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Differences in Arcuate Foramina & Ipsilateral Foramina Transversaria Lalit et al.THIEME

106 Original Article

An Anatomical Study of the Morphometric Differences between Complete Arcuate Foramina and Ipsilateral Foramina Transversaria in Human Atlas Vertebrae: Could these Be Responsible for Vaso-occlusive Symptoms?Monika Lalit1 Anupama Mahajan1 Sanjay Piplani2 Jagdev S. Kullar3

1Department of Anatomy, Sri Guru Ram Das Institute of Medical Sciences and Research, Amritsar, India

2Department of Pathology, Sri Guru Ram Das Institute of Medical Sciences and Research, Amritsar, India

3Department of Anatomy, Government Medical College, Amritsar, India

Address for correspondence Monika Lalit, MBBS, M.S Anatomy, PGD Maternal Child Health, ACME-MCI, MNAMS, 24, Lane 5, Gopal Nagar, Majitha Road, Amritsar 143001, Punjab, India (e-mail: [email protected]).

Background and Aims Arcuate foramina (AF), the atlas bridges formed by a delicate bony spicule over the posterior arch of atlas, have been implicated in the compression of the vertebral artery during extreme rotation of head and neck movements. Reduc-tion in the size of arcuate foramina as compared with foramen transversarium (FT) is also an important cause for the compression of vertebral artery. Aim of the present study was to determine the morphometric differences between complete AF and ipsi-lateral foramina transversaria.Materials and Methods Eighty dry adult human atlas vertebrae were obtained in the Department of Anatomy, Government Medical College and Sri Guru Ram Das Institute of Medical Sciences and Research, Amritsar, Punjab, India. Measurements were taken of the maximum dimensions of AF and ipsilateral FT and cross-sectional area was also calculated.Results The following results were obtained.The AF were seen in total 11 (13.75%) vertebrae, 3 (3.75%) on the right side, 6 (7.5%) on left side, and 2 (2.5%) bilateral.

• The mean ventrodorsal (AFL) and superoinferior (AFH) diameter of AF was 8.79 mm and 5.98 mm, and 8.11 mm and 5.54 mm on the right and left sides, respectively, and the difference was found to be highly significant.

• The mean ventrodorsal (FTL) and mediolateral (FTW) diameter of the FT 8.19 mm and 6.56 mm, and 7.31 mm and 6.86 mm on the right and left sides, respectively, with significant difference on the right side.

• The mean cross-sectional area of AF was 41.32 mm2 and 35.38 mm2, and FT was 42.53 mm2 and 39.71 mm2 on the right and left sides, respectively, and AF has smaller area than ipsilateral FT.

Conclusions Knowledge about the dimensions and cross-sectional area of the AF and ipsilateral foramina transversaria of the atlas vertebra can improve the success rate of surgeries, thus preventing damage to the adjoining vital structures.

Abstract

Keywords ► arcuate foramen ► ponticuli ► foramen transversarium ► vertebral artery ► area

DOI https://doi.org/ 10.1055/s-0039-1697550 ISSN 2277-4025.

©2019 Society of Clinical Anatomists

Natl J Clin Anat 2019;8:106–111

Published online: 2019-10-20

107Differences in Arcuate Foramina & Ipsilateral Foramina Transversaria Lalit et al.

