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Anomalous Origin of the Right Vertebral Artery: Incidence and Significance
Original Article
Anomalous Origin of the Right Vertebral Artery: Incidence and Significance Tanmoy Kumar Maiti, Subhas Kanti Konar, Shyamal Bir, Anil Nanda, Hugo Cuellar
OBJECTIVE: Detailed knowledge about anatomic variations of the aortic arch and its multiple branches is extremely important to endovascular and diagnostic radiologists. It is often hypothesized that anomalous origin and distribution of large aortic vessels may alter the cerebral hemodynamics and potentially lead to a vascular pathology.
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INTRODUCTION
METHODS: In this article, we describe a case of anomalous origin of the right vertebral artery, which was detected during an intervention. We further reviewed the available literature of anomalous origin of the right vertebral artery. The probable embryologic development and clinical significance are discussed.
he vertebral artery (VA) is classically described as the first branch of the ipsilateral subclavian artery (SCA). In angiographic or anatomic postmortem studies, the anomalous origin of the VA, either right or left or both, is mostly incidental. But the anatomy of the VA and its various anomalies may become relevant during endovascular intervention or neck surgery. Anomalous origin of the right vertebral artery (RVA) is less common than its counterpart. The present report describes a case of anomalous origin of the RVA and discusses the various anomalous origins of RVA described in the literature with their possible embryologic development processes.
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RESULTS: The incidence of anomalous origin of a vertebral artery seems to be underestimated in recent literature. A careful review of the literature shows more than 100 such cases. The right vertebral artery can arise from the aortic arch or one of its branches. Dual origin of the vertebral artery is not uncommon. The embryologic developmental hypotheses are contradictory and complex.
T
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CONCLUSIONS: Anomalous origin of the right vertebral artery may not be the sole reason behind a disease process. However, it can certainly lead to a misdiagnosis during diagnostic vascular studies. Detailed information is essential for any surgery or endovascular intervention in this location.
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Key words Anomalous origin - Clinical significance - Embryologic development - Misdiagnosis - Right vertebral artery -
Abbreviations and Acronyms CCA: Common carotid artery CIA: Cervical intersegmental artery LCCA: Left common carotid artery LVA: Left vertebral artery LSCA: Left subclavian artery RCCA: Right common carotid artery RSCA: Right subclavian artery
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METHODS An exhaustive literature search was conducted using electronic databases (MEDLINE, EMBASE, CAB Abstracts, Current Contents, and Google Scholar) for relevant published articles. The search terms used were “anomalous origin of RVA” and “dual origin of RVA.” The resulting citations were exported, and the articles were screened independently by 2 authors (T.M. and H.C.) by reviewing the titles, abstracts and full texts. Bibliographies of identified publications and articles citing them were also examined. Both cadaver and clinical studies were included in the analysis. Data from identifiable papers are summarized in Table 1. Illustration of normal variant and anomalous origin of RVA has been depicted in Figure 1. The associated anomalies and clinical presentation/significance are shown in Table 1 where information was available.
RVA: Right vertebral artery SCA: Subclavian artery VA: Vertebral artery Department of Neurosurgery, Louisiana State University Health Sciences Center, Shreveport, LA, USA To whom correspondence should be addressed: Hugo Cuellar, M.D, Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2015). http://dx.doi.org/10.1016/j.wneu.2015.11.018 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
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ORIGINAL ARTICLE TANMOY KUMAR MAITI ET AL.
ANOMALOUS ORIGIN OF THE RIGHT VERTEBRAL ARTERY
Table 1. Anomalous Origin of the Right Vertebral Artery: A Systematic Review of 115 Cases Including the Present Case
Number
Study
Clinical Significance/ Presentation
Other Anomaly
Table 1. Continued
Number
Study
Other Anomaly
Clinical Significance/ Presentation
I. Origin as a single vessel I. Origin as a single vessel
10
Stoesslein et al., 198214
Coarctation
11
Lemke et al., 199915
None
None
12
Kodama, 200016 None
None
13
Karcaaltincaba LVA arises between the None et al., 200317 origins of the LCCA and LSCA
14
None Ligege and Scholtz, 200418
15
Goray et al., 200519
LVA from the aortic arch Evaluation of beyond the origin of the spondyloepiphyseal LSCA (fourth branch); dysplasia with CTA RVA was the fifth branch
16
Satti et al., 200720
None
17
Al-Okaili and Schwartz, 200721
LVA arising from aortic Incidental; evaluation arch between the LCCA of trauma; identified and LSCA with MRA
18
Higashi et al., 200822
Retro-esophageal course of the RVA
19
Hsu et al., 201023
LVA distal to the LSCA Thoracic aortic trauma (fourth branch); RVA was evaluation with CTA the fifth branch
20
None Dabus and Walker, 201024
Incidental; MRA
21
Uchino et al., 201325
None
Incidental
22
Lale et al., 201426
None
Incidental
23
Present case, 2015
None
Incidental
A. Originating from the aortic arch 1. RVA originating from the ascending aorta, just above the left coronary sinus 1
Akdeniz et al., 20071
Aberrant retroesophageal RSCA
Acute coronary syndrome; coronary angiography and MRA
2. RVA from aortic arch between the innominate artery and LCCA 1e4
Poynter, 19162
Proximal to distal: innominate artery, RVA, LCCA, LVA, and LSCA
NA
3. RVA from the aortic arch between the RSCA and RCCA in cases of missing brachiocephalic arteries 1e3
4
Poynter, 19162
Proximal to distal: RSCA, RVA, RCCA, LCCA, LVA, and LSCA
NA
NA
NA
Lippert and Pabst, 19853
4. RVA from aortic arch between the LCCA and LSCA None
CTA evaluation of RTA
1
Wasserman et al., 19924
2
Albayram et al., LVA fourth branch and Evaluation of SAH RVA fifth branch; distal 20025 right anterior cerebral artery aneurysm at the A2-A3 junction
5. RVA from the aortic arch distal to the origin of the LSCA 1
Kemmentmüller, Retro-esophageal course of the RVA 19116
2
Lie, 19687
NA
NA
3
ObounouAkong, 19694
NA
NA
4
Newton and Mani, 19748
NA
NA
5
Nakaba, 19769 Retro-esophageal course of the RVA
6
Argenson et al., 198010
NA
NA
7
Sakamoto, 198011
NA
NA
8
Schwarzacher and Krammer, 198912
LVA arising from the aortic arch between the LCCA and LSCA
NA
9
Takagi and Yamashita, 199213
Coronary sinus opening Cadaver study into the left atrium
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Evaluation of CVA with CTA
MRA evaluation of left cerebellar infarct
Cadaver study
B. Origin other than the aortic arch 1. RVA directly from the brachiocephalic artery
NA
Continues
2
NA
1
Daseler and Anson, 195927
NA
NA
2
Argenson et al., 198010
NA
NA
3
Lippert and Pabst, 19853
NA
NA
4
Yamaki et al., 200628
None
Cadaver study
2. RVA from the RSCA, distal to the right thyrocervical trunk 1
Koenigsberg et al., 200329
none
CTA evaluation of CAD Continues
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ORIGINAL ARTICLE TANMOY KUMAR MAITI ET AL.
