An Exploratory Morphometric Study of the Atlantal Part of Vertebral Artery

doi:10.21203/rs.3.rs-3082363/v1

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An Exploratory Morphometric Study of the Atlantal Part of Vertebral Artery

https://doi.org/10.21203/rs.3.rs-3082363/v1

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Purpose:

The vertebral artery (VA) is a major artery in the neck region. It arises from the first segment of the subclavian artery. The artery then traverses through the transverse foramina of each cervical vertebra leaving the transverse foramina of seventh cervical vertebrae. At the level of lower border of pons, the VA from opposite sides unite its fellow artery to form the basilar artery. There are a quite good number of CT studies of this region, whereas there are limited cadaveric studies of this region. Thus, this study aims to fill up the research gap, by doing morphometric cadaveric study of V3 segmental VA in reference to length diameter and length. And Angle of the vertical and horizontal part of V3 (Atlantal) segment of vertebral artery

Methods:

The study was conducted in the 40 vertebral arteries from 20 embalmed cadavers .

Results:

The mean length of right and left VA on each part was almost similar except for the mean length of H part (R- 38.937mm & L-40.237mm) and total length of V3 segment (R- 66.87mm & L-70.350mm).

Conclusion:

This will be of great importance to neurosurgeons who intend to operate a limited part (any of the 3 parts) of V3 segment of VA. The mean values of parameters resulted in this study gives an average measurements or safe limits to the surgeons for the safe surgical procedures like occipital condyle screw technique

Vertebral artery

Neurosurgeons

transverse foramina

V3 segment

suboccipital triangle

The vertebral artery (VA) is a major artery in the neck region. It arises as a branch from the posterior-superior aspect, of the first segment of the subclavian artery. The artery then traverses through the transverse foramina of each cervical vertebra leaving the transverse foramina of seventh cervical vertebrae. This justifies that diameter of VA is not more than the diameter of the cervical foramina. Later, this artery turns medially behind the atlas' lateral masses and enters the skull through the foramen magnum. At the level of lower border of pons, the VA from opposite sides unite its fellow artery to form the basilar artery. This defines the typical course of VA. There are instances when the artery enters the cervical foramina through the C4, C5, or C7 cervical vertebrae [8].

Despite of some ambiguity put forth by different authors in understanding the segmental limits of its course, this study denominated four segments based on its position. 1- pre-foraminal (V1) segment: runs from its place of origin in subclavian artery till the transverse foramen of sixth cervical vertebrae (C6) [1], 2- foraminal (V2) segment: stretches from C6 transverse foramina to the C2 cervical foramina transversarium, 3- atlantal /extradural/extraspinal (V3) segment: lies at craniovertebral junction, commencing from C2 transverse foramen and extends to the foramen magnum [3, 9] and 4- intradural/intracranial (V4) segment: is entirely intracranial and runs from the dura at the lateral edge of the posterior atlanto-occipital membrane to the vertebrobasilar junction. [6, 13, 20].

Amidst these segments briefed above, this study puts emphasis on the third segment (V3) of VA. This V3 segment extends from the C2 transverse foramen to the foramen magnum at the craniovertebral junction [1, 9]. The artery exits slightly lateral from the transverse foramen of the axis (C2) to enter the transverse foramen of the atlas (C1). Later this segment curls backwards and medially to the lateral masses of atlas, to lie horizontally in the grooves of its posterior arch. And finally, the bottom edge of the atlanto-occipital membrane and dura mater are pierced before it passes through the foramen magnum and enters the cerebral cavity [3]. This whole V3 segment of the artery lies in the suboccipital triangle, bounded by the suboccipital group of muscles and covered up by the deep muscles of neck posteriorly. In addition to the anatomical complex of VA that is located in the suboccipital region, it also comprises the periarterial neural plexus, its branches, and the adjacent spinal nerves, all of which are cushioned in the venous compartment. Vascular, neoplastic, degenerative, congenital, or traumatological diseases could develop in this region, requiring a detailed understanding of this complex anatomical system for appropriate surgical management [2].