National Journal of Clinical Anatomy Vol. 8 No. 3/2019

IntroductionThe foramen transversarium (FT) transmitting the vertebral vascular bundle and sympathetic plexus, in the transverse processes of the atlas makes it a unique vertebra where the third part of the vertebral artery enters the FT, turns back-ward and medially, and lies in the groove on posterior arch of the atlas. The groove may be shallow or deep, or at times, bony outgrowths may appear known as atlas bridges or pon-ticuli.1 The latter may indicate anomalous ossification of the groove by oblique ligament of atlas, a fibrous tissue present at the lower border of posterior atlanto-occipital membrane converting the groove to form a complete or incomplete bony ring or arcuate foramen.1,2 The posterior bridge (retroarticu-lar canal) was first reported by Macalister.3 Later its detailed morphology studied by Macalister4 and Le Double5 has drawn attention of many anatomists since then. These bony bridges have been variously described as foramen sagittale atlantis, foramen atlantoideum posterior, Kimmerle variant, Canalis arteriae vertebralis, arcuate foramen, retrocondylar vertebral artery ring, retroarticular canal, atlas bridging, or the ponticuli.6-11 The external mechanical factors such as cus-tom of carrying heavy objects on the head could play a role in the development of anomalies of the atlas.12 Apart from absence or presence of accessory or double FT affecting the course of the vertebral artery (VA),13 occurrence of arcuate foramina (AF) may also affect the course of the VA on its exit from the FT14,15 and may mislead the surgeon to believe that the posterior arch of the atlas vertebra is unduly thick, result-ing in damage to the vertebral artery during C1–C2 screw fixation.16,17 Chances are also there that there is reduction in the size of the arcuate foramen to the size of foramen trans-versarium.18 The difference in these dimensions will decrease the cross-sectional area of the space available for the VA pass-ing through it, further result in alteration of blood flow in the vertebral vessels,18 and may lead to symptoms of headache, vasomotor disturbances of the face and recurrent disturbanc-es of swallowing and phonation constituting Barre–Lieou syndrome.7,19Thus, maintaining the vertebral artery intact constitutes an important concern and the third segment of the VA may be a reserve length to allow for neck rotation without compression to the artery. There are limited stud-ies comparing morphometry of the arcuate foramen and that of the ipsilateral foramen transversarium. Thus, aim of the present study was to measure the dimensions of complete AF and ipsilateral foramina transversaria and also to compare their morphometric differences as the difference in dimen-sions may result in compromised blood flow in the vessel. This might help explain the correlation between occurrence of the bony bridges or AF. This information is important for surgeons, radiologists, neurologists, and orthopedicians and these anatomical factors and vertebral artery entrapment should be taken into account in the therapeutic manipulation of the cervical spine.

Materials and MethodsEighty dry adult human atlas vertebrae were obtained by maceration from the cadavers in the Department of Anatomy, Government Medical College and Sri Guru Ram Das Institute of Medical Sciences and Research, Amritsar, Punjab, India. Damaged atlas vertebrae were excluded from study.

The vertebrae were examined for the evidence of exos-tosis from posterior margin of superior articular facet. The complete AF were identified following the criteria used by Mitchell.8 According to Mitchell, AF is posterior bridge or an osseous bridge that is formed between the posterior margin of superior articular facets and the posterior arch of the atlas and when complete forms the retroarticular canal. There are 3 classes of posterior bridge: class 1—groove of vertebral artery, class II—retroarticular sulcus showing incomplete ring, and class III—retroarticular canal showing complete bony ring enclosing vertebral artery. Thus, the vertebrae exhibiting bony outgrowths forming a complete bony ring or retroarticular canal or AF were included in the study.

Linear dimensions of complete AF and ipsilateral foram-ina transversaria (FT) observed during the study of 80 atlas vertebrae were measured with the help of a Vernier caliper with a least count of 0.02 mm and the data were stored on the computer sheet. Measurements were taken of the maxi-mum dimensions of AF in the ventrodorsal (arcuate foramen length [AFL]) and superoinferior (arcuate foramen height [AFH]) planes (►Fig. 1) and ipsilateral FT in the ventrodor-sal (foramen transversarium length [FTL]) and mediolateral (foramen transversarium width [FTW]) planes (►Fig. 2).

Arcuate Foramen Length (AFL): It is the maximum dimen-sion of the AF in ventrodorsal plane, taken from posterior part of groove on the posterior arch of atlas to the root of superior articular surface and marked as V’D’ (►Fig. 1).