ANOMALOUS ORIGIN OF THE RIGHT VERTEBRAL ARTERY
Table 1. Continued
Number
Study
Table 1. Continued
Other Anomaly
Clinical Significance/ Presentation
I. Origin as a single vessel
1
Iyer, 192730
ARSCA (arteria lusoria) (RSCA from the arch distal to the LSCA with a retro-esophageal course)
NA
2
Windel et al., 192831
ARSCA
NA
3
Newton and Mani, 19748
ARSCA
NA
4
Bernardi and Deton, 197532
ARSCA
NA
5e7
Palmer, 197733 ARSCA
NA
8
Tan and Spigos, ARSCA 197934
NA
9
Wackenheim ARSCA and Kleinclaus, 197935
NA
NA
10
Roszel and Keily, 199136
ARSCA
11
Chen et al., 199837
Nonopacification of the Incidental LVA, RSCA from the aortic arch, LSCA from the descending aorta distal to the origin of the RSCA
Other Anomaly
33
Park et al., 200844
ARSCA distal to the Incidental LSCA LVA originated from the aortic arch between the LCCA and the LSCA
34
Cheng et al., 200945
Aortic arch: proximal to CTA: anterior distal: RCCA, LCCA, communicating artery LSCA, and RSCA aneurysmal SAH
35
Cheng et al., 200945
Aortic arch: proximal to MRA evaluation of distal: RCCA, LCCA, apopsychia LSCA, and RSCA
36
Ishihara et al., ARSCA, persistent trigeminal artery 201146
Proximal to distal: RCCA, Evaluation of blurred LCCA, RSCA, and LSCA vision and dizziness
13
Koenigsberg et al., 200329
ARSCA
37e38 Uchino et al., 201325
ARSCA arising from the Incidental aortic arch distal to the left SCA
39
Nalamada et al., 201347
ARSCA
40
Nalamada et al., 201347
RCCA and ARSCA arose Left posterior directly from the aortic communicating aneurysm arch
14
Brouwer et al., ARSCA; LVA from the MRA evaluation of arch between the LCCA TIA 200439 and LSCA
15
Fazan et al., 200440
Proximal to distal at arch: RCCA, LCCA, LSCA, and RSCA
Cadaver study
16
Layton et al., 200641
ARSCA
Left MCA infarct
17
Ka-Tak et al., 200742
ARSCA; LVA from the Incidental aortic arch between the LCCA and LSCA ARSCA, LVA from the arch
Incidental
22e31 Tsai et al., 200743
ARSCA
Incidental
32
ARSCA distal to the LSCA
Incidental
Continues
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Ruptured left anterior choroidal aneurysm
1
Daseler and Anson, 195927
NA
NA
2
Koo and Sakai, 196648
NA
NA
3
Bernardi and Deton, 197532
Separate origin of Left hemiparesis RSCA and RCCA from arch; no brachiocephalic trunk
4
Bernardi and Deton, 197532
Separate origin of RCSA Ataxia and RCCA from arch; no brachiocephalic trunk; LVA from arch
5
Lippert and Pabst, 19853
6
Gluncic et al., 199949
LVA arising from the aortic arch
Incidental
7
Yanik et al., 200450
None
Doppler evaluation of subacute infarct in the right cerebral pedicle and cerebellar vermis
8
Ugurlucan et al., Both carotid arteries 200651 arising from the aortic arch as a common trunk
9
Uchino et al., 201325
Angiogram after MI
18e21 Tsai et al., 200743
Incidental
4. RVA from the RCCA without arteria lusoria
Best and Bumpers, 200238
Park et al., 200844
Study
I. Origin as a single vessel
3. RVA from the RCCA with anomalous right SCA
12
Number
Clinical Significance/ Presentation
NA
None
NA
Evaluation for TIA
Incidental
Continues
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ORIGINAL ARTICLE TANMOY KUMAR MAITI ET AL.
ANOMALOUS ORIGIN OF THE RIGHT VERTEBRAL ARTERY
Table 1. Continued
Number
Table 1. Continued
Study
Other Anomaly
Clinical Significance/ Presentation
I. Origin as a single vessel
Adachi and Das, 192852
NA
Matula et al., 199753
None
Melki et al., 201267
None
Vertebrobasilar CAD, pseudodissecting aneurysm in right VA
16
Uchino et al., 201325
None
None
Incidental
17
Rameshbabu et al., 201468
Dual origin of LVA (the CTA evaluation of medial limb from arch dizziness and the lateral limb from LSCA)
7. RVA from the right internal carotid artery via the hypoglossal artery 1
Other Anomaly
15 NA
6. RVA from external carotid artery 1
Study
I. Origin as a single vessel
5. RVA from the thyrocervical trunk 1
Number
Clinical Significance/ Presentation
NA
Keller and Weiss, 197354
NA
2. Dual origin from the RSCA and the brachiocephalic artery
II. Dual origin
1
Kiss, 196869
1. Dual origin from the RSCA 1
Lie, 19687
Not known
2
Babin and Haller, 197455
Elongation of RVA; dolichoarterial loop of LVA
NA Epilepsy
Paresthesia of right arm
3. Dual origin from the RSCA and the right CCA
3
Argenson et al., 198010
NA
NA
4
Rath and Prakash, 198456
NA
5
Harada et al., 198757
Hypoplastic LVA
Evaluation of dizziness
6
Hashimoto et al., 198758
None
Temporal and cerebellar infarction
7
Nishijima et al., 198959
NA
Evaluation of dizziness
8
Cavdar and Arison, 198960
NA
NA
9
Takasato et al., Rudimentary LVA, Brainstem infarction 199261 accessory artery that arose from a branch of the left thyrocervical trunk
1
Goddard et al., None 200170
2
Kumar and Kumar, 201471
Cadaver study
NA
10
Nogueira et al., 199762
11
Dual origin of LVA both MRA evaluation of Ionete and cognitive impairment Omojola, 200663 from LSCA
12
Harnier et al., 200864
Duplication of the RCCA MRA evaluation of fenestration of the LCCA dizziness
13
Thomas et al., 200865
Midbasilar trunk aneurysm
14
Mordasisni, 200866
Dual origin of LVA (1 MRA evaluation of limb from the aortic arch MCA stroke and the other from the LSCA)
None
MRA evaluation of TIA
Common origin of both None the CCA (first major branch of the aortic arch)
4. Dual origin from the RSCA and the right thyrocervical trunk 1
NA
LCCA from brachiocephalic artery, LVA from aortic arch, double axillary artery
NA
Lippert and Pabst, 19853
NA
5. Dual origin from the RSCA and aortic arch distal to the LSCA 1
Hsu et al., 201023
None
Diagnosed with CTA to evaluate a previously placed stent graft
6. Dual origin of RVA, site not mentioned LVA arising from the aortic arch
1
Cavdar et al., 198960
2
Goddard et al., None 200170
Cadaver study Incidental MRA evaluation of left MCA stroke
RVA, right vertebral artery; RSCA, right subclavian artery; MRA, magnetic resonance angiography; LCCA, left common carotid artery; LVA, left vertebral artery; LSCA, left subclavian artery; NA, not available; RCCA, right common carotid artery; CTA, computed tomography angiography; RTA, renal tubular acidosis; SAH, subarachnoid hemorrhage; CVA, cerebrovascular disease; SCA, subclavian artery; ARSCA, aberrant right SCA; MI, myocardial infarction; TIA, transient ischemic attack; MCA, middle cerebral artery; CAD, coronary artery disease; VA, vertebral artery; CCA, common carotid artery.
Continues
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ANOMALOUS ORIGIN OF THE RIGHT VERTEBRAL ARTERY
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ANOMALOUS ORIGIN OF THE RIGHT VERTEBRAL ARTERY
Figure 2. Images of the present case. (AeC) Digital subtraction angiogram. (A) Innominate artery roadmap. Right vertebral artery (RVA) is not seen to arise from the right subclavian artery (arrow). (B) RVA (white arrows) originating directly from the arch of the aorta, distal to the origin of the left subclavian artery
(black arrow). (C) RVA (white arrow) has a retro-esophageal course, left vertebral artery (black arrow). (DeG) Computed tomography angiogram: coronal view of the neck from posterior to anterior: RVA (arrows) is seen to arise directly from the aortic arch and has a retro-esophageal course.
CASE REPORT
DISCUSSION
A 56-year-old man presented with dysphagia, odynophagia, hoarseness of voice, and significant weight loss. On subsequent evaluation, he was found to have supraglottic carcinoma. He underwent a total laryngectomy, total glossectomy, and bilateral neck dissection, and he received chemoradiation. After 4 months, he developed hematemesis. He was scheduled for embolization of the residual mass. During the angiogram, an anomalous origin of the RVA was noted. It was found to originate directly from the aortic arch as the last branch (fourth branch) and have a retro-esophageal course. The left vertebral artery (LVA) originated normally from the left subclavian artery (LSCA) (Figure 2).
Both the right and left vertebral arteries usually arise from the posterosuperior aspect of the first part of the SCA. They extend inward and upward to the transverse process of C6, pass through the foramina of all of the upper cervical transverse processes, curve medially behind the lateral mass of the atlas, and then enter the cranium through the foramen magnum. Anomalous origin of the RVA is underestimated in recent literature. An aberrant right subclavian artery (RSCA) is the most common vascular ring anomaly in the aortic arch, with a reported incidence of 0.5%e2%.72 Thus, it can be argued that the RVA is anomalous when it originates from an aberrant SCA. In this article, we limit our discussion to the anomalous point of origin of the
= Figure 1. (A) Origin of the right vertebral artery (RVA) from the right subclavian artery (RSCA): normal variant. (BeM) Origin of the RVA as a single vessel: RVA from the ascending aorta (B) (n ¼ 1), aortic arch between the RSCA and the right common carotid artery (RCCA) (C) with missing brachiocephalic artery (n ¼ 4), brachiocephalic artery (D) (n ¼ 4), brachiocephalic artery, and left common carotid artery (E) (n ¼ 4), left common carotid artery and left subclavian artery (LSCA) (F) (n ¼ 2), distal to the LSCA (G) (n ¼ 23), RSCA distal to the right thyrocervical trunk (H) (n ¼ 1), RCCA with normal RSCA (I) (n ¼ 9), RCCA with aberrant RSCA (J) (n ¼ 40), right thyrocervical trunk (K) (n ¼ 1), right internal carotid artery (L) (n ¼ 1), and right external carotid artery (M) (n ¼ 1). (NeR) Dual origin of RVA: both originating from the RSCA (N) (n ¼ 17), RSCA and brachiocephalic artery (O) (n ¼ 1), RSCA and right thyrocervical trunk (P) (n ¼ 1), RSCA and RCCA (Q) (n ¼ 2), RSCA and arch distal to the LSCA (R) (n ¼ 1).