Due to the V3 segment's clinical importance, the microsurgical anatomy of this section of the VA has previously been studied like that of this study [18]. A VA violation will result in deadly complications because this section is closely related to the posterior fossa's floor. Before trying surgery at the posterior fossa and cranio-cervical junction, it is therefore imperative to have a thorough understanding of the anatomy and course of the VA, particularly the V3 segment [12], as doing so could result in iatrogenic damage [3]. Studies have been done on the suitability of the C1 and C2 vertebrae's bone structure for screw insertion, but very few have been done on the region's vascular structure for instrumentation [5]. A bone bridge that arches from the atlas lateral mass to the groove's posterior boundary is responsible for creating an abnormal foramen, which is mentioned in a few studies as well [18].

There are a quite good number of CT studies of this region, whereas there are limited cadaveric studies of this region. Thus, this study aims to fill up the research gap, by doing morphometric cadaveric study of the length, diameter and angle to facilitate safe exposure of atlantal part of VA during neurosurgical procedures.

The present study was carried out in the Anatomy department after obtaining the institutional ethical committee clearance (IEC674/2021). For this study, 40 vertebral arteries from 20 embalmed (10% formalin) cadavers which were used by first-year medical students for routine dissection classes were utilized. We clearly exposed the suboccipital triangle muscles namely: Rectus Capitis Posterior Major (RCP Major), Rectus Capitis Posterior Minor muscles (RCP Minor); superomedially, Obliquus Capitis Inferior (OCI); below, Obliquus Capitis Superior (OCS); superolaterally. These suboccipital muscles composing the triangle were detached from their bony attachments in order to clearly observe and measure the established parameters of VA. Using blunt forceps and a periosteal elevator device, the region around the atlantoaxial joint, C1 posterior arch, spinous process, and the transverse processes of C1 and C2 were rendered visible. The C2 ganglion, the ramus (ventral/dorsal) of the C2 spinal nerve, and the full course of the atlantic portion of the VA were readily visible throughout this complete dissection (Fig1).

This V3 segment of VA is further subdivided into 3 parts for the feasibility of the study. These segments are labeled as vertical part, horizontal part and exit part. The vertical part is the part of the VA between the transverse foramina of axis (C2) and atlas (C1). The horizontal part is the part that lies horizontally in the posterior groove of the atlas. While exit part is the part of the segment that exits behind the atlanto-occipital membrane to continue as the V4 segment.

A predetermined distance was maintained between the dissected area and the camera and appropriate photos were taken. This was done to prevent the image J software from incorrectly or improperly calculating the angle between the Vertical (V) and Horizontal (H) part of VA. The lined-up parameters' measurements were made.

The parameters included in the study:

The length of various parts of V3 segment of VA –

Length of Vertical part: on Right side (LVR) & on Left side (LVL) (Fig2)
Length of Posterior arch of C1 corresponding to V3 segment: on Right side (LPR) & on Left side (LPL) (Fig2)
Length of Horizontal part: on Right side (LHR) & on Left side (LHL) (Fig2)
Length of Total V3 segment: on Right side (LTR) & on Left side (LTL) (Total length of V3 segment = Adding up the measured length of vertical part, posterior arch of C1 and horizontal part)

Diameter of V3 segment of VA (at the mid-length of each part), as-

Diameter of Vertical part: on Right side (DVR) & on Left side (DVL)
Diameter of Horizontal part: on Right side (DHR) & on Left side (DHL) (Fig3)
Diameter of Exist part: on Right side (DER) & on Left side (DEL) (Fig3)
Diameter Average (average of V, H and E parts): on Right side (DAR) & on Left side (DAL)

Angle between Vertical and Horizontal part of V3 segment: on Right side (AR) & on Left side (AL)

The digital Vernier calliper and imageJ software were utilised mainly to measure the parameters listed above for this study. At the final, a statistical analysis was done on the measured parameters to determine the outcomes.

The tabular column above (Table1), shows the selected values of descriptive analysis (mean and standard deviation) of all 40 VA (right and left), on observation towards the length and diameter of artery on each of its 3 parts. The mean length of right and left on each part was almost similar except for the mean length of H part (R- 38.937mm & L-40.237mm) and total length of V3 segment (R- 66.87mm & L-70.350mm). The standard deviation of total length of artery was 13.1552 on right and 8.9415 on left. The range of total length on right was 64mm and that of left was 37mm.

