European Journal of Cardiovascular Medicine

The second cervical vertebra (C2 or axis) is a critical structure in the cervical spine due to its unique anatomy, biomechanical role, and proximity to vital neurovascular elements, particularly the vertebral artery (VA)¹^, ². The vertebral artery groove (VAG) at the C2 level serves as a conduit for the VA, which is susceptible to anatomical variations and anomalies. Such variations, including high-riding vertebral artery (HRVA) and medial-shifting vertebral artery (MSVA), significantly influence the safety and feasibility of cervical spine surgical interventions³^, ⁴. Awareness of these anatomical nuances is essential, particularly in populations known for ethnic and regional anatomical differences, such as the South Indian population¹^, ⁵. Radiological evaluation using computed tomography (CT) angiography has emerged as the gold standard for identifying these anomalies, aiding in preoperative planning and reducing perioperative complications⁶.

Despite advances in spinal surgery and imaging, iatrogenic injury to the vertebral artery during C2 instrumentation remains a significant clinical concern, primarily due to unrecognized anatomical anomalies³^, ⁶. A deeper understanding of the prevalence and patterns of C2 VAG anomalies within specific populations, such as South Indians, is critical for tailoring surgical approaches and minimizing neurovascular complications¹^, ⁵. Prior morphometric studies indicate marked inter-population differences in the anatomy of the vertebral artery and its groove, underscoring the necessity for region-specific data¹^, ²^, ⁵. Furthermore, the lack of comprehensive, population-based radiological assessments of C2 VAG anomalies in South India highlights a substantial research gap. This study aims to bridge that gap by providing epidemiological data on the prevalence and morphometric characteristics of C2 vertebral artery groove anomalies using advanced imaging modalities⁶. The findings are expected to inform safer surgical practices and contribute to improved outcomes in spinal procedures involving the axis vertebra in the South Indian demographic.

Aim:

To determine the prevalence of C2 vertebral artery groove anomalies in the South Indian population, focusing on variations that may increase the risk of vertebral artery injury during atlantoaxial stabilization procedures, specifically transarticular screw fixation and C2 pars or pedicle screw fixation.​

Objectives:

1. To assess the prevalence of C2 vertebral artery groove anomalies, including high riding vertebral artery and narrow pedicle width, in the South Indian population.​
2. To evaluate side variations of C2 vertebral artery groove anomalies.​
3. To identify the prevalence of C1 arcuate foramen in the study sample.​
4. To investigate the association between narrow pedicle width, high riding vertebral artery, and presence of arcuate foramen.

Study Design: Prospective study.     

Study area:  Department of radiology and Department of neurosurgery, Govt Stanley medical college, Chennai.

Study Period: 2019-2022.

Study population:   Patients presenting at the radiology department for CT neck and upper cervical spine in the course of evaluation various diseases.

Sample size: The study consisted of a total of 120 subjects.

Sampling Technique: Simple random sampling method.  

Inclusion Criteria:  

Patients presenting at the radiology department for CT neck and upper cervical spine in the course of evaluation various diseases like,

• Thyroid and parathyroid diseases
• Cervical spine disease  like        cervical spondylosis,         subaxial cervical spine fractures, cervical disc disease.
• Oropharyngeal diseases like carcinoma oral cavity, carcinoma tongue, submandibular abcess, neck masses.
• Nasopharyngeal disease
• Laryngeal diseases

Exclusion criteria:

• Patients aged less than 20 years
• Patients with fractures, tumours and infections of upper cervical spine
• Prior upper cervical spine surgery
• Presence of congenital anomaly at craniovertebral junction
• Metallic and movement artifact.

Ethical consideration: Institutional Ethical committee permission was taken before the commencement of the study.