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ANOMALOUS ORIGIN OF THE RIGHT VERTEBRAL ARTERY
RVA. Cases where the origin of RVA was from an aberrant SCA have not been included in the present discussion. We also excluded cases where the VA was missing. Origin of RVA as a Single Vessel VA origin can be divided into 2 groups: those originating from the aortic arch (n ¼ 34) and those originating neither from the arch nor the SCA (Table 1).1-54 Origin from the ascending aortic arch seems to be the rarest of all and is described only once in the literature,1 where it is associated with acute coronary syndrome. In his comprehensive review in 1916, Poynter2 recorded 31 cases of aortic arches with 5 branches and 4 with 6 branches. In 7 of these 35 specimens, both VAs arose from the aortic arch. The aortic branching pattern, in a proximal to distal progression, was as follows: (1) innominate artery, RVA, left common carotid artery (LCCA), LVA, and LSCA (4 cases) or (2) RSCA, RVA, right common carotid artery (RCCA), LCCA, LVA, and LSCA (3 cases). One similar case has been described by Lippert and Pabst,3 where the RVA originated from the aortic arch between the RSCA and the RCCA in cases of missing brachiocephalic arteries. Origin between the LCCA and the LSCA is another rare variation and has been documented only twice.4,5 The most common anomalous origin of the RVA occurs from distal to the origin of the LSCA. In these cases, the RVA represents the last branch of the aortic arch. In most of these cases, the RVA took a retro-esophageal course to reach its entry into the vertebral foramen. In contrast, anomalous origin of the RVA from other vessels has been noted in more than 50 occasions. It may originate directly from the brachiocephalic or innominate artery instead of the RSCA. In one case, it was noted to arise from the RSCA distal to the right thyrocervical trunk instead of being the first branch.29 Most commonly, they originate from the RCCA (n ¼ 49). In most cases, the RSCA has an anomalous origin. The RSCA is the last branch of the aortic arch and has a retro-esophageal course, known as arteria lusoria. In a study of 102 patients with aberrant RSCA, Tsai et al.43 found a VA anomaly in 15.7% of patients. Interestingly, when one VA had an anomalous origin, the incidence of a VA anomaly on the other side increased.43 Dual origin of the RVA The term “duplication” has been erroneously used interchangably with “fenestration” (Table 1).3,7,10,23,25,55-71 The term “duplication” describes the dual origin of a VA with a variable fusion at the neck. In contrast, the term “fenestration” is used to describe the single origin of a vessel with 2 parallel segments anywhere along the course. Duplication of the VA is much rarer than a fenestration.70 The frequency was identified as 0.72% in one cadaver study.73 In that study, 5 of 693 specimens had dual origin of the VA and, incidentally, all were left sided.73 The incidence seems to be more common on the left side.68 In most of these cases, both origins were from the RSCA. In other cases, 1 was from the RSCA, and others were either from the brachiocephalic artery, the RCCA, the right thyrocervical trunk, or the arch of the aorta. This pattern of origin is different from the LVA, where the lateral crus starts from the LSCA and the medial starts from the aortic
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Figure 3. Normal schematic diagram of the primitive ventral and dorsal aorta, 6 aortic arches, dorsal aortic root segments (DARS), and dorsal intersegmental arteries (DISA) (modified from Satti et al.20 and Higashi et al.22). CA, ascending cervical artery; SCA, subclavian artery; VD.
arch. Bilateral dual origin of the VA is exceedingly rare and has been reported only 3 times.68 Embryology The embryology of the VA is complex, and several hypotheses have been described in the literature (Figures 3 and 4). Accordingly, the explanations are different for the development of the various anomalies. Knowledge of the development of the aortic arch, the brachiocephalic artery, and the SCA is also important to understand the association. At the initial stage of development there are 2 aortic trunks (ventral and dorsal aorta). The primitive ventral aorta persists bilaterally. The right forms the innominate artery (brachiocephalic artery) and the right common and right external carotid arteries. The left gives rise to a short portion of the aortic arch, the left common carotid arteries, and left external carotid arteries. The earliest development of the VA is apparent when the embryo is at the 7-mm stage. The developmental process is usually complete by the 14- to 17-mm stage.8,37 At the 7-mm stage (day 32), 7 cervical intersegmental arteries (CIAs) appear, originating from each of the paired dorsal aortae accompanying the cervical segmental nerves 2e8.65,74 At the 10- to 12-mm stage,
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ANOMALOUS ORIGIN OF THE RIGHT VERTEBRAL ARTERY
Figure 4. Normal schematic diagram demonstrating the embryologic origins of the arch and its major branches. LEC, left external carotid artery; LIC, left internal carotid; REC, right external carotid artery; RIC, right internal carotid artery (modified from Satti et al.20).
a longitudinal anastomosis develops between the CIAs. At the 14- to 17-mm stage, the horizontal parts of the first 6 CIAs disappear, and the remaining seventh CIA becomes part of the SCA.8,37 On the left side, the entire proximal LSCA to the level of the internal thoracic artery results from the persistent left seventh dorsal intersegmental artery. On the right, the seventh dorsal intersegmental artery forms the distal one third of the proximal RSCA. The proximal and midzones of the proximal RSCA are formed by the right fourth aortic arch and segments 3e7 from the right dorsal aortic root.20 Segments 3e7 from the left dorsal aortic root form a small segment of the aorta at the origin of the LSCA.20 Most authorities believe that the VA originates from the persistent longitudinal anastomosis of CIAs, which persists after involution of the horizontal segments.8,37 Some authorities believe that the VA arises from the distal aspect of the seventh dorsal intersegmental artery20 (sixth according to some70). These developmental processes result in a normal origin of the VA from the SCA. A detailed review of the literature suggests that an anomalous origin of the VA is more common on the left side than the right. It is difficult to explain those anomalies. However, we discuss the more common types. Failure of involution in one of the first 6 CIAs (ie, a persistent CIA) causes a variety of abnormal origins of the VA. If the persistent CIA occurs in the upper (first or second) intersegmental arteries, the result is an abnormal origin of the VA from the internal or external carotid artery. If it occurs in the lower (third to sixth) CIAs, the result is an abnormal origin of the VA from the aortic arch or the common carotid artery (CCA).6,13 The second occurrence is the more common.
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The origin of the RVA as the last branch of the aorta distal to the LSCA can result from persistence of the right dorsal aorta and the obliteration of the right fourth arch. According to some reports, it can result from persistence of the C8 intersegmental artery.23 The incidence of anomalous origin of the RVA from the RCCA (VA-CC) is 0.18%.33 Two different embryonic mechanisms for VACC have been described.37,39,47 In the first (type I), the sixth CIA develops into the VA with degeneration of the anastomosis between the sixth and seventh CIAs. The aberrant SCA results from the involution of the ipsilateral middle dorsal aorta and the remaining ipsilateral seventh CIA connecting to the contralateral (left) dorsal aorta. The anterior spinal artery is ipsilateral in type I. The second (type II) also has a persistent lower CIA, but instead of an involution of the ipsilateral middle dorsal aorta, the persistent CIA migrates upward to the level of the CCA. Type I anomaly does not occur on the left side as the condition is incompatible with life. There are multiple explanations for dual origin of VA. It may occur when a portion of the primitive dorsal aorta persists along with 2 intersegmental vessels connected to the true VA.75 Another possible explanation is failure of regression of the fifth or sixth intersegmental arteries, which adds a further possible origin to the VA along with the normal seventh segment.76 Significance: Are they Always Incidental? In most cases, the anomalous origin of the VA is an incidental finding. Many patients were diagnosed after evaluation for dizziness. Some authors4,15 have hypothesized that an anomalous origin and the distribution of the VAs might result in cerebral hemodynamic perturbation with secondary cerebral changes. However, conclusive evidence is lacking to support such a hypothesis. Koenigsberg et al.29 found anomalous origin of the VA in 2 cases of vertebral insufficiency. However, as the authors rightly pointed out, the anomalous origin of the VA cannot be concluded to be the only reason behind the presentation. Palmer33 suggested that atheromatous disease of the proximal CCA might be considered to be of more hemodynamic significance in the presence of this anomaly. Multiple cases of coexisting pathologies can occur, for example, aneurysm,5,45,47 arterial infarct,20,50,61 transient ischemic attack,70 arachnoid cyst,63 and hereditary connective tissue disorder, such as Ehlers-Danlos syndrome.74 However, the knowledge of variants of VA origin appears to be mandatory for planning aortic arch surgery or endovascular interventions. Anomalous VA origin also represents a potential pitfall in the diagnosis of cerebrovascular injury. One or both VAs may be wrongly assumed to be occluded or diseased, either by eluding catheterization during angiography or by lying outside the region of interest during noninvasive studies such as computed tomography angiography, magnetic resonance angiography, or Doppler sonography. A surgeon using bypass techniques should be aware of this anomaly to avoid inducing vertebra-basilar ischemia while clamping the carotid artery. If a right brachial or transaxillary angiogram fails to identify the vertebral anomaly, its presence should be excluded by alternative techniques.
