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Unilateral Aplasia versus Bilateral Aplasia of the Vertebral Artery: A Review of Associated Abnormalities.

1. Introduction

The development of paired vertebral arteries (VAs) of 7 mm to 12 mm of the human embryo provides longitudinal anastomoses of so-called primitive proatlantal intersegmental artery (PIA) and six cervical intersegmental arteries (CIAs) that arise from the dorsal aorta on both sides. Actually, the sixth CIA according to Padget [1], or the seventh CIA according to Effmann et al. [2], becomes the VA and contributes to the subclavian artery (SA) in this embryonic stage, while the primitive PIA also supplies a caudal part of precursors of the basilar artery (BA), that is, paired longitudinal neural arteries (LNAs) on the developing hindbrain. After this period, the VA from its origin courses through prevertebral (V1), cervical (V2), atlantic (V3), and intracranial (V4) topographical parts before its connection with opposite artery in the BA [3].

The development of the internal carotid artery (ICA) is independent of the VA. Namely, only one part of the primitive ICA derives from the third primitive aortic arch, while all other ICA segments represent cranial extensions of the dorsal aorta on both sides. Transitory vascular channels or primitive carotid-vertebrobasilar anastomoses (CVBAs) between the LNAs and ICAs exist at a time when embryonic length is 4-5 mm [4-8]. The primitive hypoglossal (PHA), primitive otic (POA), and primitive trigeminal (PTA) arteries are determined, as cited [5-8], by their relationship with hypoglossal nerve, otic vesicle, and trigeminal ganglion, respectively, while the PIA is named according to the course between the occipital and cervical somites [1, 6]. With the formation of the posterior communicating artery (PCoA) cranially and vertebrobasilar system caudally, CVBAs regress and usually disappear by the 14 mm stage of human embryo.

Doppler sonography of health infants showed that 114/7991 (1.4%) infants had unilateral VA aplasia--left in 0.51% and right in 0.91% of cases [9]. The persistence of CVBA(s) in cases of uni- or bilateral aplasia of the VA or in cases of normal VA on both sides after this period is conditioned by different vascular factors and however insufficiently explained [5-8,10].

Recent finding of aplasia of the right VA followed by the persistence of the left PTA and so-called intermediate communicating artery on the right side inspired the authors to review literature cases with established uni- and bilateral VA aplasia and their relationships with persistence of primitive or definitive anastomoses and/or vascular variants.

2. Methods

Morphological characteristics of 108 cases of total uni- and bilateral aplasia of the VA in single reports or images of retrospective studies published between 1967 and 2016 are separately analyzed. We included one personal case, as well as literature cases in articles available on Google display network or in the library archive of our Faculty of Medicine. Five general parameters, incidence, gender, persistence of CVBA, other associated vascular variants, and associated vascular pathology, in each group of uni- and bilateral VA aplasia are mutually compared.

So-called intermediate communicating artery (ICoA) is defined according to its schematic presentation in the book of Microneurosurgery [11] and previous findings in the fetuses [12] and adult cadavers [13].

2.1. Patient Population. 31/108 (28.70%) cases of bilateral VA aplasia, 46/108 (42.59%) cases of the left VA aplasia, and 31/108 (28.70%) cases of the right VA aplasia including recent one were selected. All cases belonging to different populations, gender, and age in appropriate tables are classified (Tables 1-3).

2.2. Statistical Analysis. The incidences of all cases of uniand bilateral VA aplasia in appropriate tables were noted; statistical test, [chi square] nonparametric test, was used. Statistical significance was noted in a case of p < 0.05. Statistical analysis was performed using statistical software of IBM Corp., released in 2011, and IBM SPSS Statistics for Windows, Version 20.0, IBM Corp., Armonk, NY.

3. Theoretical Background

3.1. Bilateral VA Aplasia. There are cases without data about gender and 11/31 female and 19/31 male cases of bilateral VA aplasia; age of these cases ranged from 14 days to 76 years.

Initial symptoms or reasons of discovery of 31 cases of bilateral VA aplasia were different and unspecified. Among primary symptoms, a headache in 6/31 cases [14-19], vertigo in 5/31 cases [20-24], and weakness in 4/31 cases [25-28] preceded the discovery of VA aplasia.

Although some primitive CVBA(s) persisted in 29/31 cases, there were bilateral findings for persistent PHA (PPHA) in one [29], persistent PTA (PPTA) in two [19, 27], and persistent PIA (PPIA) in eight cases [15, 19, 24, 25, 28, 30-32]; a simultaneous presence of bilateral PPIAs and left PPTA in one case was documented [19]. Unilaterally, CVBA persisted in 19 of cases (10 on the left and 8 on the right side); there was no data about the side of the PPHA in 1 out of 19 cases [33]. A persistence of CVBA was as follows: (1) PIA persisted 17 times--8 bilaterally, 5 on the left side, and 4 on the right side [14,15,17,19, 20, 22-25, 28, 30-32, 34-37]; (2) PHA persisted 10 times--1 bilaterally, 5 on the left side, 3 on the right side, and 1 without data [16, 21, 26, 29, 33, 3842]; (3) PTA persisted 3 times--1 bilaterally, 1 on the left side (associated with bilateral PPIAs), and 1 on the right side [19, 27, 43].

Two cases of associated arterial anastomoses and bilateral VAs aplasia were exceptions. Namely, Tsai et al. [18] have described that the left occipital-vertebral anastomosis enabled posterior circulation in a 36-year-old male, while Pauliukas [44] presented the BA in continuation of the left occipital artery (OA) on an angiogram.

CVBAs were only vascular variants associated with bilateral VA aplasia in 18/31 cases.

Otherwise, associated aplasia of other vessels was related to the PCoA that was found bilaterally in 3/31 cases [20, 33, 41] and unilaterally in 1 out of 31 cases [23], as well as to the BA also in one case [43], and to some dural sinuses simultaneously with bilateral internal jugular veins in another case [30].

Other associated vascular variations in 13/31 cases were found, mostly in the form of unusual side branches or fetal origin of the posterior cerebral artery (PCA) or additional anastomoses. So, the BA as a continuation of the left OA [44], the OA as a branch of the PPIA [25], or the posterior inferior cerebellar artery (PICA) as BA branch [21, 25] or PPHA branch [33] was described. Fetal origin of the PCA [23, 43] and anastomoses with thyrocervical and/or OA branches [22, 27] in two particular cases were found. Enlargement of some dural sinuses and Galen's vein malformation [30], hypoplasia of bilateral posterior communicating arteries [42], irregular caliber of ICA [14], or tortuous course of the PPHA [41] was found in single cases.

Vascular pathology was noted in 16/31 cases. Aneurysms of different arteries, BA [16, 42], anterior communicating artery [16, 17, 33], ICA [43], PPHA [41], as well as stenosis of carotid arteries [20, 23, 27, 31-33, 35, 38, 42], or cerebral infarction [18, 25, 27] among them, angiographically were confirmed.

3.2. Single Left VA Aplasia. There were 24/46 female cases and 20/46 male cases and no data for 2 cases of single left VA aplasia; age of these cases ranged from the stillborn to the 83-year-old ones.

Initial symptoms or reasons of discovery of 46 cases of the left VA aplasia were also different and unspecified. A headache in 10 cases [45-54], cavernous hemangioma in 7 cases [55, 56], and vertigo in 4 cases [57-60] were relatively frequently evidenced.

Primitive CVBA(s) persisted in 40/46 cases, mostly unilaterally, that is, in 35 cases on the left side, 3 cases on the right side [54, 56], and 2 cases on both sides [46, 61]. Two cases of single left VA aplasia were associated with the persistence of two CVBAs also on the left side [62, 63]. A persistence of CVBA was as follows: (1) PIA persisted 20 times on the left side [30, 45, 47, 50, 53, 57, 59, 62-73], whereby it had a common trunk with PPHA at origin in one case [62], and was associated with the left PPTA in the second case [63]; (2) PHA persisted 16 times (as a single vessel in 13 cases, bilaterally in 2 cases, and as a common trunk with PPIA in one case) [46, 48, 49, 51, 52, 55, 60-62, 74-79]; (3) PTA persisted 6 times--3 cases on the left (simultaneously with the left PPIA in one case) [56, 63, 80] and 3 cases on the right side [54, 56].

CVBAs were only vascular variants associated with the left VA aplasia in 30/46 cases.

Associated aplasia of other vessels was related to the left ICA in 3 cases [56, 81], to the PCoA in 8 cases, 4 times on the left side [47, 60, 74, 75] and bilaterally in 4 cases [48, 52, 63, 79], to the left anterior inferior cerebellar artery (associated with the left PCoA aplasia) in one case [75], to the right anterior cerebral artery in one case [65], and to the left common carotid artery (CCA) simultaneously with subclavian artery (SA) in one case [81].

Other associated vascular variations in 34/46 cases were found, mostly in the form of arterial hypoplasia or unusual origin and/or branches and/or termination. Associated hypoplasia of the right VA in 16/46 cases was documented (Table 4), whereas its hyperplasia was only in two cases [54, 56]. Associated unusual branches were in 8/46 cases [30, 48, 56, 61, 63, 73, 75], while a termination of the right VA as the PICA in 5/46 cases [47, 63, 66, 70, 79] and arteriovenous malformation in 4/46 cases [49,51,53,64] were also noted. Some congenital anomalies in 7/46 patients were reasons of discovery of the left VA aplasia [30, 56, 61, 81].