Arcuate Foramen Height (AFH): It is the maximum dimen-sion of the AF in superoinferior plane, taken from floor of the groove to inner part of the overlying bony strut and marked as SI (►Fig. 1).

Fig. 1 Showing ventrodorsal (V’D’) and superoinferior (SI) dimen-sions of arcuate foramen (AF).

108


Differences in Arcuate Foramina & Ipsilateral Foramina Transversaria Lalit et al.

Foramen Transversarium Length (FTL): It is the maximum dimension of the FT in ventrodorsal plane and marked as VD (►Fig. 2).

Foramen Transversarium Width (FTW): It is the maxi-mum dimension of the FT in mediolateral plane and marked as ML (►Fig. 2).

The cross-sectional area of the ipsilateral AF and ipsilat-eral FT was calculated using the formula for the area of an ellipse8 (Mitchell, 1988a):

Area (A) = π (D1 × D2 × [1/4])

Where D1 = horizontal length of the foramen, D2 = verti-cal length of the foramen, and π = 3.14.

The student’s t-test was applied to evaluate the difference between the mean of right side and left side of the vertebrae. Results were considered significant when p < 0.05.

ResultsThe following results were obtained:

• 11 (13.75%) bones out of 80 bones showed AF. The AF were seen in 3 (3.75%) vertebrae on right side, 6 (7.5%) vertebrae on left side, and 2 (2.5%) were bilateral. In terms of sides, out of 160 sides, 13 (8.12%) sides showed the AF presence, being the 5 (3.12%) on right side and 8 (5%) on left side, respectively (►Table 1).

• The mean ventrodorsal (AFL) and superoinferior (AFH) di-ameter of the AF was 8.79 mm and 5.98 mm on the right side and 8.11 mm and 5.54 mm on the left side, respec-tively, and the difference between these two diameters

was found to be highly significant (right AFL and right AFH p = 0.00) and (left AFL and Left AFH p = 0.00) (►Table 2).

• The mean ventrodorsal (FTL) and mediolateral (FTW) diameter of the FT was 8.19 mm and 6.56 mm on the right side and 7.31 mm and 6.86 mm on the left Side, respec-tively, and there was significant difference between these two on the right side (right FTL and right FTW p = 0.013]). As opposed to the right side there was no statistically sig-nificant difference between these two parameters on the left side (left FTL and left FTW p = 0.222) (►Table 2).

• Left FTW was significantly more than left AFH (p = 0.001). No statistically significant difference was found between the right FTW and right AFH (p = 0.115) (►Table 2).

• The difference between the mean AFL and FTL of right as well as left sides was found to be statistically insignificant; that is, right FTL and right AFLp = 0.219; left FTL and left AFL p = 0.139 (►Table 2).

• The mean cross-sectional area of the Rt. and Lt. AF was 41.32 mm2 & 35.38 mm2 and Rt. and Lt. FT was 42.53 mm2 & 39.71 mm2 (►Table 3)

• The cross-sectional area of AF was smaller than right FT area and right AF areap = 0.776 and left FT area and left AF area p = 0.259 (►Table 3).

DiscussionMorphological and morphometric knowledge of AF and ipsi-lateral FT, is clinically important as the vertebral artery (VA) passes through it and differences in their dimensions partic-ularly larger dimensions of FT as compared with AF may lead to the compression of VA.

A glance at ►Table 1 reveals that in the present study, the AF were seen in total 11 (13.75%) vertebrae out of 80, 3 (3.75%) being on the right side, 6 (7.5%) on the left side, and 2 (2.5%) bilateral. This is within the range described by previ-ous authors in different populations.8,20

In the present study, ►Table 2 depicts the values obtained for AF and FT. For the AF the mean AFL was 8.79 mm on the right side and 8.11 mm on the left side. The mean AFH was 5.98 mm on the right and 5.54 mm on the left side. Our results showed AFL significantly larger than the AFH on both right and left sides (p = 0.000). It is, therefore, possible that the vertebral artery is compressed superoinferiorly.8 For the foramen transversarium (FT) the mean FTL was 8.19 mm and 7.31 mm, whereas the mean FTW was 6.56 mm and 6.86 mm on right and left sides of atlas vertebra, respectively. The mean FTL on the right side was significantly larger than the FTW (p = 0.013) whereas on left side FTL and FTW was found

Fig. 2 Showing ventrodorsal (VD) and mediolateral (ML) dimensions of foramen transversarium (FT).