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ANOMALOUS ORIGIN OF THE RIGHT VERTEBRAL ARTERY
Patients with dual origin of VA may be predisposed to damage in severe cervical spine injuries because of the additional point of attachment. Polguj et al.74 suggested that the lumen of a duplicated VA is smaller than normal. This may cause difficult catheterization and misinterpretation as hypoplastic VA. Some authors have suggested that dual origin can contribute to vertebral dissection.67 A comparative analysis suggests that the incidence of vertebral dissection is more common in cases with VA fenestration than VA duplication.74 Therefore, these 2 entities should be distinguished. Even though conventional intra-arterial digital subtraction angiography remains the gold standard method for imaging the VAs, noninvasive modalities such as ultrasonography, multislice computed tomography angiography, and magnetic resonance
REFERENCES
angiography are constantly improving and can play an increasingly important role in diagnosing VA pathology in clinical practice. CONCLUSIONS Anomalous origin of RVA is rarer than LVA. The plausible embryologic explanation is often difficult to understand. Although these findings may be incidental in most cases, detailed information is required before any surgical/endovascular intervention to avoid any misinterpretation and inadvertent injury to VA. ACKNOWLEDGMENT We thank Mr. David Wright for help and contribution to the illustrations in this article.
with both vertebral arteries as additional branches of the aortic arch. Anat Rec. 1989;225:246-250.
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3. Lippert H, Pabst R. Arterial variations in man. Vol. 6. Germany: JF Bergmann Verlag Mi.inchen; 1985: 82. 4. Wasserman BA, Mikulis DJ, Manzione JV. Origin of the right vertebral artery from the left side of the aortic arch proximal to the origin of the left subclavian artery. AJNR Am J Neuroradiol. 1992;13: 355-358. 5. Albayram S, Gailloud P, Wasserman BA. Bilateral arch origin of the vertebral arteries. AJNR Am J Neuroradiol. 2002;23:455-458. 6. Kemmetmüller H. Über eine seltene Varietät der Art. vertebralis. Anat Hefte I Abte Bd. 1911;44: 306-361. 7. Lie T. Congenital anomalies of the carotid arteries. Vol. 30. The Netherlands: Excerpta Medica Foundation; 1968:84-93. 8. Newton T, Mani R. The vertebral artery. In: Newton TH, Potts DG, eds. Radiology of skull and brain. St. Louis: Mosby; 1974:1659-1672. 9. Nakaba H. A drawing of a peculiar right vertebral artery. In: Kumaki K, ed. Anatomical data from the dissection practice of the Kanazawa University School of Medicine. Kanazawa: 2nd Department of Anatomy in Kanazawa University School of Medicine; 1980:334. 10. Argenson C, Francke J, Sylla S, Dintimille H, Papasian S, diMarino V. The vertebral arteries (Segments V1 and V2). Anat Clin. 1980;2:29-32. 11. Sakamoto H. A case of the right vertebral artery as the last branch of the aortic arch. Acta Anat Nippon (in Japanese with English summary). 1980;55:503-509. 12. Schwarzacher SW, Krammer EB. Complex anomalies of the human aortic arch system: unique case
15. Lemke AJ, Benndorf G, Liebig T, Felix R. Anomalous origin of the right vertebral artery: review of the literature and case report of right vertebral artery origin distal to the left subclavian artery. AJNR Am J Neuroradiol. 1999;20:1318-1321. 16. Kodama K. Vertebral artery. In: Sato T, Akita K, eds. Anatomic Variations in Japanese. Tokyo: University of Tokyo Press (in Japanese); 2000:213-215. 17. Karcaaltincaba M, Strottman J, Washington L. Multidetector-row CT angiographic findings in the bilateral aortic arch origin of the vertebral arteries. AJNR Am J Neuroradiol. 2003;24:157. 18. Ligege P, Scholtz L. Rare variation in the origin of the right vertebral artery. SA J Radiol. 2004;8:34-35. 19. Goray VB, Joshi AR, Garg A, Merchant S, Yadav B, Maheshwari P. Aortic arch variation: a unique case with anomalous origin of both vertebral arteries as additional branches of the aortic arch distal to left subclavian artery. AJNR Am J Neuroradiol. 2005;26: 93-95. 20. Satti SR, Cerniglia CA, Koenigsberg RA. Cervical vertebral artery variations: an anatomic study. AJNR Am J Neuroradiol. 2007;28:976-980. 21. Al-Okaili R, Schwartz ED. Bilateral aortic origins of the vertebral arteries with right vertebral artery arising distal to left subclavian artery: case report. Surg Neurol. 2007;67:174-176 [discussion: 176]. 22. Higashi N, Shimada H, Simamura E, Hatta T. Right vertebral artery as the fourth branch of the aortic arch. Anat Sci Int. 2008;83:314-318. 23. Hsu DP, Alexander AD, Gilkeson RC. Anomalous vertebral artery origins: the first and second reports of two variants. J Neurointerv Surg. 2010;2: 160-162.
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24. Dabus G, Walker MT. Right vertebral artery arising from the aortic arch distal to the left subclavian artery diagnosed with magnetic resonance angiography. Arch Neurol. 2010;67:508. 25. Uchino A, Saito N, Takahashi M, Okada Y, Kozawa E, Nishi N, et al. Variations in the origin of the vertebral artery and its level of entry into the transverse foramen diagnosed by CT angiography. Neuroradiology. 2013;55:585-594. 26. Lale P, Toprak U, YagJz G, Kaya T, UyanJk SA. Variations in the Branching Pattern of the Aortic Arch Detected with Computerized Tomography Angiography. Adv Radiol. 2014;2014:1-6. 27. Daseler EH, Anson BJ. Surgical anatomy of the subclavian artery and its branches. Surg Gynecol Obstet. 1959;108:149-174. 28. Yamaki K, Saga T, Hirata T, Sakaino M, Nohno M, Kobayashi S, et al. Anatomical study of the vertebral artery in Japanese adults. Anat Sci Int. 2006;81:100-106. 29. Koenigsberg RA, Pereira L, Nair B, McCormick D, Schwartzman R. Unusual vertebral artery origins: examples and related pathology. Catheter Cardiovasc Interv. 2003;59:244-250. 30. Iyer AA. Some Anomalies of Origin of the Vertebral Artery. J Anat. 1927;62:121-122. 31. Windle WF, Zeiss FR, Adamski MS. Note on a Case of Anomalous Right Vertebral and Subclavian Arteries. J Anat. 1928;62:512-514. 32. Bernardi L, Deton P. Angiographic study of a rare anomalous origin of the vertebral artery. Neuroradiology. 1975;9:43-47. 33. Palmer FJ. Origin of the right vertebral artery from the right common carotid artery: angiographic demonstration of three cases. Br J Radiol. 1977;50: 185-187. 34. Tan WS, Spigos DG. Right vertebral artery originating from the right common carotid (author’s transl). Radiologe. 1979;19:155-156. 35. Wackenheim A, Kleinclaus D. [Right subclavian arteria lusoria with anomaly of the origin of the two vertebral arteries. A cause of functional vertebrobasilar insufficiency (author’s transl)]. J Radiol. 1979;60:657-658.
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ANOMALOUS ORIGIN OF THE RIGHT VERTEBRAL ARTERY
36. Roszel AJ, Kiely ML. A retroesophageal right subclavian artery with the right vertebral artery originating from the right common carotid artery. Clin Anat. 1991;4:373-379.
50. Yanik B, Conkbayir I, Keyik B, Hekimoglu B. A rare anomalous origin of right vertebral artery: findings on Doppler sonography. J Clin Ultrasound. 2004;32:211-214.
65. Thomas AJ, Germanwala AV, Vora N, Prevedello DM, Jovin T, Kassam A, et al. Dual origin extracranial vertebral artery: case report and embryology. J Neuroimaging. 2008;18:173-176.
37. Chen CJ, Wang LJ, Wong YC. Abnormal origin of the vertebral artery from the common carotid artery. AJNR Am J Neuroradiol. 1998;19:1414-1416.
51. Ugurlucan M, Sayin OA, Surmen B, Alpagut U, Dayioglu E, Onursal E. Common carotid trunk and right vertebral artery originating from the right common carotid artery in a patient with carotid stenosis. J Card Surg. 2006;21:423-424.
66. Mordasisni P, Schmidt F, Schroth G, Remonda L. Asymmetrical bilateral duplication of the extracranial vertebral arteries: Report of a unique case. Eur J Radiol Extra. 2008;67:e91-e94.