Vascular pathology in 24/46 cases was noted; aneurysms of different arteries, ICA [57, 81], PCA [64], PICA [45], PPHA-PICA junction [48], PPHA-BA junction [52], ACA [52], SA [65], as well as stenosis of ICA [60, 67, 70, 78], CCA [66, 78], PPHA [78, 79], or SA [65, 69] and cerebral hemorrhagic lesions [46, 61, 65, 68, 69, 74], angiographically were confirmed.

3.3. Single Right VA Aplasia. There were 14/31 female cases, 14/31 male cases, and 3/31 cases without data about gender of single right VA aplasia; age of these cases ranged from 4 days to 79 years.

Initial symptoms or reasons of discovery of 31 cases of the right VA aplasia were also different and unspecified. Among primary symptoms, a headache in 5 cases [75,82-85], weakness in 4 cases [86-89], or vertigo in 3 cases [90-92] was evidenced.

Primitive CVBA(s) persisted in 25/31 cases, mostly unilaterally, that is, on the right side (21/25), except 4 cases of its persistence on the left. A persistence of CVBA was as follows: (1) PIA persisted 5 times--4 on the right [85, 92-94] and 1 on the left side [91]; PHA persisted 16 times--15 on the right [40, 82-84, 87, 95-104] and 1 on the left side [75]; PTA persisted in a case described by Moller-Hartmann et al. [90] and in recent case (Figure 1); unnamed right external carotidvertebral anastomosis persisted in one case [89], "unusual" right CVBA in another case [88], and ICoA in the recent case (associated with the left PPTA).

Associated aplasia of other vessels was related to the ICA on the right side in one case [105] and on the left side in the second case [106], bilateral external carotid arteries (ECAs) in one case [92], right SA branches in one case [107], BA in one case [90], unilateral PCoA in 4 cases including recent case [75, 93, 96], and bilateral PCoAs in three cases [87, 88, 99] and the right ACA (associated with bilateral PCoA aplasia) in one case [88].

Other associated vascular variations in 23/31 cases are found, mostly in the form of arterial hypoplasia or unusual origin or course and/or branches and/or termination. Associated hypoplasia of the left VA in 13/31 cases was documented (Table 5). Variable origin of some arteries in 5/31 cases including recent one was found [88, 92, 95,105]. Associated unusual branches or termination of arteries in 9/31 cases including the recent one [75, 83, 86, 88, 90, 92, 94,107] was documented.

Vascular pathology in 20/31 cases was noted. Aneurysms of different arteries, middle cerebral artery [83, 94], both anterior choroidal arteries [85], VA [108], PPHA [82], BA [99], posterior inferior cerebellar artery [103], or multiple cerebral arteries [101], usually in single cases were discovered. Stenosis of ICA in 8/31 cases was found [84, 87, 90, 93, 95, 96, 104, 105]. Occlusion of some cerebral arteries was also evidenced in 5/31 cases [89, 95, 96, 99,100].

3.4. Single Left VA versus Bilateral VA Aplasia. Calculated incidences of selected morphological parameters in Table 6 are presented.

(1) Incidence was as follows: single left VA aplasia was more common than bilateral VA aplasia.

(2) Gender was as follows: although female gender was frequent in cases of single left VA aplasia, male gender was more frequent in cases of bilateral VA aplasia; generally, there was no significant sex difference in cases of the left VA aplasia, either single or associated with the right VA aplasia.

(3) Persistence of CVBA was characteristic as follows: (A) there was significant incidence of unilateral persistence of CVBA in cases of both single left and bilateral VA aplasia, especially in cases of single left VA aplasia; (B) as bilateral CVBA persisted in one-third of cases of bilateral VA aplasia, one can say that this bilateral persistence was not the rule; (C) low incidence of persistence of two different CVBAs in both single left and bilateral VA aplasia was found; (D) PIA persisted in about one-half of the cases; however, it was more common in cases of bilateral VA aplasia; (E) PHA persisted in one-third of cases of both single left and bilateral VA aplasia; and (F) PTA persisted in both single left and bilateral VA aplasia with almost equal (low) frequency.

(4) Additional vascular variants were as follows: (A) aplasia of different arteries, CCA, ICA, ACA, PCoA, anterior inferior cerebellar artery [AICA], or SA, followed single left VA aplasia, while aplasia of only PCoA and BA was followed by bilateral VA aplasia; (B) absence of some dural sinuses and internal jugular veins only in one case of bilateral VA aplasia was associated; (C) one-third of cases of hypoplastic right VA with the left VA aplasia were associated; and (D) more than one-third of cases of other vascular variants, such as unusual origin or side branches or termination or additional anastomoses with single left VA and bilateral VA aplasia, were associated.

(5) Associated vascular pathology was presented as follows: (A) aneurysms of different definitive cerebral arteries in one-fifth of cases of bilateral VA aplasia were found; (B) rare aneurysms of CVBAs characterized cases of single left and bilateral VA aplasia; (C) there was high incidence of other cerebral pathology (stenosis or occlusion or cerebral infarction or stroke) in cases of single left and bilateral VA aplasia; and (D) low incidence of noncerebral pathology characterized only cases of single left VA aplasia.

3.5. Single Right VA versus Bilateral VA Aplasia. Calculated incidences of selected morphological parameters in Table 7 are presented.

(1) Incidence was as follows: right VA aplasia was more common when associated with left VA aplasia than when it was a single abnormality.

(2) Gender was as follows: although female gender was frequent in cases of single right VA aplasia while male gender was more common in cases of bilateral VA aplasia, generally, male gender was more common in cases of both single right and bilateral VA aplasia.

(3) Persistence of CVBA was characteristic as follows: (A) there was significant incidence of unilateral persistence of CVBA in cases of both single right and bilateral VA aplasia, especially in cases of single right VA aplasia; (B) bilateral persistence of CVBA in cases of single right VA aplasia was not found; it was significant in cases of bilateral VA aplasia; (C) there was no persistence of two different CVBAs in cases of single right VA aplasia, while they persisted with low incidence in cases of bilateral VA aplasia; (D) there was significant persistence of PIA in cases of bilateral VA aplasia in regard to single right VA aplasia; (E) there was persistence of PHA in one-half of cases of single right VA in regard to one-third of cases of bilateral VA aplasia; (F) PTA persisted in both right and bilateral VA aplasia with almost the same (low) frequency; and (G) there was, also, low frequency of persistence of additional arterial anastomoses in cases of both single right and bilateral VA aplasia.

(4) Additional vascular variants were as follows: (A) aplasia of different arteries, ECA, ICA, ACA, PCoA, BA, and SA branches, characterized single right VA aplasia, while aplasia of only two arteries (BA and PCoA) was associated with bilateral VA aplasia; (B) associated unilateral PCoA aplasia was more common in cases of single right VA aplasia; (C) there were about one-half of the cases of hypoplastic left VA in cases of aplasia of the right VA; and (D) different vascular variants in one-third of cases of single right VA aplasia were associated, while they were more frequent in cases of bilateral VA aplasia.

(5) Associated vascular pathology was presented as follows: (A) aneurysms of definitive arteries were more common in cases of single right VA aplasia than in cases of bilateral VA aplasia; (B) aneurysms of CVBAs were rare findings in cases of single right and bilateral VA aplasia; (C) other cerebral pathology in one-third of cases of single and bilateral VA aplasia was discovered; and (D) low incidence of noncerebral pathology in cases of single right and bilateral VA aplasia was found.

3.6. Single Left VA versus Right VA Aplasia. Calculated incidences of selected morphological parameters in Table 8 are presented.

(1) Incidence was as follows: single left VA aplasia was more common than single right VA aplasia.

(2) Gender was as follows: although female and male gender were more common in cases of left VA aplasia than in cases of right VA aplasia, there was no significant sex difference in cases of unilateral VA aplasia.

(3) Persistence of CVBA was characteristic as follows: (A) incidence of persistence of CVBA was high and almost equal in both cases of unilateral VA aplasia, but not as an absolute rule; (B) CVBA always presented if one VA is aplastic and the other VA is hypoplastic;

(C) there was no bilateral persistence of CVBAs in cases of single right VA aplasia, while it was rare finding in cases of single left VA aplasia; (D) there was no persistence of two different CVBAs in cases of single right VA aplasia, while it was a possible (rare) finding in cases of single left VA aplasia; (E) PIA persisted more frequently in cases of single left VA aplasia; (F) PHA persisted in one-third of cases of single left VA aplasia and in one-half of cases of single right VA aplasia; (G) although PTA persisted with low incidence in cases of single left VA aplasia, it was twice more often than on the right side; and (H) there were no additional vascular anastomoses in cases of single left VA aplasia, while they were rare findings in cases of single right VA aplasia.

(4) Additional vascular variants were as follows: (A) aplasia of the same four arteries, CCA, ICA, ACA, and PCoA, for both cases was characterized; aplasia of the AICA and SA was specific for single left VA aplasia, while aplasia of BA and SA branches was specific for single right VA aplasia; (B) there were more than one-third of cases of hypoplastic VA associated with aplasia of opposite VA; (C) the left VA was more commonly hypoplastic in cases of single right VA aplasia than the right VA in cases of single left VA aplasia; (D) characteristic finding was associated aplasia of other arteries in 8/16 and 6/13 cases, respectively, of mutual aplasia of one VA and hypoplasia of the other VA; and (E) associated vascular variants (except those of a vessel's aplasia and presence of CVBA) in one-third of cases of single left or right VA aplasia were presented.

