrant left retro-esophageal brachiocephalic artery to a pulmonary artery. The red lines indicate areas of regression. [Reprinted from Paediatric Cardiology, 3rd Edition, Anderson RH, Baker EJ, Penny DJ, Redington AN, Rigby ML, Wernovsky G [eds], “Vascular Rings, Pulmonary Arterial Sling, and Related Conditions”, Yoo S-J and Bradley TJ, pp967-989, with permission from Elsevier; originally modified from Edwards
ACCEPTED MANUSCRIPT Udupa 15 JE: Anomalies of the derivatives of the aortic arch system. Med Clin N Am 1948;32:925–948; and Edwards JE: Vascular rings and slings. in Moller JH, Neal AN [eds]: Fetal, Neonatal, and Infant
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Cardiac disease. Norwalk, CT: Appleton & Lange, 1990, pp 745–754.].
Video Legend
3D volume rendered magnetic resonance angiogram of a right aortic arch with an aberrant left retro-
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esophageal brachiocephalic artery. The prominent base of the brachiocephalic artery, reminiscent of a diverticulum of Kommerrell, indicates that the arterial duct originated from the brachiocephalic artery
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to connect to the pulmonary trunk.
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