38. Best IM, Bumpers HL. Anomalous origins of the right vertebral, subclavian, and common carotid arteries in a patient with a four-vessel aortic arch. Ann Vasc Surg. 2002;16:231-234. 39. Brouwer PA, Souza MP, Agid R, Terbrugge KG. A five-vessel aortic arch with an anomalous origin of both vertebral arteries and an aberrant right subclavian artery. Interv Neuroradiol. 2004;10:309-314. 40. Fazan VP, Caetano AG, Filho OA. Anomalous origin and cervical course of the vertebral artery in the presence of a retroesophageal right subclavian artery. Clin Anat. 2004;17:354-357. 41. Layton KF, Miller GM, Kalina P. Aberrant origin of the right vertebral artery from the right common carotid artery: depiction of a rare vascular anomaly on magnetic resonance angiography. J Vasc Interv Radiol. 2006;17:1065-1067. 42. Ka-Tak W, Lam WW, Yu SC. MDCT of an aberrant right subclavian artery and of bilateral vertebral arteries with anomalous origins. AJR Am J Roentgenol. 2007;188:W274-W275. 43. Tsai IC, Tzeng WS, Lee T, Jan SL, Fu YC, Chen MC, et al. Vertebral and carotid artery anomalies in patients with aberrant right subclavian arteries. Pediatr Radiol. 2007;37:1007-1012. 44. Park JK, Kim SH, Kim BS, Choi G. Two cases of aberrant right subclavian artery and right vertebral artery that originated from the right common carotid artery. Korean J Radiol. 2008;9 (Suppl): S39-S42. 45. Cheng M, Xiaodong X, Wang C, You C, Mao B, He M, et al. Two anatomic variations of the vertebral artery in four patients. Ann Vasc Surg. 2009;23:689.e1-689.e5. 46. Ishihara H, San Millan Ruiz D, Abdo G, Asakura F, Yilmaz H, Lovblad KO, et al. Combination of rare right arterial variation with anomalous origins of the vertebral artery, aberrant subclavian artery and persistent trigeminal artery. A case report. Interv Neuroradiol. 2011;17:339-342. 47. Nalamada K, Chitravanshi N, Duffis EJ, Prestigiacomo CJ, Gandhi CD. Anomalous origin of the right vertebral artery from the right common carotid artery associated with an aberrant right subclavian artery. J Neurointerv Surg. 2013;5:e34. 48. Koo K, Sakai M. Uber einen Ausnahmefall der A. Vertebralis. Kurume Igakukai Zasshi (Jpn, with Ger abstract). 1966;29:167-173. 49. Gluncic V, Ivkic G, Marin D, Percac S. Anomalous origin of both vertebral arteries. Clin Anat. 1999;12: 281-284.
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52. Adachi B, Das A. Arteriensystem der Japaner, 1st edition. Vol. 1. Kyoto: Kenkyusha; 1928. 53. Matula C, Trattnig S, Tschabitscher M, Day JD, Koos WT. The course of the prevertebral segment of the vertebral artery: anatomy and clinical significance. Surg Neurol. 1997;48:125-131. 54. Keller HL, Weiss D. Origin of an artery supplying the vertebral region, descending from the cervical sector of the right internal carotid artery. Fortschr Geb Rontgenstr Nuklearmed. 1973;118:473-474. 55. Babin E, Haller M. Correlation between bony radiological signs and dolichoarterial loops of the cervical vertebral artery. Neuroradiology. 1974;7:15-17. 56. Rath G, Prakash R. Double vertebral artery in an Indian cadaver. Anat Clin. 1984;6:117-119. 57. Harada J, Nishijima M, Yamatani K, Endo S, Takaku A. A case of the duplicate origin of right vertebral artery. No Shinkei Geka. 1987;15:321-325. 58. Hashimoto H, Ohnishi H, Yuasa T, Kawaguchi S. Duplicate origin of the vertebral artery: report of two cases. Neuroradiology. 1987;29:301-303. 59. Nishijima M, Harada J, Akai T, Endo S, Takaku A. Operative correction of a kinked duplicate origin of the vertebral artery in a patient with dizziness. Case report. Surg Neurol. 1989;32:356-359. 60. Cavdar S, Arisan E. Variations in the extracranial origin of the human vertebral artery. Acta Anat (Basel). 1989;135:236-238. 61. Takasato Y, Hayashi H, Kobayashi T, Hashimoto Y. Duplicated origin of right vertebral artery with rudimentary and accessory left vertebral arteries. Neuroradiology. 1992;34:287-289. 62. Nogueira TE, Chambers AA, Brueggemeyer MT, Miller TJ. Dual origin of the vertebral artery mimicking dissection. AJNR Am J Neuroradiol. 1997; 18:382-384. 63. Ionete C, Omojola MF. MR angiographic demonstration of bilateral duplication of the extracranial vertebral artery: unusual course and review of the literature. AJNR Am J Neuroradiol. 2006;27:1304-1306. 64. Harnier S, Harzheim A, Limmroth V, Horz R, Kuhn J. Duplication of the common carotid artery and the ipsilateral vertebral artery with a fenestration of the contralateral common carotid artery. Neurol India. 2008;56:491-493.
67. Melki E, Nasser G, Vandendries C, Adams D, Ducreux D, Denier C. Congenital vertebral duplication: a predisposing risk factor for dissection. J Neurol Sci. 2012;314:161-162. 68. Rameshbabu C, Gupta OP, Gupta KK, Qasim M. Bilateral asymmetrical duplicated origin of vertebral arteries: Multidetector row CT angiographic study. Indian J Radiol Imaging. 2014;24:61-65. 69. Kiss J. Bifid origin of the right vertebral artery: a case report. Radiology. 1968;91:931. 70. Goddard AJ, Annesley-Williams D, Guthrie JA, Weston M. Duplication of the vertebral artery: report of two cases and review of the literature. Neuroradiology. 2001;43:477-480. 71. Kumar S, Kumar P. Truncus bicaroticus with aberrant right subclavian artery and origin of right vertebral from right common carotid artery. Surg Radiol Anat. 2014;36:829-831. 72. Epstein DA, Debord JR. Abnormalities associated with aberrant right subclavian arteries-a case report. Vasc Endovascular Surg. 2002;36:297-303. 73. Bergman R, Thompson S, Afifi A, Saadeh F. Compendium of human anatomic variation: catalog, atlas and world literature. Baltimore: Urban & Schwarzenberg; 1988. 74. Polguj M, Podgorski M, Jedrzejewski K, Topol M, Majos A. Fenestration and duplication of the vertebral artery: the anatomical and clinical points of view. Clin Anat. 2013;26:933-943. 75. Sim E, Vaccaro AR, Berzlanovich A, Thaler H, Ullrich CG. Fenestration of the extracranial vertebral artery: review of the literature. Spine (Phila Pa 1976). 2001;26:E139-E142. 76. Kendi AT, Brace JR. Vertebral artery duplication and aneurysms: 64-slice multidetector CT findings. Br J Radiol. 2009;82:e216-e218.
Conflicts of interest: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 10 August 2015; accepted 7 November 2015 Citation: World Neurosurg. (2015). http://dx.doi.org/10.1016/j.wneu.2015.11.018 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2015.11.018
Anomalous Origin of the Right Vertebral Artery: Incidence and Significance Tanmoy Kumar Maiti, Subhas Kanti Konar, Shyamal Bir, Anil Nanda, Hugo Cuellar
OBJECTIVE: Detailed knowledge about anatomic variations of the aortic arch and its multiple branches is extremely important to endovascular and diagnostic radiologists. It is often hypothesized that anomalous origin and distribution of large aortic vessels may alter the cerebral hemodynamics and potentially lead to a vascular pathology.
-
INTRODUCTION
METHODS: In this article, we describe a case of anomalous origin of the right vertebral artery, which was detected during an intervention. We further reviewed the available literature of anomalous origin of the right vertebral artery. The probable embryologic development and clinical significance are discussed.
he vertebral artery (VA) is classically described as the first branch of the ipsilateral subclavian artery (SCA). In angiographic or anatomic postmortem studies, the anomalous origin of the VA, either right or left or both, is mostly incidental. But the anatomy of the VA and its various anomalies may become relevant during endovascular intervention or neck surgery. Anomalous origin of the right vertebral artery (RVA) is less common than its counterpart. The present report describes a case of anomalous origin of the RVA and discusses the various anomalous origins of RVA described in the literature with their possible embryologic development processes.
-
RESULTS: The incidence of anomalous origin of a vertebral artery seems to be underestimated in recent literature. A careful review of the literature shows more than 100 such cases. The right vertebral artery can arise from the aortic arch or one of its branches. Dual origin of the vertebral artery is not uncommon. The embryologic developmental hypotheses are contradictory and complex.
T
-
CONCLUSIONS: Anomalous origin of the right vertebral artery may not be the sole reason behind a disease process. However, it can certainly lead to a misdiagnosis during diagnostic vascular studies. Detailed information is essential for any surgery or endovascular intervention in this location.