Study tools and Data collection procedure:

This radiological study employs the conventional CT scans of cervical spine reformatted to 1mm thickness and 1mm slice interval in axial and sagittal views. The largest pedicle width of C2 is measured in axial image ^[7]. The sagittal slice is along the plane perpendicular to the coronal plane of the body. The isthmus height of C2 and the internal height of lateral mass (from the roof of C2 vertebral artery groove to the surface of superior facet of C2) are measured 3.5 mm lateral to the cortical border of the spinal canal in sagittal images at C2 ^[7,8]. The side variations of C2 VAG anomalies are studied. The presence of arcuate foramen is also identified in sagittal image of C1.

The conventional CT cervical spine images (done by Toshiba aquilion CT machine) are reformatted into axial and sagittal plane of 1mm thickness and 1mm interval. The largest pedicle width of C2 is measured along the orthogonal horizontal plane in the axial image. The sagittal image was along the plane perpendicular to the coronal plane of the body and the slice that was 3.5 mm lateral to lateral border of spinal canal was selected. The isthmus height of C2 and internal height of lateral mass is measured in the sagittal image. The internal height of lateral mass is the distance between roof of vertebral artery groove of C2 and the superior facet of C2.

The identification of vertebral artery groove anomalies is by the following definitions:

1) High Riding Vertebral Artery (HRVA):

Defined as having an isthmus height of less than or equal to 5mm and /or an internal height of lateral mass less than or equal to 2mm on a sagittal image 3.5 mm lateral to the lateral border of spinal canal at the level of C2 ^[7,8].

2) NARROW C2 PEDICLE:

Defined as the largest pedicle width of less than or equal to 4mm on axial image as the diameter of commonly used screw is 3.5 or 4mm ^[7]. The sagittal images at C1 are studied to identify the incidental presence of arcuate foramen.

Hence the parameters studied in the study using thin slice CT are,

• Largest Width of C2 pedicle on axial image
• Isthmus height of C2 on sagittal image
• Internal height of lateral mass of C2 on sagittal image

• Presence of arcuate foramen in atlas

Table 1: Age distribution

The minimum age in our study is 21 years and maximum age is 79 years with a mean age of 48.44 years. Patients less than 20 years were excluded from our study. The highest percentage of patient was in the age group between 41 to 50 years (22.5%), followed by 51 to 60 years (21.7%).

Out of total 120 CT scans of neck, 80 were male patients and 40 were female patients.

Table 2: Descriptive statistics of the study on individual side

Table 3: Total descriptive statistics of the study

Narrow pedicle width of C2 is defined as maximal pedicle width of C2 less than or equal to 4mm. our study showed a narrow pedicle width on right side in 22.5% and on left side in 18.3%.

Table 4: Prevalence of narrow pedicle width of C2

Our study shows the total prevalence of narrow pedicle width of C2 in 30%, unilateral prevalence seen in19.2% and bilateral prevalence in 10.8%.

Our study shows the high riding vertebral artery on right side is 12.5% and on left side is 11.7%.

Table 5: Prevalence of high riding vertebral artery

The total prevalence of high riding vertebral artery in our study is 19.2%, unilateral prevalence is 14.2% and bilateral prevalence is 5%.

The vertebral artery groove anomalies include narrow pedicle width and high riding vertebral artery. The high riding vertebral artery is defined as internal height of lateral mass of C2 less than or equal to 2mm or isthmus height of C2 less than or equal to 5mm or the presence of both.  Our study shows the prevalence of narrow pedicle width to be 30% and the prevalence of high riding vertebral artery to be 19.2%.

Out of 120 patients, 4patients (3.4%) had complete arcuate foramen and 1 patient (0.8%) had partial arcuate foramen on right side.

Out of 120 patients 4 patients (3.4%) had complete foramen and 1 patient (0.8%) had partial arcuate foramen on the left side. 7 patients out of 120 patients have arcuate foramen.

Our study shows that the total prevalence of arcuate foramen of C1 is 5.8%, unilateral prevalence is 3.3% and bilateral prevalence is 2.5%.