(5) Associated vascular pathology was presented as follows: (A) aneurysms of definitive arteries were more frequent in cases of single right VA aplasia than in cases of single left VA aplasia; (B) aneurysms of CVBAs were rare findings in both cases of unilateral VA aplasia; (C) different cerebral pathology in cases of single left and right VA aplasia in more than one-third of cases was documented; and (D) low incidence of noncerebral pathology, especially in cases of single left VA aplasia, was noted.

3.7. Uni- and Bilateral VA Aplasia versus Persistence of CVBA. Generally, a relationship of the VA aplasia and persistence of CVBA was as follows: (A) the side of the VA aplasia has significant influence on the side of CVBA persistence (p < 0.001); (B) CVBA is significantly more common on the left side (p = 0.046 (p < 0.05)) independently of the side of VA aplasia; and (C) CVBA of ICA origin is significantly more common (p < 0.001).

4. Conclusions

Summarizing previous data, we point out the following facts:

(1) Almost 50% of cases of uni- and bilateral VA aplasia in three countries, USA, Japan, and India, were discovered.

(2) Two-thirds of VA aplasia cases belonged to patients of ages 31 to 80.

(3) Although there was no significant sex difference in appearance of VA aplasia, male gender was more common in cases of bilateral VA aplasia.

(4) The side of the VA aplasia has significant influence on the side of CVBA persistence, or vice versa.

(5) CVBA persistence is significantly more common on the left side in cases of uni- and bilateral VA aplasia.

(6) Associated aplasia of other arteries was more common in cases of unilateral VA aplasia.

(7) The left VA was more commonly hypoplastic in cases of single right VA aplasia than the right VA in cases of single left VA aplasia.

(8) There was high incidence of cerebral artery stenosis, occlusion, cerebral infarction, or stroke in cases of single left and bilateral VA aplasia.

(9) Aneurysms of definitive arteries were more frequent in cases of single right VA aplasia than in cases of single left VA aplasia.

Disclosure

This work was partially presented at the 8th International Symposium of Clinical and Applied Anatomy in Budapest, Hungary, September 1-3, 2016, and at the 5th Congress of Serbian Anatomical Society with international participation in Novi Sad, Serbia, September 8-10, 2016.

https://doi.org/ 10.1155/2017/7238672

Conflicts of Interest

The authors report no conflicts of interest concerning the materials or methods used in this study or the findings specified in this paper.

Acknowledgments

The authors express their gratitude to Mrs. Zorica Antic, Professor of English at the Faculty of Medicine of Nis, for her editing of this manuscript. The authors would like to thank the contract grant sponsor Ministry of Science and Technological Development of Republic of Serbia (nos. 41018 and 175092) and their Faculty of Medicine (Internal Projects nos. 14,15, and 22).

References

[1] D. H. Padget, "Designation of the embryonic intersegmental arteries in reference to the vertebral artery and subclavian stem," The Anatomical Record, vol. 119, no. 3, pp. 349-356,1954.

[2] E. L. Effmann, S. A. Whitman, and B. R. Smith, "Aortic arch development," RadioGraphics, vol. 6, no. 6, pp. 1065-1089,1986.

[3] L. Vasovic, G. Radenkovic, M. Trandafilovic, and G. Dordevic, "Variable left and/or right vertebral artery in prevertebral part: a review of features in the postnatal period," Series: Medicine and Biolology, vol. 17, no. 1, pp. 1-25, 2015.

[4] M. Okahara, H. Kiyosue, H. Mori, S. Tanoue, M. Sainou, and H. Nagatomi, "Anatomic variations of the cerebral arteries and their embryology: A pictorial review," European Radiology, vol. 12, no. 10, pp. 2548-2561, 2002.

[5] L. Vasovic, Z. Milenkovic, I. Jovanovic, R. Cukuranovic, P. Jovanovic, and I. Stefanovic, "Hypoglossal artery: A review of normal and pathological features," Neurosurgical Review, vol. 31, no. 4, pp. 385-395, 2008.

[6] L. Vasovic, M. Mojsilovic, Z. Ancrossed D Signelkovic et al., "Proatlantal intersegmental artery: A review of normal and pathological features," Child's Nervous System, vol. 25, no. 4, pp. 411-421, 2009.

[7] L. Vasovic, S. Arsic, S. Vlajkovic et al., "Otic artery: a review of normal and pathological features," Medical Science Monitor, vol. 16, no. 5, pp. RA101-RA109, 2010.

[8] L. Vasovic, I. Jovanovic, S. Ugrenovic, S. Vlajkovic, P. Jovanovic, and V. Stojanovic, "Trigeminal artery: A review of normal and pathological features," Child's Nervous System, vol. 28, no. 1, pp. 33-46, 2012.

[9] K.-H. Deeg, T. Rupprecht, and M. Hofbeck, "Doppler sonography in infancy and childhood," Doppler Sonography in Infancy and Childhood, pp. 1-745, 2015.

[10] V. Ljiljana, J. Ivan, U. Sladana, V. Slobodan, J. Predrag, and D. Gordana, "Extracranial Segments of the Vertebral Artery: Insight in the Developmental Changes up to the 21st Year of Life," Advances and technical standards in neurosurgery, vol. 40, pp. 111-139, 2014.

[11] M. G. Yasargil, Microneurosurgery, vol. I, Thieme, New York, NY, USA, 1984.

[12] L. P. Vasovic, "The tenth vascular component in a rare form of the cerebral arterial circle of fetuses," Cells Tissues Organs, vol. 178, no. 4, pp. 231-238, 2004.

[13] L. Vasovic, M. Trandafilovic, I. Jovanovic et al., "An excess vessel in the posterior part of the human cerebral arterial circle (CAC): a case series," BioMed Central Neurology, vol. 10, no. 1, p. 53, 2010.

[14] N. A. Hutchinson and J. D. Miller, "Persistent proatlantal artery," Journal of Neurology Neurosurgery and Psychiatry, vol. 33, no. 4, pp. 524-527, 1970.

[15] C. C. Lui, Y. H. Liu, Y. Y. Wai, and C. C. Tsai, "Persistence of both proatlantal arteries with absence of vertebral arteries," Neuroradiology, vol. 29, no. 3, pp. 304-305,1987.

[16] J. R. Bapuraj, V. Ojili, N. Khandelwal, A. K. P. Shanbhogue, and S. K. Gupta, "Basilar artery aneurysm treated with coil embolization via persistent primitive hypoglossal artery," Australasian Radiology, vol. 51, no. 4, pp. B340-B343, 2007.

[17] S. Tsukamoto, Y. Hori, S. Utsumi, T. Tanigake, N. Horiike, and R. Otani, "Proatlantal intersegmental artery with absence of bilateral vertebral arteries. Case report," Journal of Neurosurgery, vol. 54, no. 1, pp. 122-124,1981.

[18] F. Y. Tsai, J. Mahon, J. W. Woodruff, and J. F. Roach, "Congenital absence of bilateral vertebral arteries with occipital-vertebral anastomosis," American Journal of Roentgenology, vol. 124, no. 2, pp. 281-286, 1975.

[19] M. Zarghouni and D. Marichal, "Persistent bilateral proatlantal type II artery," Baylor University Medical Center Proceedings, vol. 26, no. 1, pp. 50-51, 2013.

[20] R. Kolbinger, W. Heindel, G. Pawlik, and H. Erasmi-Korber, "Right proatlantal artery type I, right internal carotid occlusion, and left internal carotid stenosis: Case report and review of the literature," Journal of the Neurological Sciences, vol. 117, no. 1-2, pp. 232-239, 1993.

[21] R. M. Nagaraju and B. Bhimarao, "MR angiography in persistent hypoglossal artery with absent bilateral vertebral arteries: a rare anomaly," Journal of Evidence Based Medicine and Healthcare, vol. 2, no. 17, pp. 2646-2650, 2015.

[22] J. E. Cohen, S. Grigoriadis, and E. Itshayek, "Type II proatlantal artery (occipital subtype) with bilateral absence of the vertebral arteries," Clinical Anatomy, vol. 24, no. 8, pp. 950-952, 2011.

[23] M. Montechiari, A. Iadanza, A. Falini, and L. S. Politi, "Monolateral type i proatlantal artery with bilateral absence of vertebral arteries: Description of a case and review of the literature," Surgical and Radiologic Anatomy, vol. 35, no. 9, pp. 863-865, 2013.

[24] G. Y. Luh, B. L. Dean, T. A. Tomsick, and R. C. Wallace, "The persistent fetal carotid-vertebrobasilar anastomoses," American Journal of Roentgenology, vol. 172, no. 5, pp. 1427-1432,1999.

[25] R. K. Menon, R. H. Swartz, R. I. Aviv, and S. P. Symons, "Bilateral Type II persistent proatlantal intersegmental arteries," Canadian Journal of Neurological Sciences, vol. 40, no. 6, pp. 873-874, 2013.

[26] M. R. Srinivas, K. S. Vedaraju, B. H. Manjappa, and B. R. Nagaraj, "Persistent primitive hypoglossal artery (PPHA) - a rare anomaly with literature review," Journal of Clinical and Diagnostic Research, vol. 10, no. 1, article no. A116, pp. TD13TD14, 2016.