Table 1 Showing incidence of arcuate foramen in the present study

Author Year Population Presence of AF

Total bones/sides

Present study

2019 Punjab, India Right Left Bilateral –

3 (3.75%) 6 (7.5%) 2 (2.5%) 11 bones/80 bones (13.75%)

5 (3.12%) 8 (5%) – 13 sides/160 sides (8.12%)



to be insignificant (p = 0.222) in the present study. It is also evident from ►Table 2 that there was a significant differ-ence between the mean left FTW and left AFH (p = 0.001). As opposed to left, the mean right FTW and right AFH was found to be insignificant (p = 0.115). Dimensions of FTL and AFL were also calculated on both the sides but were found to be statistically insignificant.

A look at the comparative analysis of ►Table 4 eluci-dates that the AF and FT dimensions (AFL, AFH, FTL, and FTW) showed no major differences when compared with studies done by previous researchers.8,9,18,21-23 However, there was no mention of AFH by Tubbs et al in American and Iranian population.18,21 It is also revealed from ►Table 4 that the AFL was more than the AFH in the stud-ies done by previous researchers in South African, Indian (Uttar Pradesh and Tamil Nadu), American, Iranian and Kenyan population.8,9,18,21-23 The measurements of FTL and FTW are in concordance with the studies of previous

researchers.9,22,23 However there was paucity of informa-tion on the dimensions of ipsilateral FTL and FTW in South African, American, and Iranian population.8,18,21

As revealed from ►Tables 3 and 5 , the mean cross-sec-tional area of the AF in the present study was 41.32 mm2 and 35.38 mm2 on right and left sides, respectively. It was found to be higher in the present study than in South African,8 American,18 Iranian,21 and Kenyan population22 and less than in UP and Tamil Nadu population.9,23 Most probably the difference might be due to racial factors and ethnic variations. The mean cross-sectional area of the right FT was 42.53 mm2 while that of the left was 39.71 mm2 and comparative analysis of ►Table 5 shows that this is significantly higher than that measured among Iranian21 and Kenyans22 and less than that measured among UP pop-ulation.9 No mention has been made about the ipsilateral FT area among South African, American, and Tamil Nadu population.8,18,23

Table 2 Dimensions of complete arcuate foramina (AF) and ipsilateral foramina transversaria (FT) of the atlas vertebrae in the present study

Author Year/popula-tion

N Right arcuate foramen (mean ± standard deviation)

Left arcuate foramen (mean ± standard deviation)

Right foramen transversarium(mean ± standard deviation)

Left foramen transversarium(mean ± standard deviation)

AFL(V-D)mm

AFH(S-I)mm

AFL(V-D)mm

AFH(S-I)mm

FTL(V-D)mm

FTW(M-L)Mm

FTL(V-D)mm

FTW(M-L)Mm

Present study

2019Punjab, India

80 8.79 ± 0.39440

5.98 ± 0.27884

8.11 ± 1.029828

5.54 ± 0.48286

8.19 ± 0.92275

6.56 ± 0.68303

7.31±0.60717 6.86 ± 0.78638

Groups and p-Value p value = 0.000right AFL and right AFH

p value = 0.000left AFL left AFH

p value = 0.13right FTL and right FTW

p value = 0.222left FTL and left FTW

p value = 0.219right FTL and right AFL

p value = 0.139left FTL and left AFL

p value = 0.115right FTW and right AFH

p value = 0.001left FTW and left AFH

Table 3 Mean cross-sectional area of complete arcuate foramina (AF) and ipsilateral foramina transversaria (FT) of right and left sides of atlas in the present study