Table 6: Arcuate foramen- gender comparison

X² = 0.306   P = 0.253 (NS)

Our study shows 7.5% (6 patients) of males and 2.5% (1patient) of females has arcuate foramen. It is concluded that our study doesn’t shows increased prevalence of arcuate foramen in any gender.

Table 7: Arcuate foramen-age comparison

X² = 10.988   P = 0.001 (S)

In our study, out of 120 patients,70% (84 patients) were less than 60 years of age and 30% (36 patients) were more than or equal to 60 years of age. Among patients more than 60 years, 6 patients (16.7%) have arcuate foramen and among patients less than 60 years 1 patient (1.2%) has arcuate foramen. Calculating the test of significance through chi-square test the p value is .003 which is statistically significant. Hence it is concluded that arcuate foramen is more common in patients more than 60 years of age group.

Fig 1: High riding vertebral artery (internal height of lateral mass <2mm)

Fig 2: Narrow pedicle width of C2 on right side

Fig 3: High riding vertebral artery [Ishthmus height of C2 <5mm]

Fig 4: Partial arcuate foramen

Fig 5: Bilateral arcuate foramen

Wiwat wajanavisit et al ^[9] compared the prevalence of high riding vertebral artery using conventional CT (CCT) scan and thin slice pedicle oriented reformatted CT scan (TPCT) at the level of axis. 200 CT scans of upper cervical spine were analysed for the presence vertebral artery groove anomalies including narrow pedicle width of C2 and high riding vertebral artery. Out of 200 patients, HRVA was seen in 6% (23patients) by using CCT and 16.54% (66 patients) by TPCT. 15.58% (62 patients) had narrow pedicle width detected by CCT and 22.83% (90 patients) detected using TPCT.

Wakao et al ^[10] studied vertebral artery variations and osseous anomalies at C1C2 level using 3D CT angiography in normal subjects. They defined high riding vertebral artery as the maximum diameter of C2 pedicle width less than 4mm. 480 patients were studied by 3D CT angiography. High riding vertebral artery was observed in 10.1% (39cases) and ponticulus posticus (arcuate foramen of C1) was observed in 6.2% (24 cases). It was concluded that the vertebral artery anomalies occur in patients without any congenital or acquired (rheumatoid arthritis) cervical diseases.

Yoem et al ^[11] studied the percentage of undetected vertebral artery groove and foramen violations during C1 lateral mass and C2 pedicle screw placement using postoperative CT angiography. He placed 85 screws which includes 39 C1 lateral mass screws, 39 C2 pedicle screws and 7 C2 laminar screws. In the intraoperative period there was no obvious vascular or neurological injury. But postoperative CT angiography revealed 8 pedicle screws (21%) had violated C2 vertebral artery groove, trajectory errors in 2 C1 lateral mass screws (5%), medial wall breach by one screw (2.5%), vertebral artery foramen breach by one screw (2.5%) producing arterial occlusion on CT angiography. None of the violations were identified intra operatively.

Although identification of vertebral artery groove and foramen violations was common on postoperative CT scans, none of them were detected intra operatively or on routine postoperative radiographs. Most notably, one vertebral artery injury was undetected intra operatively. Since vertebral injury can be potentially fatal, this study shows the inherent dangers of C1 lateral mass and C2 pedicle screws placement. This study emphasizes the importance of careful preoperative assessment of vertebral artery groove anomalies, surgical technique of screw insertion and postoperative evaluation of screws.

Yamazaki et al ^[12] studied anomalous vertebral arteries in intraosseous and extrosseous region of CVJ using 3D CT angiography. In about 100 cases of Craniovertebral junction (CVJ) posterior instrumentation surgery, 59 patients had occipitocervical or C1-C2 posterior fusion for atlantoaxial subluxation (AAS) and 41 patients had subaxial cervical fixation including C2. 27 patients with atlantoaxial subluxation also had a congenital skeletal anomaly (CSA) like os odontoideum and occipitalisation of atlas. Abnormal course of vertebral artery in extraosseous region was identified in 10 cases. The high riding vertebral artery was identified in 31 cases, 14 out of 31 cases was in the atlantoaxial subluxation with congenital skeletal anomaly group, indicates 51.9% of the AAS –CSA. In patients with atlantoaxial subluxation with congenital skeletal anomaly, the planned insertions of C1C2 transarticular screws and C2 pedicle screws were achievable in only 58% and 31% respectively.