[27] Y. Okada, T. Shima, M. Nishida et al., "Bilateral persistent trigeminal arteries presenting with brain-stem infarction," Neuroradiology, vol. 34, no. 4, pp. 283-286,1992.

[28] T. Gumus, B. Onal, and E. T. Ilgit, "Bilateral persistence of type 1 proatlantal arteries: Report of a case and review of the literature," American Journal of Neuroradiology, vol. 25, no. 9, pp. 1622-1624, 2004.

[29] H. Takahashi, H. Tanaka, N. Fujita, and N. Tomiyama, "Bilateral persistent hypoglossal arteries: MRI findings," British Journal of Radiology, vol. 85, no. 1010, pp. e46-e48, 2012.

[30] S. Purkayastha, A. K. Gupta, R. Varma, and T. R. Kapilamoorthy, "Proatlantal intersegmental arteries of external carotid artery origin associated with Galen's vein malformation," American Journal of Neuroradiology, vol. 26, no. 9, pp. 2378-2383, 2005.

[31] R. Pulli, M. Gatti, and C. Pratesi, "Carotid endarterectomy in rare bilateral carotidvertebral anastomosis," Journal of Vascular Surgery, vol. 33, no. 5, pp. 1122-1124, 2001.

[32] R. J. Woodcock, H. J. Cloft, and J. E. Dion, "Bilateral type 1 proatlantal arteries with absence of vertebral arteries," American Journal of Neuroradiology, vol. 22, no. 2, pp. 418-420, 2001.

[33] A. Pasco, X. Papon, S. Bracard, J. Y. Tanguy, A. Ter Minassian, and P. Mercier, "Persistent carotid-vertebrobasilar anastomoses: How and why differentiating them?" Journal of Neuroradiology, vol. 31, no. 5, pp. 391-396, 2004.

[34] T.-H. Li, M.-Y. Lan, J.-S. Liu, Y.-L. Tseng, H.-S. Wu, and Y.Y. Chang, "Type II proatlantal intersegmental artery associated with objective pulsatile tinnitus," Neurology, vol. 71, no. 4, pp. 295-296, 2008.

[35] L. Berger, D. Gouicem, E. D. Lebied, A. Felisaz, O. Coffin, and D. Maiza, "Internal carotid and ipsilateral type II proatlantal artery stenoses causing simultaneous hemispheric and vertebrobasilar transient ischemia," Journal of Vascular Surgery, vol. 53, no. 2, pp. 475-477, 2011.

[36] Y. Shimamura, Y. Kawakami, T. Tamiya, and T. Chihara, "Ascending pharyngeal-vertebral anastomosis with bilateral absence of vertebral arteries-case report.," Neurologia medicochirurgica, vol. 26, no. 7, pp. 552-555, 1986.

[37] R. A. Anderson and F. K. Sondheimer, "Rare carotid-vertebrobasilar anastomoses with notes on the differentiation between proatlantal and hypoglossal arteries," Neuroradiology, vol. 11, no. 3, pp. 113-118, 1976.

[38] S. F. McCartney, M. A. Ricci, P. Labreque, and J. F. Symes, "Persistent hypoglossal artery encountered during carotid endarterectomy," Annals of Vascular Surgery, vol. 3, no. 3, pp. 257-260, 1989.

[39] M. Gupta, R. Gupta, and A. Seith, "Persistent primitive hypoglossal artery associated with Chiari II malformation: Diagnosis and clinical implications," Indian Journal of Radiology and Imaging, vol. 20, no. 4, pp. 258-260, 2010.

[40] D. Spizzichino, Persistent hypoglossal artery, in Neuroradiology on the net. http://neuroradiologyonthenet.blogspot.rs/2008/ 05/persistent-hypoglossal-artery.html, 2008.

[41] S. Baldi, T. Zander, M. Rabellino, and M. Maynar, "Stentassisted coil embolization of a wide-neck aneurysm of a persistent primitive hypoglossal artery," CardioVascular and Interventional Radiology, vol. 32, no. 2, pp. 352-355, 2009.

[42] M. Anderson, "Persistent primitive hypoglossal artery with basilar aneurysm," Journal of Neurology, vol. 213, no. 4, pp. 377-381, 1976.

[43] D. M. Patel, M. M. Mortazavi, R. S. Tubbs, J. Cure, and W. S. Fisher, "Two unusual cases of the posterior cranial fossa blood supply," Cureus, vol. 6, no. 4, p. 176, 2014.

[44] P. Pauliukas, Loops, kinks and anomalies of vertebral arteries, http://www.pauliukoklinika.lt/get.php?f.6365 2014.

[45] Y. Tian, Y.-F. Wang, H.-G. Du, J. Xu, J.-M. Zhang, and S.-X. Guo, "Left type I proatlantal artery with bilateral aberrant vertebral arteries and a ruptured aneurysm: a case report and review of the literature," Surgical and Radiologic Anatomy, vol. 37, no. 6, pp. 689-692, 2015.

[46] K. Mugundhan and P. Senthilkumar, "Persistent hypoglossal artery--a rare vascular anomaly," Journal of Association of Physicians of India, vol. 61, no. 11, pp. 812-813, 2013.

[47] F. Briganti, F. Tortora, A. Elefante, A. Volpe, and F. Maiuri, "Persistent carotid-vertebral anastomosis associated with contralateral accessory middle cerebral artery," Surgical and Radiologic Anatomy, vol. 27, no. 5, pp. 450-454, 2005.

[48] P. Huynh-Le, T. Matsushima, H. Muratani, T. Hikita, and E. Hirokawa, "Persistent primitive hypoglossal artery associated with proximal posterior inferior cerebellar artery aneurysm," Surgical Neurology, vol. 62, no. 6, pp. 546-551, 2004.

[49] H. Kageyama, T. Toyooka, H. Osada, and N. Tsuzuki, "Infratentorial arteriovenous malformation associated with persistent primitive hypoglossal artery," Surgical Neurology International, vol. 6, no. 1, p. 71, 2015.

[50] K. Nakashima, H. Itokawa, A. Oishi, Y. Imaizumi, and H. Izumiyama, "Persistent primitive first cervical intersegmental artery (proatlantal artery II) associated with subarachnoid hemorrhage of unknown origin," Clinical Neurology and Neurosurgery, vol. 114, no. 1, pp. 90-92, 2012.

[51] Y. Shibata, A. Hyodo, A. Saito, Y. Yoshii, and T. Nose, "Large arteriovenous malformation associated with persistent primitive hypoglossal artery-case report," Neurologia Medico-Chirurgica, vol. 31, no. 12, pp. 804-808,1991.

[52] S. Waga, Y. Morooka, and T. Kojima, "Aneurysm on a persistent hypoglossal artery," Acta Neurochirurgica, vol. 59, no. 1-2, pp. 7178, 1981.

[53] L. A. Arraez-Aybar, P. Navia-Alvarez, and J. C. Mendez-Cendon, "A case of a type II proatlantal artery with arteriovenous malformation," Surgical and Radiologic Anatomy, vol. 33, no. 1, pp. 85-89, 2011.

[54] P. B. Nielsen and M. Jonson, "Persistent primitive trigeminal artery demonstrated by vertebral arteriography," Radiology, vol. 101, no. 1, pp. 47-51, 1967.

[55] S. Hahnel, M. Hartmann, O. Jansen, and K. Sartor, "Persistent hypoglossal artery: MRI, MRA and digital subtraction angiography," Neuroradiology, vol. 43, no. 9, pp. 767-769, 2001.

[56] I. Pascual-Castroviejo, J. Viano, F. Moreno et al., "Hemangiomas of the head, neck, and chest with associated vascular and brain anomalies: A complex neurocutaneous syndrome," American Journal of Neuroradiology, vol. 17, no. 3, pp. 461-471,1996.

[57] S. W. Jeon, H. W. Chang, M. J. Kim, and J. Cho, "Persistent proatlantal artery in magnetic resonance angiography: a case report," Journal of the Korean Society of Magnetic Resonance in Medicine, vol. 17, no. 1, pp. 55-58, 2013.

[58] H. M. Keller, W. E. Meier, and D. A. Kumpe, "Noninvasive angiography for the diagnosis of vertebral artery disease using doppler ultrasound (Vertebral artery doppler)," Stroke, vol. 7, no. 4, pp. 364-369, 1976.

[59] H. Akay, A. Ozturk, K. K. Oguz, and S. Cekirge, "Type 2 persistent proatlantal intersegmental artery: Demonstration by multislice computed tomography angiography," European Journal of Radiology Extra, vol. 56, no. 3, pp. 65-67, 2005.

[60] G. A. Fantini, L. M. Reilly, and R. J. Stoney, "Persistent hypoglossal artery: Diagnostic and therapeutic considerations concerning carotid thromboendarterectomy," Journal of Vascular Surgery, vol. 20, no. 6, pp. 995-999, 1994.

[61] J. Karasawa, H. Kikuchi, S. Furuse, T. Sakaki, Y. Yoshida, and H. Ohnishi, "Bilateral persistent carotid basilar anastomoses," American Journal of Roentgenology, vol. 127, no. 6, pp. 1053-1056, 1976.