Present study, 2019, Punjab, India

S. No. Specimen No.

Area S. No. Specimen No. Area

Right AF Right FT Left AF Left FT

1. 9 44.69 37.39 1. 7 48.26 47.42

2. 12 35.83 48.7 2. 14 36 42.59

3. 26 42.05 30.06 3. 30 30.58 37.14

4. 30 39.8 47.72 4. 39 37.89 45.74

5. 42 44.23 48.78 5. 42 42.37 49.36

Mean ± standard deviation

41.32 ± 3.63347 42.53 ± 8.45559 6. 51 30.02 33.09

p value 0.776 7. 59 31.16 31.14

8 68 26.81 31.21

Mean ± standard deviation

35.38 ± 7.21567 39.71 ± 7.49615

p value –.259

110


Differences in Arcuate Foramina & Ipsilateral Foramina Transversaria Lalit et al.

More notable is the fact that the cross-sectional area of AF was found to be smaller than FT; however, the findings were statistically insignificant. This concurs with the findings of previous researchers.9,18,21,22 This difference in the dimensions of the complete AF and ipsilateral FT of the atlas suggests that the space for vertebral artery to pass through is reduced, resulting in compromised blood flow in the vessel specially during extreme rotational movements of the head and neck.8,24 Our study supports previous assertions that presence of com-plete AF may lead to compression of the vertebral artery in the absence of arterial disease and may be an aggravating factor in case of disease.8,24This compression becomes evidently symp-tomatic in extreme manipulations of the neck.19,25

The presence of this foramen has been associated with chronic tension-type headaches and sensorineural hearing loss26 and shoulder as well as arm pain, neck pain, and vertigo.27 It has also been implicated as a cause of vertebral artery dis-section and stroke in children due to tethering of the vertebral artery within it.28 Osteophytes that narrow the mediolateral diameter can also distort or decrease the inner lumen of the FT and arcuate foramina which can further lead to compression of vertebral artery and compromised blood flow.29,30Thus it is emphasized that bony bridge forming AF may cause external pressure on the vertebral artery as the latter passes through it to the foramen magnum31and may lead to further dilatation or tortuosity of VA and ultimately its insufficiency.32

Table 4 Comparison of average dimensions of complete arcuate foramina (AF) and ipsilateral foramina transversaria (FT) of atlas in different populations

Author Year/population

N Right arcuate foramen

Left arcuate foramen

Ipsilateral right foramen transversarium

Ipsilateral Left foramen transversarium

AFL(V-D)mm

AFH(S-I)mm

AFL(V-D)mm

AFH(S-I)mm

FTL(V-D)mm

FTW(M-L)Mm

FTL(V-D)mm

FTW(M-L)Mm

Mitchell8 1998South African

1354 6.4 5.3 6.6 5.1 – – – –

Hasan et al9 2001UP

350 8.80 7.30 8.50 7.00 8.25 7.70 8.33 8.17

Tubbs et al18 2007aAmerican

75 12 – 12 – – – – –

Tubbs et al21 2007bIranian

60 7 mm – 7 mm – – – – –

Karau et al22 2010Kenya

102 6.29 5.11 6.00 5.16 7.05 6.50 7.04 6.76

Senthil23 2016Tamil Nadu

75 8.80 7.70 8.70 8.60 7.70 6.70 8.00 6.00

Present study 2019Punjab, India

80 8.79 ±.39440

5.98 ±.27884

8.11 ± 1.29828

5.54 ±.48286

8.19 ±.92275

6.56 ±.68303 7.31 ±.60717

6.86 ±.78638

Abbreviations: Arcuate foramen length, AFL; arcuate foramen height, AFH; foramen transversarium length, FTL; foramen transversarium width FTW.