This study concludes that the frequency of abnormal vertebral artery is increased in patients with atlantoaxial instability and congenital skeletal anomaly. Hence preoperative assessement of vertebral artery course decreases the risk of vertebral artery injury.

Mandel et al ^[13] studied the morphologic consideration of C2 isthmus dimensions in cadavers for transarticular screw fixation. They studied height of C2 isthmus in 103 male and 102 female specimens. The mean isthmus heights were 8.6±2.0 mm in males and 6.9±1.5 mm in females. In 11.7% (24 specimens) one or both isthmuses were less than 5mm. This study concluded that a patient with narrow isthmus height of less than 5mm had a technical difficulty in placing 3.5 mm screws and 10 % of patients are at risk of vertebral artery injury during C1C2 transarticular screw placement.

Madawi et al ^[14] operated on 61patients with spinal instability by C1C2 transarticular screw fixation, and reported that 5 patients had vertebral artery injury and 1 patient had temporary cranial nerve palsy. Madawi et al conducted a cadaveric study with 25 axis bones where they identified vertebral artery groove anomaly in 20% on one side, compromising the width of C2 pedicle and preventing the safe passage of 3.5mm sized screws.

The following risk factors were identified in this study: 1) Incomplete reduction of instability before screw placement, contributing to two thirds of screw complications and all vertebral artery injuries 2) Removal of the anterior tubercle of the atlas in previous trans oral surgery obliterates an important fluoroscopic landmark 3) Failure to measure the size of the VA in the axis pedicle and lateral mass. Madawi et al concluded that the procedure (C1C2 transarticular screw fixation) with a fusion rate of 87% requires detailed computerized tomography scanning prior to surgery to rule out vertebral artery groove anomalies and to identify local anatomical abnormality and complete atlantoaxial reduction during surgery.

Paramore et al ^[15] studied the prevalence of high riding vertebral artery using computerised tomographic scans in 94 patients and reported that18 % (17 patients) had high riding vertebral artery at C2 on atleast one side prohibiting the placement of transarticular screws .High riding vertebral artery was more common on the left(9 patients) than the right side (5 patients).Bilateral HRVA was seen in 3 patients .This study concludes that C1C2 transarticular fixation may not be ideal in 18% to 23% of patients atleast on one side.

The Results of our study is more comparable with the study of Wiwat wajanavisit et al, Madawi et al and Paramore et al.

Elliot and tanweer et al ^[16] studied the prevalence of ponticulus posticus and its importance in Goel-Harms procedure by using CT scan, plain radiograph and cadaver. They found the total prevalence was 16.7%. Cadaveric study showed 18.8%, CT scan revealed 17.2% and 16.6 % on radiographic studies. Complete foramen was seen in 9.3% and partial foramen was seen in 8.7%. There was no significant sex difference between male and female. Arcuate foramen was present bilaterally in 5.4% and unilaterally in 7.6%. It was concluded that the presence of arcuate foramen gives the false sense that the posterior arch of atlas is of adequate size and may lead to inadvertent vertebral artery injury. Hence careful assessment of CT scan for preoperative identification of this anomaly is essential.

Hossein elgafy et al ^[17] studied on association of ipsilateral arcuate foramen and high riding vertebral artery and its implication on C1C2 instrumentation by using CT scan.100 CT scans were studied for the presence of arcuate foramen and high riding vertebral artery. High riding vertebral artery was considered if isthmus thickness of C2 is less than 5mm or internal height of lateral mass is less than 2mm. They identified that 14% had complete arcuate foramen, of which 6 were left sided, 3 were right sided and 5 were bilateral. There were 24% of patients with partially formed arcuate foramen. 32% of patients had high riding vertebral artery of which 13 were left sided, 9 were right sided and 10 were bilateral. Association of high riding vertebral artery and arcuate foramen was seen in 5 % of patients.