[62] S. Suzuki, T. Nobechi, I. Itoh, M. Yakura, and K. Iwashita, "Persistent proatlantal intersegmental artery and occipital artery originating from internal carotid artery," Neuroradiology, vol. 17, no. 2, pp. 105-109, 1979.

[63] A. Uchino, N. Saito, and K. Inoue, "Type 2 proatlantal intersegmental artery associated with persistent trigeminal artery diagnosed by MR angiography," Surgical and Radiologic Anatomy, vol. 34, no. 8, pp. 773-776, 2012.

[64] I. G. Berman and S. L. Stuckey, "Anomalous communication of external carotid and vertebral arteries with associated intracranial parenchymal arteriovenous malformation: Magnetic resonance angiography and angiographic findings," Australasian Radiology, vol. 47, no. 4, pp. 472-474, 2003.

[65] K. Buljan, I. Hegedus, T. Gilman Kuric et al., "Type i persistent proatlantal artery associated with fusiform subclavian artery aneurysm. Report of one case," Revista Medica de Chile, vol. 143, no. 8, pp. 1081-1084, 2015.

[66] F. Grego, R. Stramana, S. Lepidi et al., "Primitive proatlantal intersegmental artery and carotid endarterectomy," Journal of Vascular Surgery, vol. 39, no. 3, p. 691, 2004.

[67] N. Hirota, H. Hokaku, A. Katoh, T. Sakurai, T. Miyo, and M. Tsuyumu, "Carotid artery stenting for symptomatic stenosis of cervical carotid artery with a persistent proatlantal artery: case report," Journal of Neuroendovascular Therapy, vol. 4, no. 3, pp. 157-163, 2010.

[68] Y. Z. Bahsi, H. Uysal, S. Peker, and M. Yurdakul, "Persistent Primitive Proatlantal Intersegmental Artery (Proatlantal Artery I) Results in 'Top of the Basilar' Syndrome," Stroke, vol. 24, no. 12, pp. 2114-2117, 1993.

[69] A. A. Abla, P. Kan, S. Jahshan, T. M. Dumont, E. I. Levy, and A. H. Siddiqui, "External carotid dissection and external carotid proatlantal intersegmental artery with subclavian steal prompting external carotid and subclavian artery stenting," Journal of Neuroimaging, vol. 24, no. 4, pp. 399-403, 2014.

[70] J. M. Liechty, R. J. Weddle, W. P. Shutze, and B. L. Smith, "Occurrence of a type 2 proatlantal intersegmental artery during carotid endarterectomy for symptomatic stenosis," Journal of Vascular Surgery, vol. 64, no. 3, pp. 807-808, 2016.

[71] P. Morris, Practical Neuroangiography, Wolters Kluwer/ Lippincot Williams and Wilkins, Philadelphia, 3rd edition, 2013.

[72] K. Ouriel, R. M. Green, and J. A. DeWeese, "Anomalous carotidbasilar anastomoses in cerebrovascular surgery," Journal of Vascular Surgery, vol. 7, no. 6, pp. 774-777,1988.

[73] M. L. Pinstein and B. Gerald, "Anomalous communication of the external carotid and vertebral arteries. Persistence of the proatlantal artery," Radiology, vol. 118, no. 3, p. 626,1976.

[74] S. Avcu, I. Van Der Schaaf, H. N. Ozcan, I. Sengul, and H. Fransen, "Persistent hypoglossal artery detected incidentally in a hypertensive patient with intracerebral hemorrhage: A case report and review of the literature," Cases Journal, vol. 2, no. 7, article no. 8571, 2009.

[75] G. Arnould, P. Tridon, M. Laxenaire, L. Picard, M. Weber, and G. Gougaud, "L'artere hypoglosse primitive. Etude anatomique et radiologique. A propos de deux observations," Revue Neurologique, vol. 118, no. 5, pp. 372-379,1968.

[76] M. Vlychou, M. Georganas, G. Spanomichos, P. Kanavaros, C. Artinopoulos, and G. M. Zavras, "Angiographic findings and clinical implications of persistent primitive hypoglossal artery," BMC Medical Imaging, vol. 3, article no. 2, 2003.

[77] G. Khodadad, "Persistent hypoglossal artery in the fetus," Acta Anatomica, vol. 99, no. 4, pp. 477-481,1977.

[78] W. P. Thayer, J. R. Gaughen, and N. L. Harthun, "Surgical revascularization in the presence of a preserved primitive carotid-basilar communication," Journal of Vascular Surgery, vol. 41, no. 6, pp. 1066-1069, 2005.

[79] A. L. Wagner, "Isolated stenosis of a persistent hypoglossal artery visualized at 3D CT angiography," American Journal of Neuroradiology, vol. 22, no. 8, pp. 1613-1614, 2001.

[80] N. A. Not Available, "Persistent trigeminal artery associated with basilar artery hypoplasia: MR and MRA findings," Austin Journal of Radiology, vol. 2, no. 2, p. 1014, 2015.

[81] T. Xie, X.-B. Zhang, Q.-P. Li, W. Zhu, H. Zhou, and Y. Gu, "Hemifacial spasm patient with ipsilateral total absence of common carotid artery, vertebral artery and aneurysm of the contralateral internal carotid artery," Surgical and radiologic anatomy: SRA, vol. 32, no. 7, pp. 707-710, 2010.

[82] D. Kimball, H. Ples, G. D. Miclaus, P. Matusz, and M. Loukas, "Persistent hypoglossal artery aneurysm located in the hypoglossal canal with associated subarachnoid hemorrhage," Surgical and Radiologic Anatomy, vol. 37, no. 2, pp. 205-209, 2015.

[83] N. Nakanishi, T. Sugino, K. Morikawa, N. Ohkawa, and A. Fukusumi, "The Posterior inferior cerebellar artery arising from the internal carotid artery directly: a variant of the persistent primitive hypoglossal artery," No To Shinkei, vol. 56, no. 3, pp. 253-257, 2004.

[84] C. Nishida, R. Ashikaga, Y. Araki et al., "Persistent hypoglossal artery associated with arteriovenous malformation: A case report," European Journal of Radiology, vol. 33, no. 1, pp. 59-62, 2000.

[85] J. K. Kwon, M. S. Kim, and C. H. Lee, "Persistent proatlantal artery type I observed in a patient with subarachnoid hemorrhage: case report," Korean Journal of Cerebrovascular Surgery, vol. 10, no. 2, pp. 387-390, 2008.

[86] M. Bora and R. S. Mittal, "Vertebral artery agenesis in AAD and basilar invasination: a case report," World Spinal Column Journal, vol. 5, no. 3, pp. 130-135, 2014.

[87] K. Nii, H. Aikawa, M. Tsutsumi et al., "Carotid artery stenting in a patient with internal carotid artery stenosis and ipsilateral persistent primitive hypoglossal artery presenting with transient ischemia of the vertebrobasilar system," Neurologia Medico-Chirurgica, vol. 50, no. 10, pp. 921-924, 2010.

[88] A. I. Ranchod, S. Gora, R. N. Swartz, S. Andronikou, and V. Mngomezulu, "A rare carotid-basilar anastomosis traversing the jugular foramen: Origin and clinical implications," Interventional Neuroradiology, vol. 17, no. 3, pp. 347-350, 2011.

[89] E. R. Hackett and C. B. Wilson, "Congenital external carotidvertebral anastomosis," American Journal of Roentgenology Radium Therapy and Nuclear Medicine, vol. 104, no. 1,pp. 86-89, 1968.

[90] W. Moller-Hartmann, P. Reichel, J. Berkefeld, and F. E. Zanella, "Persistierende Arteria trigemina primitiva mit Aplasie der Arteria basilaris und der kontralateralen Arteria vertebralis eine weitere Variante der karotido-basilaren Anastomosen," Klinische Neuroradiologie, vol. 9, no. 3, pp. 167-171,1999.

[91] B.-G. Yoo, K.-T. Ji, K.-S. Kim, K.-M. Yoo, S.-M. Kim, and Y.D. Joh, "Proatlantal intersegmental artery type II observed in a patient with Locked-in syndrome," Journal of the Korean Neurological Association, vol. 20, no. 1, pp. 97-99, 2002.

[92] C. C. Basekim, E. Silit, H. Mutlu, M. Z. Pekkafali, E. Ozturk, and E. Kizilkaya, "Type I proatlantal artery with bilateral absence of the external carotid arteries," American Journal of Neuroradiology, vol. 25, no. 9, pp. 1619-1621, 2004.

[93] P. Bour, S. Bracard, N. Frisch, R. Frisch, and G. Fieve, "Persistent proatlantal artery associated with carotid artery stenosis treatment by percutaneous transluminal balloon angioplasty," Annals of Vascular Surgery, vol. 5, no. 1, pp. 38-40,1991.

[94] K. Kurose, H. Kishi, and Y. Nishijima, "Type 2 proatlantal artery associated with a ruptured aneurysm: case report," Neurologia Medico-Chirurgica, vol. 30, no. 3, pp. 191-193, 1990.

[95] A. B. Conforto, M. de Souza, P. Puglia Jr., F. I. Yamamoto, C. da Costa Leite, and M. Scaff, "Bilateral occipital infarcts associated with carotid atherosclerosis and a persistent hypoglossal artery," Clinical Neurology and Neurosurgery, vol. 109, no. 4, pp. 364-367, 2007.