Table 5 Comparison of mean cross-sectional area of complete arcuate foramina (AF) and ipsilateral foramina transversaria (FT) of atlas in different populations

Author Year Population N Right arcuate foramen(area)mm2

Left arcuate foramen(area)mm2

Right foramina transversaria(area) mm2

Left foramina transversaria(area) mm2

Mitchell8 1998 South African 1354 26.6 ± 5.9 26.6 ± 6.5 – –

Hasan et al9 2001 UP 350 46.75 50.28 53.79 51.46

Tubbs et al18 2007a American 75 12.5 mm –

Tubbs et al21 2007b Iranian 60 14.2 18.0

Karau et al22 2010 Kenya 102 23.44 24.98 36.30 37.20

Senthil23 2016 South Indian(Tamil Nadu)

75 53 59 – –

Present study 2019 Punjab, India 80 41.32± 3.63347

35.387.21567

42.53± 8.45559

39.717.49615



ConclusionThis is among the first study providing information on the morphometry of complete AF and ipsilateral FT and their implications in Punjab, and the results are comparable to that in other populations. The observation of the area of arcuate foramina being smaller than the ipsilateral FT suggests that they are an important cause of vertebral artery compression. Thus, knowledge of such variations of the atlas vertebra is important for radiologists, otolaryngologists, neurologists, and orthopedicians. It is suggested that a correlation should be worked out between dimensions of Ponticuli, FT, and VA by angiograms, X-rays, and clinical symptoms, keeping in view the valuable inputs from the study of osteology and dissec-tion of the cadavers. Patients presenting with vertebrobasilar insufficiency, vertebral artery dissection, and cervicogenic syndromes should be evaluated to explore the possibility of the presence of atlas bridges as etiological factor.

Conflict of InterestNone.

References

1 William M, Newell RLM, Collin P, The back: cervical vertebrae. In: Standring S, Ellis H, Haely JC, Johson D, Williams A, eds. Gray’s Anatomy. 39th ed. Edinburg, London: Elsevier Churchill Livingstone; 2005:742–746

2 Romanus T, Tovi A. A variation of the atlas. Roentgenolgic inci-dence of a bridge over the groove on the atlas for the vertebral artery. Acta Radiol Diagn (Stockh) 1964;2:289–297

3 Macalister A. Notes on the homologics and comparative anat-omy of the atlas and axis. J Anat and Physiol 1869;3:54–64

4 Macalister A. Notes on the development and variations of the atlas. J Anat Physiol 1893;27(Pt 4):519–542

5 Le double AF. Traiteu des variations de la colonne vertebrae de i’homme et de leur signification au point de vue de i’anthro-pologique zoologique. Paris: vigot fréres; 1912.

6 Pyo J, Lowman RM. The ponticulus posticus of the first cervical vertebra. Radiology 1959;72(6):850–854

7 Lamberty BG, Zivanović S. The retro-articular vertebralartery ring of the atlas and its significance. Acta Anat (Basel) 1973;85(1):113–122

8 Mitchell J. The incidence and dimensions of the retroar-ticular canal of the atlas vertebra. Acta Anat (Basel) 1998 a;163(2):113–120

9 Hasan M, Shukla S, Siddiqui MS, Singh D. Posterolateral tunnels and ponticuli in human atlas vertebrae. J Anat 2001;199(Pt 3): 339–343

10 Unur E, Erdogan N, Ülger H, Ekinci N, Oztürk O. Radiographic incidence of complete arcuate foramen in Turkish population. Erciyes Med J 2004;26:50–54

11 Lalit M, Piplani S, Arora AK, Kullar JS, Tripta Sharma T. Incidence of atlas bridges and tunnels—their phylogeny, ontogeny and clinical implications. Rev Arg de Anat Clin 2014;6(1):26–34

12 Taitz C, Nathan H. Some observations on the posterior and lat-eral bridge of the atlas. Acta Anat (Basel) 1986;127(3):212–217