-
Key words Anomalous origin - Clinical significance - Embryologic development - Misdiagnosis - Right vertebral artery -
Abbreviations and Acronyms CCA: Common carotid artery CIA: Cervical intersegmental artery LCCA: Left common carotid artery LVA: Left vertebral artery LSCA: Left subclavian artery RCCA: Right common carotid artery RSCA: Right subclavian artery
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METHODS An exhaustive literature search was conducted using electronic databases (MEDLINE, EMBASE, CAB Abstracts, Current Contents, and Google Scholar) for relevant published articles. The search terms used were “anomalous origin of RVA” and “dual origin of RVA.” The resulting citations were exported, and the articles were screened independently by 2 authors (T.M. and H.C.) by reviewing the titles, abstracts and full texts. Bibliographies of identified publications and articles citing them were also examined. Both cadaver and clinical studies were included in the analysis. Data from identifiable papers are summarized in Table 1. Illustration of normal variant and anomalous origin of RVA has been depicted in Figure 1. The associated anomalies and clinical presentation/significance are shown in Table 1 where information was available.
RVA: Right vertebral artery SCA: Subclavian artery VA: Vertebral artery Department of Neurosurgery, Louisiana State University Health Sciences Center, Shreveport, LA, USA To whom correspondence should be addressed: Hugo Cuellar, M.D, Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2015). http://dx.doi.org/10.1016/j.wneu.2015.11.018 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
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ORIGINAL ARTICLE TANMOY KUMAR MAITI ET AL.
ANOMALOUS ORIGIN OF THE RIGHT VERTEBRAL ARTERY
Table 1. Anomalous Origin of the Right Vertebral Artery: A Systematic Review of 115 Cases Including the Present Case
Number
Study
Clinical Significance/ Presentation
Other Anomaly
Table 1. Continued
Number
Study
Other Anomaly
Clinical Significance/ Presentation
I. Origin as a single vessel I. Origin as a single vessel
10
Stoesslein et al., 198214
Coarctation
11
Lemke et al., 199915
None
None
12
Kodama, 200016 None
None
13
Karcaaltincaba LVA arises between the None et al., 200317 origins of the LCCA and LSCA
14
None Ligege and Scholtz, 200418
15
Goray et al., 200519
LVA from the aortic arch Evaluation of beyond the origin of the spondyloepiphyseal LSCA (fourth branch); dysplasia with CTA RVA was the fifth branch
16
Satti et al., 200720
None
17
Al-Okaili and Schwartz, 200721
LVA arising from aortic Incidental; evaluation arch between the LCCA of trauma; identified and LSCA with MRA
18
Higashi et al., 200822
Retro-esophageal course of the RVA
19
Hsu et al., 201023
LVA distal to the LSCA Thoracic aortic trauma (fourth branch); RVA was evaluation with CTA the fifth branch
20
None Dabus and Walker, 201024
Incidental; MRA
21
Uchino et al., 201325
None
Incidental
22
Lale et al., 201426
None
Incidental
23
Present case, 2015
None
Incidental
A. Originating from the aortic arch 1. RVA originating from the ascending aorta, just above the left coronary sinus 1
Akdeniz et al., 20071
Aberrant retroesophageal RSCA
Acute coronary syndrome; coronary angiography and MRA
2. RVA from aortic arch between the innominate artery and LCCA 1e4
Poynter, 19162
Proximal to distal: innominate artery, RVA, LCCA, LVA, and LSCA
NA
3. RVA from the aortic arch between the RSCA and RCCA in cases of missing brachiocephalic arteries 1e3
4
Poynter, 19162
Proximal to distal: RSCA, RVA, RCCA, LCCA, LVA, and LSCA
NA
NA
NA
Lippert and Pabst, 19853
4. RVA from aortic arch between the LCCA and LSCA None
CTA evaluation of RTA
1
Wasserman et al., 19924
2
Albayram et al., LVA fourth branch and Evaluation of SAH RVA fifth branch; distal 20025 right anterior cerebral artery aneurysm at the A2-A3 junction
5. RVA from the aortic arch distal to the origin of the LSCA 1
Kemmentmüller, Retro-esophageal course of the RVA 19116
2
Lie, 19687
NA
NA
3
ObounouAkong, 19694
NA
NA
4
Newton and Mani, 19748
NA
NA
5
Nakaba, 19769 Retro-esophageal course of the RVA
6
Argenson et al., 198010
NA
NA
7
Sakamoto, 198011
NA
NA
8
Schwarzacher and Krammer, 198912
LVA arising from the aortic arch between the LCCA and LSCA
NA
9
Takagi and Yamashita, 199213
Coronary sinus opening Cadaver study into the left atrium
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Evaluation of CVA with CTA
MRA evaluation of left cerebellar infarct
Cadaver study
B. Origin other than the aortic arch 1. RVA directly from the brachiocephalic artery
NA
Continues
2
NA
1
Daseler and Anson, 195927
NA
NA
2
Argenson et al., 198010
NA
NA
3
Lippert and Pabst, 19853
NA
NA
4
Yamaki et al., 200628
None
Cadaver study
2. RVA from the RSCA, distal to the right thyrocervical trunk 1
Koenigsberg et al., 200329
none
CTA evaluation of CAD Continues
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ORIGINAL ARTICLE TANMOY KUMAR MAITI ET AL.
ANOMALOUS ORIGIN OF THE RIGHT VERTEBRAL ARTERY
Table 1. Continued
Number
Study
Table 1. Continued
Other Anomaly
Clinical Significance/ Presentation
I. Origin as a single vessel
1
Iyer, 192730
ARSCA (arteria lusoria) (RSCA from the arch distal to the LSCA with a retro-esophageal course)
NA
2
Windel et al., 192831
ARSCA
NA
3
Newton and Mani, 19748
ARSCA
NA
4
Bernardi and Deton, 197532
ARSCA
NA
5e7
Palmer, 197733 ARSCA
NA
8
Tan and Spigos, ARSCA 197934
NA
9
Wackenheim ARSCA and Kleinclaus, 197935
NA
NA
10
Roszel and Keily, 199136
ARSCA
11
Chen et al., 199837
Nonopacification of the Incidental LVA, RSCA from the aortic arch, LSCA from the descending aorta distal to the origin of the RSCA
Other Anomaly
33
Park et al., 200844
ARSCA distal to the Incidental LSCA LVA originated from the aortic arch between the LCCA and the LSCA
34
Cheng et al., 200945
Aortic arch: proximal to CTA: anterior distal: RCCA, LCCA, communicating artery LSCA, and RSCA aneurysmal SAH
35
Cheng et al., 200945
Aortic arch: proximal to MRA evaluation of distal: RCCA, LCCA, apopsychia LSCA, and RSCA
36
Ishihara et al., ARSCA, persistent trigeminal artery 201146
Proximal to distal: RCCA, Evaluation of blurred LCCA, RSCA, and LSCA vision and dizziness
13
Koenigsberg et al., 200329
ARSCA
37e38 Uchino et al., 201325
ARSCA arising from the Incidental aortic arch distal to the left SCA
39
Nalamada et al., 201347
ARSCA
40
Nalamada et al., 201347
RCCA and ARSCA arose Left posterior directly from the aortic communicating aneurysm arch
14
Brouwer et al., ARSCA; LVA from the MRA evaluation of arch between the LCCA TIA 200439 and LSCA
15
Fazan et al., 200440
Proximal to distal at arch: RCCA, LCCA, LSCA, and RSCA
Cadaver study
16
Layton et al., 200641
ARSCA
Left MCA infarct
17
Ka-Tak et al., 200742
ARSCA; LVA from the Incidental aortic arch between the LCCA and LSCA ARSCA, LVA from the arch
Incidental
22e31 Tsai et al., 200743
ARSCA
Incidental
32
ARSCA distal to the LSCA
Incidental
Continues
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Ruptured left anterior choroidal aneurysm
1
Daseler and Anson, 195927
NA
NA
2
Koo and Sakai, 196648
NA
NA
3
Bernardi and Deton, 197532
Separate origin of Left hemiparesis RSCA and RCCA from arch; no brachiocephalic trunk
4
Bernardi and Deton, 197532
Separate origin of RCSA Ataxia and RCCA from arch; no brachiocephalic trunk; LVA from arch
5
Lippert and Pabst, 19853
6
Gluncic et al., 199949
LVA arising from the aortic arch
Incidental
7
Yanik et al., 200450
None
Doppler evaluation of subacute infarct in the right cerebral pedicle and cerebellar vermis
8
Ugurlucan et al., Both carotid arteries 200651 arising from the aortic arch as a common trunk
9
Uchino et al., 201325
Angiogram after MI
18e21 Tsai et al., 200743
Incidental
4. RVA from the RCCA without arteria lusoria
Best and Bumpers, 200238
Park et al., 200844
Study
I. Origin as a single vessel
3. RVA from the RCCA with anomalous right SCA
12
Number
Clinical Significance/ Presentation
NA
None
NA
Evaluation for TIA
Incidental
Continues
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ORIGINAL ARTICLE TANMOY KUMAR MAITI ET AL.