[96] R. Cartier, P. Cartier, G. Hudon, and M. Rousseau, "Combined endarterectomy of the internal carotid artery and persistent hypoglossal artery: An unusual case of carotid revascularization," Canadian Journal of Surgery, vol. 39, no. 2, pp. 159-162, 1996.

[97] D. Ben Salem, M. Allaoui, E. Dumousset et al., "Chondroblastoma of the temporal bone associated with a persistent hypoglossal artery," Acta Neurochirurgica, vol. 144, no. 12, pp. 1315-1318, 2002.

[98] G. K. Paraskevas, P. P. Tsitsopoulos, B. Papaziogas, and S. Spanidou, "Persistent primitive hypoglossal artery: An incidental autopsy finding and its significance in clinical practice," Folia Morphologica, vol. 66, no. 2, pp. 143-147, 2007.

[99] K. Sakai, Y. Tanaka, K. Tokushige, A. Tanabe, and S. Kobayashi, "Basilar bifurcation aneurysms associated with persistent primitive hypoglossal artery," Neurosurgical Review, vol. 21, no. 4, pp. 290-294, 1998.

[100] A. Uchino and N. Saito, "Persistent hypoglossal artery arising from the external carotid artery diagnosed by MR angiography," Surgical and Radiologic Anatomy, vol. 33, no. 6, pp. 543-545, 2011.

[101] M. Trandafilovic, L. Vasovic, S. Vlajkovic, I. Jovanovic, and S. D. S. Ugrenovic, "Discovery of the PPHA," Neurosurgery, vol. 73, no. 1, pp. E195-E197, 2013.

[102] G. Chaljub, F. C. Guinto, and W. N. Crow, "Persistent hypoglossal artery: Mri and mra findings," Journal of Computer Assisted Tomography, vol. 19, no. 4, pp. 668-669,1995.

[103] S. He, J. J. Russin, P. Adamczyk, S. L. Giannotta, A. P. Amar, and W. J. Mack, "A Persistent Primitive Hypoglossal Artery Arising from the External Carotid Artery Associated with Subarachnoid Hemorrhage," World Neurosurgery, vol. 82, no. 12, pp. 239-239.e3, 2014.

[104] M. D. Widmann and B. E. Sumpio, "Persistent hypoglossal artery: An anomaly leading to false-positive carotid duplex sonography," Annals of Vascular Surgery, vol. 6, no. 2, pp. 176-178, 1992.

[105] G. L. Heyer, M. M. Dowling, D. J. Licht et al., "The cerebral vasculopathy of PHACES syndrome," Stroke, vol. 39, no. 2, pp. 308-316, 2008.

[106] R. Kumar, A. Mehrotra, J. Chunnilal, K. Das, and A. Srivastava, "Atlanto-axial dislocation associated with anomalous single vertebral artery and agenesis of unilateral internal carotid artery," Asian Journal of Neurosurgery, vol. 8, no. 3, pp. 173-175, 2013.

[107] O. Karabulut, K. Iltimur, and M. Cudi Tuncer, "Coexisting of aortic arch variation of the left common carotid artery arising from brachiocephalic trunk and absence of the main branches of right subclavian artery: a review of the literature," Romanian Journal of Morphology and Embryology, vol. 51, no. 3, pp. 569-572, 2010.

[108] C.-L. Kao, K.-T. Tsai, and J.-P. Chang, "Large extracranial vertebral aneurysm with absent contralateral vertebral artery," Texas Heart Institute Journal, vol. 30, no. 2, pp. 134-136, 2003.

[109] M. C. Tuncer, Y. H. Akgiil, and O. Karabulut, "MR Angiography Imaging of Absence Vertebral Artery Causing of Pulsatile Tinnitus: A Case Report," International Journal of Morphology, vol. 28, no. 2, pp. 357-363, 2010.

[110] S. Duan, S. Lv, F. Ye, and Q. Lin, "Imaging anatomy and variation of vertebral artery and bone structure at craniocervical junction," European Spine Journal, vol. 18, no. 8, pp. 1102-1108, 2009.

L. Vasovic, (1) M. Trandafilovic, (1) S. Vlajkovic, (1) G. Djordjevic, (2) M. Dakovic-Bjelakovic, (1) and M. Pavlovic (1)

(1) Department of Anatomy, Faculty of Medicine, University of Nis, 81 Blvd. Dr. Zoran Djindjic, 18000 Nis, Serbia

(2) Health Center Nis, 15 Vojvode TankosiCa St., 18000 Nis, Serbia

Correspondence should be addressed to L. Vasovic; likica@medfak.ni.ac.rs

Received 16 March 2017; Accepted 4 July 2017; Published 28 August 2017

Academic Editor: Tobias De Zordo

Caption: Figure 1: Some arteries of the carotid and vertebrobasilar systems on the brain base and in the middle and posterior cranial fossae in a 77year-old man autopsied because of myocardial infarction in the Institute of Forensic Medicine; the approval for coauthor's (MT) investigation of cadaveric cases was obtained from the Research Ethics Committee (number 01-9068-4) of our Faculty of Medicine. (a) Additional vascular component, so-called intermediate communicating artery (ICoA) between the right posterior cerebral artery (PCA) of carotid (C4) origin (PCAc) and right PCA of basilar (BA) origin (PCAb) in the cerebral arterial circle marking, is separately shown. (b) Main arteries of the carotid and vertebrobasilar systems from original picture are extracted and marked. The cerebral arterial circle has the shape of a decagon; its vascular components are as follows: subparts of the cerebral parts (C4) of paired internal carotid arteries, precommunicating part (A1) of paired anterior cerebral arteries connected by network configuration of the anterior communicating artery (ACoA), and then the left posterior communicating artery (PCoA), which connects and divides ipsilateral PCA in the precommunicating (P1) and postcommunicating (P2) parts. So-called ICoA connecting the right PCAc and PCAb presents the tenth vascular component in the cerebral arterial circle. Additional BA branch on the left side, located below the superior cerebellar artery (SCA), as a persistent primitive trigeminal artery (PPTA) is marked. Besides Heubner's artery (RAH), a large side branch of the left anterior cerebral artery and sphenoidal part (M1) of paired middle cerebral arteries are also marked. The right SCA, as partially duplicated vessel and single left SCA, as well as single anterior inferior cerebellar artery (AICA) on both sides and the right posterior inferior cerebellar artery (PICA) are side branches of the BA, while the left PICA is a branch of ipsilateral vertebral artery (VA). (c) View on a part of the middle and posterior cranial fossae of the same case. It shows the left PPTA as a branch of the cavernous part (C3) of the internal carotid artery and only the left VA in the course through the foramen magnum.
Table 1: Distribution of single cases of the vertebral artery (VA)
aplasia in various countries.

Side
of VA                                      Countries * [references]
aplasia

Bilaterally                                   Canada [14,     China
                                                25, 38]      [15, 34]

Number                                             3            2

Left          Australia   Belgium                             China
                [64]        [74]                             [45, 81]

Number            1          1                                  2

Right                                Brazil     Canada        China
                                      [95]       [96]       [108, 110]
Number                                 1           1            2
[SIGMA]           1          1         1           4            6

Side
of VA                                Countries * [references]
aplasia

Bilaterally                France         Germany
                           [33, 35]         [20]

Number                        2              1

Left          Croatia      France         Germany      Greece
                [65]         [75]           [55]        [76]

Number           1            1              1            1

Right                      France         Germany      Greece
                         [75, 93, 97]       [90]        [98]
Number                        3              1            1
[SIGMA]          1            6              3            2

Side
of VA                                   Countries * [references]
aplasia

Bilaterally                India [16,      Israel    Italy [23,
                             21, 26,        [22]      31, 40]
                             30, 39]
Number                          5             1          3

Left                          India                    Italy
                             [30, 46]                 [47, 66]

Number                          3                        2

Right         Grenada         India                    Italy
                [82]        [86, 106]                   [40]
Number            1             2                        1
[SIGMA]           1             10            1          6

Side
of VA                            Countries * [references]
aplasia

Bilaterally     Japan [17,       Lithuania
                27, 29, 36]        [44]

Number               4               1

Left           Japan [48-52,
                 61-63, 67]

Number               9

Right         Japan [83, 84,                 Serbia **    South Africa
              87, 94, 99, 100]                 [101]          [88]
Number               6                           2             1
[SIGMA]              19              1           2             1

Side
of VA                                Countries * [references]
aplasia

Bilaterally                   Spain                    Turkey [28]
                               [41]

Number                          1                           1

                                          Sweden
Left          South Korea     Spain     Switzerland    Turkey [59,
                  [57]       [53, 56]    [54] [58]     68, 80, 109]

Number             1            7           1 1             4

Right         South Korea                                Turkey
                [85, 91]                                [92, 107]
Number             2                                        2
[SIGMA]            3            8           1 1             7

Side
of VA         Countries * [references]    [SIGMA]
aplasia
                              USA
Bilaterally   UK [42]      [18, 19,
                        24, 32, 37, 43]

Number           1             6            31

Left                       USA [60,
                         69-73, 77-79]

Number                        10            46

Right                      USA [89,
                           102-105]
Number                         5            31
[SIGMA]          1            21            108

* Alphabetical order. ** Recent case is included.

Table 2: Distribution of the vertebral artery (VA) aplasia according
to the gender.