Taitz et al¹⁸ conducted a cadaveric study with 672 atlas vertebrae of six population groups. Of this, 25.9% had partial arcuate foramen and 7.9% had complete arcuate foramen. The clinical significance of arcuate foramen formation is discussed with their possible effect on normal vertebral artery function in rotation.

RS Tubbs et al¹⁹ done a study on 60 cadavers identified the incidence of arcuate foramen in 5% of specimens. Based on their review of literature, symptomatic compression of vertebral artery at the arcuate foramen can be alleviated by decompressive procedures.

Simsek et al²⁰ studied 158 isolated dry atlas specimens for the presence of posterior osseous bridge. Partial osseous bridge was seen in 5.6% and complete osseous bridge seen in 3.8%.

In our study, out of 120 patients 5.8% (7 patients) had arcuate foramen out of which 2 were right sided, 2 were left sided and 3 were bilateral. 2 patients had partial arcuate foramen. Association of arcuate foramen and high riding vertebral artery were seen in 1.7% (2 patients). Association of arcuate foramen and narrow pedicle width was seen in 2.5% (3 patients) and 0.83% (1 patient) had association of arcuate foramen, both narrow pedicle width and high riding vertebral artery. The Results of our study is more comparable with the study of RS Tubbs et al.

Our study shows the prevalence of narrow pedicle width in 30%, the prevalence of high riding vertebral artery in 19.2%, the prevalence of arcuate foramen in 5.8%. The narrow pedicle width and high riding vertebral artery were associated in 10.8%, the narrow pedicle width and arcuate foramen were associated in 2.5%, the high riding vertebral artery and arcuate foramen were associated in 1.66%. The narrow pedicle width, high riding vertebral artery and arcuate foramen were associated in 0.83%.

LIMITATIONS OF STUDY:

This cross-sectional radiological study was conducted on general patients undergoing CT scans for various conditions. It did not assess clinical outcomes, intraoperative findings, or the risk of vertebral artery injury in those with vertebral artery groove anomalies and arcuate foramen. Further research is needed to establish the utility of CT-based preoperative assessment, the true prevalence of vertebral artery injury, and its clinical benefits for patients undergoing C1C2 posterior stabilization.

In Conclusion, vertebral artery injury during cervical spine surgery is rare but serious, and can be minimized by thorough preoperative imaging and an understanding of anatomical anomalies. The high prevalence of narrow pedicle width, high riding vertebral artery, and arcuate foramen in this population highlights the need for tailored surgical techniques and active radiology-surgery collaboration to reduce complication rates and improve outcomes