ANOMALOUS ORIGIN OF THE RIGHT VERTEBRAL ARTERY
Table 1. Continued
Number
Table 1. Continued
Study
Other Anomaly
Clinical Significance/ Presentation
I. Origin as a single vessel
Adachi and Das, 192852
NA
Matula et al., 199753
None
Melki et al., 201267
None
Vertebrobasilar CAD, pseudodissecting aneurysm in right VA
16
Uchino et al., 201325
None
None
Incidental
17
Rameshbabu et al., 201468
Dual origin of LVA (the CTA evaluation of medial limb from arch dizziness and the lateral limb from LSCA)
7. RVA from the right internal carotid artery via the hypoglossal artery 1
Other Anomaly
15 NA
6. RVA from external carotid artery 1
Study
I. Origin as a single vessel
5. RVA from the thyrocervical trunk 1
Number
Clinical Significance/ Presentation
NA
Keller and Weiss, 197354
NA
2. Dual origin from the RSCA and the brachiocephalic artery
II. Dual origin
1
Kiss, 196869
1. Dual origin from the RSCA 1
Lie, 19687
Not known
2
Babin and Haller, 197455
Elongation of RVA; dolichoarterial loop of LVA
NA Epilepsy
Paresthesia of right arm
3. Dual origin from the RSCA and the right CCA
3
Argenson et al., 198010
NA
NA
4
Rath and Prakash, 198456
NA
5
Harada et al., 198757
Hypoplastic LVA
Evaluation of dizziness
6
Hashimoto et al., 198758
None
Temporal and cerebellar infarction
7
Nishijima et al., 198959
NA
Evaluation of dizziness
8
Cavdar and Arison, 198960
NA
NA
9
Takasato et al., Rudimentary LVA, Brainstem infarction 199261 accessory artery that arose from a branch of the left thyrocervical trunk
1
Goddard et al., None 200170
2
Kumar and Kumar, 201471
Cadaver study
NA
10
Nogueira et al., 199762
11
Dual origin of LVA both MRA evaluation of Ionete and cognitive impairment Omojola, 200663 from LSCA
12
Harnier et al., 200864
Duplication of the RCCA MRA evaluation of fenestration of the LCCA dizziness
13
Thomas et al., 200865
Midbasilar trunk aneurysm
14
Mordasisni, 200866
Dual origin of LVA (1 MRA evaluation of limb from the aortic arch MCA stroke and the other from the LSCA)
None
MRA evaluation of TIA
Common origin of both None the CCA (first major branch of the aortic arch)
4. Dual origin from the RSCA and the right thyrocervical trunk 1
NA
LCCA from brachiocephalic artery, LVA from aortic arch, double axillary artery
NA
Lippert and Pabst, 19853
NA
5. Dual origin from the RSCA and aortic arch distal to the LSCA 1
Hsu et al., 201023
None
Diagnosed with CTA to evaluate a previously placed stent graft
6. Dual origin of RVA, site not mentioned LVA arising from the aortic arch
1
Cavdar et al., 198960
2
Goddard et al., None 200170
Cadaver study Incidental MRA evaluation of left MCA stroke
RVA, right vertebral artery; RSCA, right subclavian artery; MRA, magnetic resonance angiography; LCCA, left common carotid artery; LVA, left vertebral artery; LSCA, left subclavian artery; NA, not available; RCCA, right common carotid artery; CTA, computed tomography angiography; RTA, renal tubular acidosis; SAH, subarachnoid hemorrhage; CVA, cerebrovascular disease; SCA, subclavian artery; ARSCA, aberrant right SCA; MI, myocardial infarction; TIA, transient ischemic attack; MCA, middle cerebral artery; CAD, coronary artery disease; VA, vertebral artery; CCA, common carotid artery.
Continues
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ORIGINAL ARTICLE TANMOY KUMAR MAITI ET AL.
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ANOMALOUS ORIGIN OF THE RIGHT VERTEBRAL ARTERY
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Figure 2. Images of the present case. (AeC) Digital subtraction angiogram. (A) Innominate artery roadmap. Right vertebral artery (RVA) is not seen to arise from the right subclavian artery (arrow). (B) RVA (white arrows) originating directly from the arch of the aorta, distal to the origin of the left subclavian artery
(black arrow). (C) RVA (white arrow) has a retro-esophageal course, left vertebral artery (black arrow). (DeG) Computed tomography angiogram: coronal view of the neck from posterior to anterior: RVA (arrows) is seen to arise directly from the aortic arch and has a retro-esophageal course.
CASE REPORT
DISCUSSION
A 56-year-old man presented with dysphagia, odynophagia, hoarseness of voice, and significant weight loss. On subsequent evaluation, he was found to have supraglottic carcinoma. He underwent a total laryngectomy, total glossectomy, and bilateral neck dissection, and he received chemoradiation. After 4 months, he developed hematemesis. He was scheduled for embolization of the residual mass. During the angiogram, an anomalous origin of the RVA was noted. It was found to originate directly from the aortic arch as the last branch (fourth branch) and have a retro-esophageal course. The left vertebral artery (LVA) originated normally from the left subclavian artery (LSCA) (Figure 2).
Both the right and left vertebral arteries usually arise from the posterosuperior aspect of the first part of the SCA. They extend inward and upward to the transverse process of C6, pass through the foramina of all of the upper cervical transverse processes, curve medially behind the lateral mass of the atlas, and then enter the cranium through the foramen magnum. Anomalous origin of the RVA is underestimated in recent literature. An aberrant right subclavian artery (RSCA) is the most common vascular ring anomaly in the aortic arch, with a reported incidence of 0.5%e2%.72 Thus, it can be argued that the RVA is anomalous when it originates from an aberrant SCA. In this article, we limit our discussion to the anomalous point of origin of the
= Figure 1. (A) Origin of the right vertebral artery (RVA) from the right subclavian artery (RSCA): normal variant. (BeM) Origin of the RVA as a single vessel: RVA from the ascending aorta (B) (n ¼ 1), aortic arch between the RSCA and the right common carotid artery (RCCA) (C) with missing brachiocephalic artery (n ¼ 4), brachiocephalic artery (D) (n ¼ 4), brachiocephalic artery, and left common carotid artery (E) (n ¼ 4), left common carotid artery and left subclavian artery (LSCA) (F) (n ¼ 2), distal to the LSCA (G) (n ¼ 23), RSCA distal to the right thyrocervical trunk (H) (n ¼ 1), RCCA with normal RSCA (I) (n ¼ 9), RCCA with aberrant RSCA (J) (n ¼ 40), right thyrocervical trunk (K) (n ¼ 1), right internal carotid artery (L) (n ¼ 1), and right external carotid artery (M) (n ¼ 1). (NeR) Dual origin of RVA: both originating from the RSCA (N) (n ¼ 17), RSCA and brachiocephalic artery (O) (n ¼ 1), RSCA and right thyrocervical trunk (P) (n ¼ 1), RSCA and RCCA (Q) (n ¼ 2), RSCA and arch distal to the LSCA (R) (n ¼ 1).
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ORIGINAL ARTICLE TANMOY KUMAR MAITI ET AL.