Side of VA aplasia       Female            Male          Unknown
                                        Number (%)

Bilateral            11/108 (10.18)   19/108 (17.59)   1/108 (0.92)
Left                 24/108 (22.22)   20/108 (18.52)   2/108 (1.85)
Right                14/108 (12.96)   14/108 (12.96)   3/108 (2.77)

Total                49/108 (45.37)   53/108 (49.07)     6 (5.55)

Table 3: Distribution of 108 cases of the vertebral artery (VA)
aplasia according to age.

Age of patients                           Number of cases of VA aplasia

                            Bilaterally   Left side    Right side
Stillborn                                     1
Newborn (few hours                            1
  after birth)
Neonate ([less than or           1            1
  equal to] 28 days)
Suckling ([less than             1            5
  or equal to] 12 months)
Tot ([less than or                            3
  equal to] 3 years)
Preschool age                                              1
([less than or equal
  to] 5 years)
School age (6-12)                1
Adolescent (13-18)                            1
19-30                            1            2            1
31-40                            2            3            8
41-50                            4            4            4
51-60                            6            9            3
61-70                           11            7            5
71-80                            3            5            6
>81                                           2
Unknown age                      1            2            3

Age of patients             ([SIGMA] =108)

Stillborn                         1
Newborn (few hours                1
  after birth)
Neonate ([less than or            2
  equal to] 28 days)
Suckling ([less than              6
  or equal to] 12 months)
Tot ([less than or                3
  equal to] 3 years)
Preschool age                     1
([less than or equal
  to] 5 years)
School age (6-12)                 1
Adolescent (13-18)                1
19-30                             4
31-40                             13
41-50                             12
51-60                             18
61-70                             23
71-80                             14
>81                               2
Unknown age                       6

Table 4: Sixteen (16/46) literature casesa of total aplasia of the
left vertebral artery (VA) and hypoplasia of the right VA.

Number    Gender/ age    Initial symptoms or   Associated vascular
          [reference]    reasons of research   aplasia Other arteries
                                               and/or veins

(1)       F/0 [77]       Stillborn

(2)       M/14 [47]      Headache/nausea/      Left PCoA
                         slight neck
                         stiffness

(3)       M/28 [55]      Cavernous
                         hemangioma in the
                         skin of the
                         forehead

(4)       F/43 [45]      Headache

(5)       M/51 [76]      Loss of
                         consciousness

(6)       M/52 [75]      Right hemiparesis/    Left AICA and PCoA
                         aphasia

(7)       F/54 [52]      Headache/weakness     Bilateral PCoAs
                         of the right lower
                         limb

(8)       F/55 [68]      Coma

(9)       F/55 [78]      Self-audible left
                         neck bruit

(10)      M/61 [65]      Speech disorder/      Right ACA
                         left supranuclear
                         facial palsy

(11)      F/62 [60]      Intermittent          Left PCoA
                         diplopia

(12)      F/63 [70]      Transient right
                         hand weakness/left
                         amaurosis fugax

(13)      F/65 [79]      Left carotid bruit    Both PCoAs

(14)      F/73 [74]      Acute paresis in      Left PCoA
                         the left arm

(15)      F/78 [66]      Transischemic
                         attacks with right-
                         sided paresis

(16)      M/83 [63]      Cerebral infarction   Bilateral PCoAs

                                      Left VA aplasia ed persistent
Number                                          Associated
                                        CVBA and/or other vascular
            Type of persistent     Other variants and/or abnormalities
          CVBA (vascular source)              abnormalities

(1)          Left PPHA (ICA)        Hypoplastics right VA/left A1 and
                                                   PCoA

(2)          Left PPIA (ICA)         Hypoplastic right VA terminated
                                         as the PICA Low left CCA
                                     bifurcation Accessory right MCA

(3)          Left PPHA (ICA)         Hypoplastic right VA Dilatation
                                             of Galen's vein

(4)          Left PPIA (ICA)               Hypoplastic right VA

(5)          Left PPHA (ICA)               Hypoplastic right VA

(6)          Left PPHA (ICA)          Hypoplastic right VA Left PICA
                                      and ASA of PPHA origin Ectatic
                                      left CCA Dolicho-left ICA BT-
                                          left CCA common trunk

(7)          Left PPHA (ICA)               Hypoplastic right VA

(8)          Left PPIA (ICA)               Hypoplastic right VA

(9)          Left PPHA (CCA)               Hypoplastic right VA

(10)         Left PPIA (ICA)               Hypoplastic right VA

(11)         Left PPHA (ICA)          Hypoplastic right VA. BT and
                                          left CCA common origin

(12)         Left PPIA (ECA)         Hypoplastic right VA terminated
                                               as the PICA

(13)         Left PPHA (ICA)         Hypoplastic right VA terminated
                                               as the PICA

(14)         Left PPHA (ICA)               Hypoplastic right VA

(15)         Left PPIA (ICA)          Hypoplastic right VA did not
                                               form the BA

(16)         Left PPIA (ECA)          Hypoplastic right VA supplied
           Lateral type of the         only ipsilateral PICA Distal
            left PPTA (ICA-C3         branch of the left OA of PPIA
                  part)                           origin

Number      Diagnosed pathology

(1)

(2)                SAH

(3)

(4)        Aneurysm of the left
               PICA SAH/IVH

(5)

(6)

(7)       Aneurysms of the right
             AC A and PPHA-BA
                 junction

(8)       Calcified atheromatous
             plaques in both
             carotid systems
          Lesions from the level
           of the mesencephalon
           to the both thalami

(9)        Stenosis of the left
            CCA, ICA, and PPHA

(10)      Calcified atheromatous
             plaques in both
           carotid systems and
            PPIA. Stenosis of
          bilateral SAs Aneurysm
             of the right SA.
             Lacunar ischemic
             changes in basal
                 ganglia

(11)       Irregular lesion of
               the left CCA
            bifurcation and a
          moderate stenosis with
            ulceration of the
               proximal ICA

(12)       Severe ICA stenosis

(13)       Stenosis of the left
               PPHA origin

(14)      Bleeding in the right
          parietooccipital lobe

(15)       Stenosis of the left
             CCA bifurcation
             Ulcerated plaque
          extended into the ECA
           ICA, and PPIA origin

(16)

(a) Cases according to age are listed; number "0" for stillborn
status is used; other Arabian numbers indicate age in years; CVBA,
carotid-vertebrobasilar anastomosis; F, female; PPHA, persistent
primitive hypoglossal artery; ICA, internal carotid artery; Al,
precommunicating part of the anterior cerebral artery; PCoA,
posterior communicating artery; M, male; PPIA, persistent
proatlantal intersegmental artery (independently of its subtype);
PICA, posterior inferior cerebellar artery; CCA, common carotid
artery; MCA, middle cerebral artery; SAH, subarachnoid hemorrhage;
IVH, intraventricular hemorrhage; AICA, anterior inferior cerebellar
artery; ASA, anterior spinal artery; BT, brachiocephalic trunk; ACA,
anterior cerebral artery; BA, basilar artery; SA, subclavian artery;
ECA, external carotid artery; PPTA, persistent primitive trigeminal
artery; C3, cavernous part of the internal carotid artery; OA,
occipital artery.

Table 5: Thirteen (13/31) literature casesa of total aplasia of the
right vertebral artery (VA) and hypoplasia of the left VA.

Number       Gender/age             Initial symptoms or reasons
               (author)                      of research

(1)           F/30 [84]          Headache (of the 37th-week pregnant
                                               woman)

(2)           F/31 [97]           History of pain beginning in the
                                    right temporomandibular joint

(3)           F/34 [85]                       Headache

(4)           M/37 [88]                  Left-sided weakness

(5)           M/41 [92]                        Vertigo

(6)           F/43 [99]                          SAH

(7)           F/49 [103]                         SAH

(8)           M/58 [93]                  Right carotid bruit

(9)           M/62 [87]         Vertigo/left upper extremity weakness

(10)          M/66 [95]                Sudden visual blurring

(11)          F/74 [96]               Bilateral carotid bruits

(12)          F/74 [94]                 Loss of consciousness

(13)           (U) [98]                  Anatomy dissection

Number        Associated          Type of persistent CVBA (vascular
           vascular aplasia                    source)
            Other arteries
             and/or veins

(1)                                       Right PPHA (ICA)

(2)                                       Right PPHA (ICA)

(3)                                       Right PPIA* (ICA)

(4)         Bilateral PCoA             Unusual right CBA (ICA)
              Right ACA

(5)         Bilateral ECA                 Right PPIA (ICA)

(6)         Bilateral PCoA                   Right PPHA

(7)                                       Right PPHA (ECA)

(8)           Right PCoA                  Right PPIA (ICA)

(9)         Bilateral PCoA                Right PPHA (ICA)

(10)                                      Right PPHA (ICA)

(11)          Right PCoA                  Right PPHA (ICA)

(12)                                      Right PPIA (ECA)

(13)                                      Right PPHA (ICA)

           Right VA aplasia
Number        associated                 Diagnosed pathology
           persistent CVBA
          and other variants
                and/or
            abnormalities

            Other variants
                and/or
            abnormalities

(1)       Hypoplastics left        Stenosis of the left ICA at the
            ICA and VA AVM        entrance from the carotid siphon
                                       Intracranial hemorrhage

(2)        Hypoplastic left                Chondroblastoma
          VA Displaced right
            temporal lobe

(3)        Hypoplastic left      Ruptured aneurysm of the left AChA
                  VA            Unruptured aneurysm of the right AChA