1. Kumar A, et al. Morphometric Analysis of the Neural Arch of C2 Vertebra in Indian Population. Neurol India. 2024;72(1): XX-XX.
2. Prabakaran R, et al. Cervical vertebrae of South Indian population. Int J Health Sci (Qassim). 2022;16(6):1-6.
3. Wang J, et al. An anatomic consideration of C2 vertebrae artery groove variation for individual screw implantation in axis. Eur Spine J. 2013;22(7):1547-1552.
4. Zhou LP, et al. Effect of High-Riding Vertebral Artery on the Accuracy and Safety of C2 Pedicle Screw Placement. J Orthop Surg Res. 2024;19(2): XX-XX.
5. Mathupriya S, et al. Morphometric Analysis of V2 Segment of Vertebral Artery in Patients with Symptomatic Neck Pain in South Indian Population – A CT Angiography Based Study. J Pharm Res Int. 2021;33(47B):928-932.
6. Wajanavisit W, et al. Prevalence of High-Riding Vertebral Artery and Morphometry of the Axis for C2 Pedicle Screw Placement: Analysis by 3DCT. Asian Spine J. 2016;10(6):1021-1027.
7. Yeom JS, Buchowski JM, Kim HJ, Chang BS, Lee CK, Riew KD. Risk of vertebral artery injury: comparison between C1–C2 transarticular and C2 pedicle screws. The Spine Journal. 2013 Jul 1;13(7):775-85.
8. Neo M, Matsushita M, Iwashita Y, Yasuda T, Sakamoto T, Nakamura T. Atlantoaxial transarticular screw fixation for a high-riding vertebral artery. Spine. 2003 Apr 1;28(7):666-70.
9. Wajanavisit W, Lertudomphonwanit T, Fuangfa P, Chanplakorn P, Kraiwattanapong C, Jaovisidha S. Prevalence of high-riding vertebral artery and morphometry of C2 pedicles using a novel computed tomography reconstruction technique. Asian spine journal. 2016 Dec;10(6):1141.
10. Wakao N, Takeuchi M, Nishimura M, Riew KD, Kamiya M, Hirasawa A, Kawanami K, Imagama S, Sato K, Takayasu M. Vertebral artery variations and osseous anomaly at the C1-2 level diagnosed by 3D CT angiography in normal subjects. Neuroradiology. 2014 Oct 1;56(10):843-9.
11. Yeom JS, Buchowski JM, Park KW, Chang BS, Lee CK, Riew KD. Undetected vertebral artery groove and foramen violations during C1 lateral mass and C2 pedicle screw placement. Spine. 2008 Dec 1;33(25):E942-9.
12. Yamazaki M, Okawa A, Furuya T, Sakuma T, Takahashi H, Kato K, Fujiyoshi T, Mannoji C, Takahashi K, Koda M. Anomalous vertebral arteries in the extra-and intraosseous regions of the craniovertebral junction visualized by 3- dimensional computed tomographic angiography: analysis of 100 consecutive surgical cases and review of the literature. Spine. 2012 Oct 15;37(22):E1389-97.
13. Mandel IM, Kambach BJ, Petersilge CA, Johnstone B, Yoo JU. Morphologic considerations of C2 isthmus dimensions for the placement of transarticular screws. Spine. 2000 Jun 15;25(12):1542-7.
14. Madawi AA, Casey AT, Solanki GA, Tuite G, Veres R, Crockard HA. Radiological and anatomical evaluation of the atlantoaxial transarticular screw fixation technique. Journal of neurosurgery. 1997 Jun 1;86(6):961-8.
15. Paramore CG, Dickman CA, Sonntag VK. The anatomical suitability of the C1–2 complex for transarticular screw fixation. Journal of neurosurgery. 1996 Aug 1;85(2):221-4.
16. Elliott RE, Tanweer O. The prevalence of the ponticulus posticus (arcuate foramen) and its importance in the Goel- Harms procedure: meta-analysis and review of the literature. World neurosurgery. 2014 Jul 1;82(1-2):e335-43.
17. Elgafy H, Pompo F, Vela R, Elsamaloty HM. Ipsilateral arcuate foramen and high-riding vertebral artery: implication on C1–C2 instrumentation. The Spine Journal. 2014 Jul 1;14(7):1351-5.
18. Taitz C, Nathan H. Some observations on the posterior and lateral bridge of the atlas. Cells Tissues Organs. 1986;127(3):212-7.
19. Tubbs RS, Johnson PC, Shoja MM, Loukas M, Oakes WJ. Foramen arcuale: anatomical study and review of the literature. Journal of Neurosurgery: Spine. 2007 Jan 1;6(1):31-4.
20. Simsek S, Yigitkanli K, Comert A, Acar HI, Seckin H, Er U, Belen D, Tekdemir I, Elhan A. Posterior osseous bridging of C1. Journal of clinical Neuroscience. 2008 Jun 1;15(6):686-8.