ANOMALOUS ORIGIN OF THE RIGHT VERTEBRAL ARTERY
RVA. Cases where the origin of RVA was from an aberrant SCA have not been included in the present discussion. We also excluded cases where the VA was missing. Origin of RVA as a Single Vessel VA origin can be divided into 2 groups: those originating from the aortic arch (n ¼ 34) and those originating neither from the arch nor the SCA (Table 1).1-54 Origin from the ascending aortic arch seems to be the rarest of all and is described only once in the literature,1 where it is associated with acute coronary syndrome. In his comprehensive review in 1916, Poynter2 recorded 31 cases of aortic arches with 5 branches and 4 with 6 branches. In 7 of these 35 specimens, both VAs arose from the aortic arch. The aortic branching pattern, in a proximal to distal progression, was as follows: (1) innominate artery, RVA, left common carotid artery (LCCA), LVA, and LSCA (4 cases) or (2) RSCA, RVA, right common carotid artery (RCCA), LCCA, LVA, and LSCA (3 cases). One similar case has been described by Lippert and Pabst,3 where the RVA originated from the aortic arch between the RSCA and the RCCA in cases of missing brachiocephalic arteries. Origin between the LCCA and the LSCA is another rare variation and has been documented only twice.4,5 The most common anomalous origin of the RVA occurs from distal to the origin of the LSCA. In these cases, the RVA represents the last branch of the aortic arch. In most of these cases, the RVA took a retro-esophageal course to reach its entry into the vertebral foramen. In contrast, anomalous origin of the RVA from other vessels has been noted in more than 50 occasions. It may originate directly from the brachiocephalic or innominate artery instead of the RSCA. In one case, it was noted to arise from the RSCA distal to the right thyrocervical trunk instead of being the first branch.29 Most commonly, they originate from the RCCA (n ¼ 49). In most cases, the RSCA has an anomalous origin. The RSCA is the last branch of the aortic arch and has a retro-esophageal course, known as arteria lusoria. In a study of 102 patients with aberrant RSCA, Tsai et al.43 found a VA anomaly in 15.7% of patients. Interestingly, when one VA had an anomalous origin, the incidence of a VA anomaly on the other side increased.43 Dual origin of the RVA The term “duplication” has been erroneously used interchangably with “fenestration” (Table 1).3,7,10,23,25,55-71 The term “duplication” describes the dual origin of a VA with a variable fusion at the neck. In contrast, the term “fenestration” is used to describe the single origin of a vessel with 2 parallel segments anywhere along the course. Duplication of the VA is much rarer than a fenestration.70 The frequency was identified as 0.72% in one cadaver study.73 In that study, 5 of 693 specimens had dual origin of the VA and, incidentally, all were left sided.73 The incidence seems to be more common on the left side.68 In most of these cases, both origins were from the RSCA. In other cases, 1 was from the RSCA, and others were either from the brachiocephalic artery, the RCCA, the right thyrocervical trunk, or the arch of the aorta. This pattern of origin is different from the LVA, where the lateral crus starts from the LSCA and the medial starts from the aortic
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Figure 3. Normal schematic diagram of the primitive ventral and dorsal aorta, 6 aortic arches, dorsal aortic root segments (DARS), and dorsal intersegmental arteries (DISA) (modified from Satti et al.20 and Higashi et al.22). CA, ascending cervical artery; SCA, subclavian artery; VD.
arch. Bilateral dual origin of the VA is exceedingly rare and has been reported only 3 times.68 Embryology The embryology of the VA is complex, and several hypotheses have been described in the literature (Figures 3 and 4). Accordingly, the explanations are different for the development of the various anomalies. Knowledge of the development of the aortic arch, the brachiocephalic artery, and the SCA is also important to understand the association. At the initial stage of development there are 2 aortic trunks (ventral and dorsal aorta). The primitive ventral aorta persists bilaterally. The right forms the innominate artery (brachiocephalic artery) and the right common and right external carotid arteries. The left gives rise to a short portion of the aortic arch, the left common carotid arteries, and left external carotid arteries. The earliest development of the VA is apparent when the embryo is at the 7-mm stage. The developmental process is usually complete by the 14- to 17-mm stage.8,37 At the 7-mm stage (day 32), 7 cervical intersegmental arteries (CIAs) appear, originating from each of the paired dorsal aortae accompanying the cervical segmental nerves 2e8.65,74 At the 10- to 12-mm stage,
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ORIGINAL ARTICLE TANMOY KUMAR MAITI ET AL.
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Figure 4. Normal schematic diagram demonstrating the embryologic origins of the arch and its major branches. LEC, left external carotid artery; LIC, left internal carotid; REC, right external carotid artery; RIC, right internal carotid artery (modified from Satti et al.20).
a longitudinal anastomosis develops between the CIAs. At the 14- to 17-mm stage, the horizontal parts of the first 6 CIAs disappear, and the remaining seventh CIA becomes part of the SCA.8,37 On the left side, the entire proximal LSCA to the level of the internal thoracic artery results from the persistent left seventh dorsal intersegmental artery. On the right, the seventh dorsal intersegmental artery forms the distal one third of the proximal RSCA. The proximal and midzones of the proximal RSCA are formed by the right fourth aortic arch and segments 3e7 from the right dorsal aortic root.20 Segments 3e7 from the left dorsal aortic root form a small segment of the aorta at the origin of the LSCA.20 Most authorities believe that the VA originates from the persistent longitudinal anastomosis of CIAs, which persists after involution of the horizontal segments.8,37 Some authorities believe that the VA arises from the distal aspect of the seventh dorsal intersegmental artery20 (sixth according to some70). These developmental processes result in a normal origin of the VA from the SCA. A detailed review of the literature suggests that an anomalous origin of the VA is more common on the left side than the right. It is difficult to explain those anomalies. However, we discuss the more common types. Failure of involution in one of the first 6 CIAs (ie, a persistent CIA) causes a variety of abnormal origins of the VA. If the persistent CIA occurs in the upper (first or second) intersegmental arteries, the result is an abnormal origin of the VA from the internal or external carotid artery. If it occurs in the lower (third to sixth) CIAs, the result is an abnormal origin of the VA from the aortic arch or the common carotid artery (CCA).6,13 The second occurrence is the more common.
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The origin of the RVA as the last branch of the aorta distal to the LSCA can result from persistence of the right dorsal aorta and the obliteration of the right fourth arch. According to some reports, it can result from persistence of the C8 intersegmental artery.23 The incidence of anomalous origin of the RVA from the RCCA (VA-CC) is 0.18%.33 Two different embryonic mechanisms for VACC have been described.37,39,47 In the first (type I), the sixth CIA develops into the VA with degeneration of the anastomosis between the sixth and seventh CIAs. The aberrant SCA results from the involution of the ipsilateral middle dorsal aorta and the remaining ipsilateral seventh CIA connecting to the contralateral (left) dorsal aorta. The anterior spinal artery is ipsilateral in type I. The second (type II) also has a persistent lower CIA, but instead of an involution of the ipsilateral middle dorsal aorta, the persistent CIA migrates upward to the level of the CCA. Type I anomaly does not occur on the left side as the condition is incompatible with life. There are multiple explanations for dual origin of VA. It may occur when a portion of the primitive dorsal aorta persists along with 2 intersegmental vessels connected to the true VA.75 Another possible explanation is failure of regression of the fifth or sixth intersegmental arteries, which adds a further possible origin to the VA along with the normal seventh segment.76 Significance: Are they Always Incidental? In most cases, the anomalous origin of the VA is an incidental finding. Many patients were diagnosed after evaluation for dizziness. Some authors4,15 have hypothesized that an anomalous origin and the distribution of the VAs might result in cerebral hemodynamic perturbation with secondary cerebral changes. However, conclusive evidence is lacking to support such a hypothesis. Koenigsberg et al.29 found anomalous origin of the VA in 2 cases of vertebral insufficiency. However, as the authors rightly pointed out, the anomalous origin of the VA cannot be concluded to be the only reason behind the presentation. Palmer33 suggested that atheromatous disease of the proximal CCA might be considered to be of more hemodynamic significance in the presence of this anomaly. Multiple cases of coexisting pathologies can occur, for example, aneurysm,5,45,47 arterial infarct,20,50,61 transient ischemic attack,70 arachnoid cyst,63 and hereditary connective tissue disorder, such as Ehlers-Danlos syndrome.74 However, the knowledge of variants of VA origin appears to be mandatory for planning aortic arch surgery or endovascular interventions. Anomalous VA origin also represents a potential pitfall in the diagnosis of cerebrovascular injury. One or both VAs may be wrongly assumed to be occluded or diseased, either by eluding catheterization during angiography or by lying outside the region of interest during noninvasive studies such as computed tomography angiography, magnetic resonance angiography, or Doppler sonography. A surgeon using bypass techniques should be aware of this anomaly to avoid inducing vertebra-basilar ischemia while clamping the carotid artery. If a right brachial or transaxillary angiogram fails to identify the vertebral anomaly, its presence should be excluded by alternative techniques.
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Patients with dual origin of VA may be predisposed to damage in severe cervical spine injuries because of the additional point of attachment. Polguj et al.74 suggested that the lumen of a duplicated VA is smaller than normal. This may cause difficult catheterization and misinterpretation as hypoplastic VA. Some authors have suggested that dual origin can contribute to vertebral dissection.67 A comparative analysis suggests that the incidence of vertebral dissection is more common in cases with VA fenestration than VA duplication.74 Therefore, these 2 entities should be distinguished. Even though conventional intra-arterial digital subtraction angiography remains the gold standard method for imaging the VAs, noninvasive modalities such as ultrasonography, multislice computed tomography angiography, and magnetic resonance
REFERENCES
angiography are constantly improving and can play an increasingly important role in diagnosing VA pathology in clinical practice. CONCLUSIONS Anomalous origin of RVA is rarer than LVA. The plausible embryologic explanation is often difficult to understand. Although these findings may be incidental in most cases, detailed information is required before any surgical/endovascular intervention to avoid any misinterpretation and inadvertent injury to VA. ACKNOWLEDGMENT We thank Mr. David Wright for help and contribution to the illustrations in this article.
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Conflicts of interest: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 10 August 2015; accepted 7 November 2015 Citation: World Neurosurg. (2015). http://dx.doi.org/10.1016/j.wneu.2015.11.018 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
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