(4)        Hypoplastic left
             VA Right CBA
           coursing through
             the jugular
             foramen and
          distributed right
            PICA Aberrant
               right SA

(5)        Hypoplastic left
            VA Left CCA-SA
             common trunk
           Bilaterally CCA
           distributes ECA
               branches

(6)        Hypoplastic left    Aneurysm of the BA bifurcation Partial
          VA Kinking of the           occlusion of the right PI
               right PI

(7)        Hypoplastic left              Right PICA aneurysm
                  VA

(8)       Hypoplastics left    Tight stenosis of the right ICA origin
             VA and PCoA

(9)        Hypoplastic left           Stenosis of the right ICA
                  VA

(10)       Hypoplastic left    Occlusion of bilateral PCA. Stenosis of
          VA. Right SA, left     the right CCA and ICA and left MCA.
          VA, and both CCAs        Right occipital ischemic stroke
              originated
          directly from the
             aortic arch

(11)       Hypoplastic left    Occlusion of the left ICA. Stenosis of
                  VA                 the left ECA/right ICA/ECA

(12)       Hypoplastic left     SAH. Aneurysm of the MCA trifurcation
           VA terminated as
               the PICA

(13)       Hypoplastic left
                  VA

(a) Cases according to the age are listed; Arabian numbers indicate
age in years; CVBA, carotid-vertebrobasilar anastomosis; F, female;
PPHA, persistent primitive hypoglossal artery; ICA, internal carotid
artery; AVM, arteriovenous malformation; PPIA*, persistent
proatlantal intersegmental artery (independently of its type); AChA,
anterior choroidal artery; M, male; PCoA, posterior communicating
artery; ACA, anterior cerebral artery; CBA, carotid-basilar
anastomosis; PICA, posterior inferior cerebellar artery; SA,
subclavian artery; ECA, external carotid artery; CCA, common carotid
artery; SAH, subarachnoid hemorrhage; PI, precommunicating part of
the posterior cerebral artery; BA, basilar artery; PCA, posterior
cerebral artery; MCA, middle cerebral artery; U, unknown gender.

Table 6: Left VA aplasia versus bilateral VA aplasia.

Number    Parameters

(i)       Incidence
(2)       Gender
            Female
            Male
            Female/male/unknown gender
(3)       Persistence of CVBA
            Unilateral persistence of CVBA
            Bilateral persistence of CVBA
            Persistence of two different CVBAs
            Persistence of determined CVBA
              PPIA
              PPHA
              PPTA
              Unusual arterial anastomoses
(4)       Additional vascular variants
                                         Uni-           Bi-    Uni-
                                         CCA                   3.22%
                                         ICA                   6.52%
                                         ACA                   3.22%
          Associated
          aplasia of other               PCoA          PCoAs   8.69%
          blood vessels
                                                 BA
                                         AICA                  3.22%
                                          SA                   3.22%
                                        Some dural sinuses/bilateral
                                                 IJV
            Hypoplastic right VA
            Unusual origin or side branches or termination or
          hypoplasia of other arteries or additional anastomoses

(5)       Associated vascular pathology
            Aneurysms of definitive arteries
            Aneurysms of CVBAs
            Different cerebral pathology (except that of
          aneurysms)
            Noncerebral pathology

Number    Left VA                        Bilateral VA
          46 cases                         31 cases
(i)        59.74%                           40.26%
(2)
           31.16%                           14.28%
           25.97%                           24.67%
                     45.44%/50.64%/3.89%
(3)
           82.60%                           59.07%
           4.35%                            34.48%
           4.34%                            3.22%

           43.47%                           54.83%
           34.78%                           32.25%
           13.04%                           9.67%
                                            6.45%
(4)
                        Bi-      Uni-                    Bi-

                       8.69%     3.22%                  9.67%

                                            3.22%

                                            3.22%

           34.78%
           39.13%                           41.93%

(5)
           8.69%                            19.35%
           4.34%                            3.22%
           41.30%                           41.93%

           4.34%                              0

VA, vertebral artery; CVBA, carotid-vertebrobasilar anastomosis;
PPIA, persistent primitive proatlantal intersegmental artery
(without mark of the type); PPHA, persistent primitive hypoglossal
artery; PPTA, persistent primitive trigeminal artery; ECA, external
carotid artery; ICA, internal carotid artery; ACA, anterior cerebral
artery; PCoA, posterior communicating artery; BA, basilar artery;
SA, subclavian artery; IJV, internal jugular vein.

Table 7: Single right VA aplasia versus bilateral VA aplasia.

Number    Parameters

(1)       Incidence
(2)       Gender
            Female
            Male
          Female/male/unknown gender
(3)       Persistence of CVBA
            Unilateral persistence of CVBA
            Bilateral persistence of CVBA
            Persistence of two different CVBAs
            Persistence of determined CVBA
              PPIA
              PPHA
              PPTA
              Unusual arterial anastomoses
(4)       Additional vascular variants
                                          Uni-           Bi-     Uni-
                                                        ECAs
            Associated                    ICA                   6.45%
          aplasia of other                ACA                   3.22%
          vessels                         PCoA          PCoAs   12.90%
                                                   BA
                                           SA                   3.22%
                                        branches
            Hypoplastic left VA Unusual origin or side branches or
          termination or hypoplasia of other arteries or additional
          anastomoses
(5)       Associated vascular pathology Aneurysms of definitive
               arteries
            Aneurysms of CVBAs
            Different cerebral pathology (except that of
              cerebral aneurysms)
            Noncerebral pathology

Number      Right VA                           Bilateral VA
            31 cases                             31 cases

(1)          40.32%                               59.68%
(2)
             22.58%                               17.74%
             22.58%                               30.64%
                          40.32%/53.12%/6.45%
(3)
             80.64%                               59.07%
                0                                 34.48%
                0                                 3.22%

             16.13%                               54.83%
             51.61%                               32.25%
              6.45%                               9.67%
              6.45%                               6.45%
(4)
                            Bi-       Uni-                     Bi-
                           3.22%

                           6.45%     3.22%                    9.67%
              3.22%                               3.22%

          41.93% 32.25%                           41.93%

(5)          25.80%                               16.13%

              3.22%                               3.22%
             35.48%                               35.48%

              9.67%                               3.22%

VA, vertebral artery; CVBA, carotid-vertebrobasilar anastomosis;
PPIA, persistent primitive proatlantal intersegmental artery; PPHA,
persistent primitive hypoglossal artery; PPTA, persistent primitive
trigeminal artery; CCA, common carotid artery; ICA, internal carotid
artery; ACA, anterior cerebral artery; PCoA, posterior communicating
artery; BA, basilar artery; AICA, anterior inferior cerebellar
artery; SA, subclavian

Table 8: Single left VA aplasia versus right VA aplasia.

Number    Parameters

(i)       Incidence
(2)       Gender
            Female
            Male
            Female/male/unknown gender
(3)       Persistence of CVBA
            Unilateral persistence of CVBA
            Bilateral persistence of CVBA
            Persistence of two different CVBA
            Persistence of determined CVBA
              PPIA
              PPHA
              PPTA
              Unusual arterial anastomoses
(4)       Additional vascular variants
                                           Uni-           Bi-    Uni-
                                           CCA                   3.22%
                                           ECA
                                           ICA                   6.45%
            Associated                     ACA                   3.22%
          aplasia of other blood vessels   PCoA          PCoAs   8.69%
                                                    BA
                                           AICA                  3.22%
                                         SA trunk                3.22%
                                            SA
                                         branches
            Hypoplastic (opposite) VA
            Unusual origin or side branches or termination or
          additional anastomoses
(5)       Associated vascular pathology
            Aneurysms of definitive arteries
            Aneurysms of CVBAs
            Other cerebral pathology
            Noncerebral pathology

Number    Left VA aplasia                   Right VA aplasia
             46 cases                           31 cases
(i)           59.74%                             40.26%
(2)
              31.16%                             18.18%
              25.97%                             18.18%
                            49.34%/44.15%/6.49%
(3)
              82.60%                             80.64%
               4.34%                               0
               4.34%                               0

              43.47%                             16.13%
              34.78%                             51.61%
              13.04%                             6.45%
                 0                               6.45%
(4)
                            Bi-     Uni-                        Bi-
                                   3.22%
                                                               3.22%
                                   6.45%
                                   3.22%
                                   12.90%                      6.45%
                                                 3.22%

                                   3.22%

              34.78%                             41.93%
              39.13%                             32.25%

(5)
               8.69%                             25.80%
               4.34%                             3.22%
              41.30%                             35.48%
               4.34%                             9.67%

VA, vertebral artery; CVBA, carotid-vertebrobasilar anastomosis;
PPIA, persistent primitive proatlantal intersegmental artery; PPHA,
persistent primitive hypoglossal artery; PPTA, persistent primitive
trigeminal artery; CCA, common carotid artery; ECA, external carotid
artery; ICA, internal carotid artery; ACA, anterior cerebral artery;
PCoA, posterior communicating artery; BA, basilar artery; SA,
subclavian artery.
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Author:Vasovic, L.; Trandafilovic, M.; Vlajkovic, S.; Djordjevic, G.; Dakovic-Bjelakovic, M.; Pavlovic, M.
Publication:BioMed Research International
Article Type:Report
Date:Jan 1, 2017
Words:10480
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