13 Ebraheim NA, Xu R, Ahmad M, Heck B. The quantitative anatomy of the vertebral artery groove of the atlas and

its relation to the posterior atlantoaxial approach. Spine 1998;23(3):320–323

14 Anderson RE, Shealy CN. Cervical pedicle erosion and rootlet compression caused by a tortuous vertebral artery. Radiology 1970;96(3):537–538

15 Paraskevas G, Papaziogas B, Tsonidis C, Kapetanos G. Gross morphology of the bridges over the vertebral artery groove on the atlas. Surg Radiol Anat 2005;27(2):129–136

16 Elliott RE, Tanweer O. The prevalence of the ponticulus posti-cus (arcuate foramen) and its importance in the Goel-Harms procedure: meta-analysis and review of the literature. World Neurosurg 2014;82(1–2):e335–e343

17 Huang MJ, Glaser JA. Complete arcuate foramen precluding C1 lateral mass screw fixation in a patient with rheumatoid arthritis: case report. Iowa Orthop J 2003;23:96–99

18 Tubbs RS, Johnson PC, Shoja MM, Loukas M, Oakes WJ. Fora-men arcuale: anatomical study and review of the literature. J Neurosurg Spine 2007b;6(1):31–34

19 Limousin CA. Foramen arcuale and syndrome of Barre-Lieou. Its surgical treatment. Int Orthop 1980;4(1):19–23

20 Lalit M, Piplani S, Verma P. Study of dimensions of retroartic-ular bony rings in human atlas vertebrae: an original research article. Int J Anat Res (IJAR) 2016;4(3):2526–2530

21 Tubbs RS, Shoja MM, Shokouhi G, Farahani RM, Loukas M, Oakes WJ. Simultaneous lateral and posterior ponticles result-ing in the formation of a vertebral artery tunnel of the atlas: case report and review of the literature. Folia Neuropathol 2007a;45(1):43–46

22 Karau Bundi P, Ogengo JA, Hassanali J, Odula PO. Morphometry and variations of bony poticles of the atlas vertebrae in Ken-yans. Int J Morphol 2010;28(4):1019–1024

23 Babu SK. Arcuate foramen of atlas vertebra. Innovare Journal of Medical. Science 2016;4(3):22–24

24 Mitchell J. The incidence of the lateral bridge of the atlas verte-bra. J Anat 1998;193(pt 2):283–285

25 Parkin PJ, Wallis WE, Wilson JE. Vertebral artery occlusion following manipulation of the neck. N Z Med 1978;88(625): 441–443

26 Koutsouraki E, Avdelidi E, Michmizos D, Kapsali SE, Costa V, Baloyannis S. Kimmerle’s anomaly as a possible causative factor of chronic tension-type headaches and neurosensory hearing loss: case report and literature review. Int J Neurosci 2010;120(3):236–239

27 Cakmak O, Gurdal E, Ekinci G, Yildiz E, Cavdar S. Arcu-ate foramen and its clinical significance. Saudi Med J 2005;26(9):1409–1413

28 Cushing KE, Ramesh V, Gardner-Medwin D, et al. Tethering of the vertebral artery in the congenital arcuate foramen of the atlas vertebra: a possible cause of vertebral artery dissection in children. Dev Med Child Neurol 2001;43(7):491–496

29 Nathan H. Osteophytes of the vertebral column: an anatomical study of their development according to age, race and sex. J Bone and Joint Surg 1962;44A(2):243–268

30 Malhotra VK, Tewari SP, Bajpai RN. Study of vertebral artery foramen on atlas vertebra. J Anat Soc India 1979;28(2):103–105

31 Krishnamurthy A, Nayak SR, Khan S, et al. Arcuate foramen of atlas: incidence, phylogenetic and clinical significance. Rom J Morphol Embryol 2007;48(3):263–266

32 Dahipale VP, Bahetee BH. The retro articular vertebral artery ring of the atlas and its significance. J Anat Soc India 2009;58(2):149–151

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