Table 1: Represents morphometric measurements (length and diameter)-descriptive analysis in 40 VA.

Descriptive analysis
		Mean(mm)	N	Std. Deviation
Pair 1	LVR	23.720000	20	4.9809743
Pair 1	LVL	23.450	20	4.7570
Pair 2	LHR	38.937	19	6.7035
Pair 2	LHL	40.237	19	7.0816
Pair 3	LPR	6.400	20	1.8750
Pair 3	LPL	6.725	20	1.7953
Pair 4	LTR	66.810	20	13.1552
Pair 4	LTL	70.350	20	8.9415
Pair 5	DVR	3.550000	20	1.1614419
Pair 5	DVL	3.547500	20	.9721754
Pair 6	DHR	3.6305	19	1.40876
Pair 6	DHL	3.695	19	1.4077
Pair 7	DER	3.415789	19	1.2566548
Pair 7	DEL	3.458	19	1.3664
Pair 8	DAR	3.6980	20	1.28796
Pair 8	DAL	3.5645	20	1.12524

The mean diameters of the VA on right and left sides for each part were similar except for a slight change in average diameter on VA (i.e.3.6980mm on right and 3.5645mm on left). The range of average diameter of VA was 5.7mm on right and 4.95mm on left. The total length and average diameter of VA was compared using paired t test and they were correlated using Pearson’s correlation test, in order to check the simultaneous relationship between the two parameters. When compared between total length of right (LTR) with average diameter of right (DAR)- It was found that the p value was 0.991 and it was not statistically significant (>0.05) and the null hypothesis is accepted. The Pearson’s r value was very weakly positive (+0.003). (Graph1). This correlation results that, when LTR increases then DAR increases but their relationship is not very strong. When compared between total length of left (LTL) with average diameter of left (DAL) - It was found that the p value was 0.511 that is >0.05, indicates that it statistically insignificant and the null hypothesis is accepted. The Pearson’s r value was very weakly positive i.e.,0.021 (Graph 2).

Lastly, the angle between the V and H part on both right and left sides of all cadvers were taken and the descriptive analysis was done (Table-2). The analysis showed that the mean angle on right side (AR) was greater 80.8° then that of left 78.5° with their standard deviation 24.45° on right and 22.43 on left.

Table 2: represents the descriptive analysis of AR and AL

Descriptive analysis
	Mean (degree)	N	SD
AR	80.8°	19	24.45
AL	78.5°	19	22.43

The AR and AL was compared using paired t test and the p value 0.345 (>0.05) was statistically insignificant. Angle on right (AR) and angle on left (AL) was also correlated using Pearson’s correlation test and the Pearson’s r value was 0.911 which indicates that the correlation level was very strongly positive. The p value in correlation was <0.001, this value represents that the correlation between AR and AL was significant (Graph 3).

This study also correlated the angle between the V and H part on right (AR) and left (AL) side with the difference in diameter of V and H part of VA on right (DDR) and left (DDL). The correlation between DDR and AR showed the Pearson’s r value 0.221 to be weakly positive. The p value was 0.364, which shows that the correlation is insignificant. Similarly, the correlation between DDL and AL was done and the Pearson’s r value was -0.320, which shows that the level of correlation was weakly negative. The p value of the same pair is 0.169, this shows that the correlation is insignificant.

A few studies were done previously on morphometry of suboccipital or atlantal segment of VA. Confining to the length of the atlantal part of VA, the studies were as follows. In one study done by S. Muralimohan et al–found the mean length of vertical segment of VA represented as Vv was 15.0 ± 1.53 mm, with a range of 12.6mm − 17.4 mm. While, the mean length of horizontal segment of VA represented as Vh was 35.6 ± 2.44mm with a range of 31.5 mm- 40 mm [14]. In a 20 specimens cadaveric study by Goel et al, found the mean length of the Vv Vh segment to be 15.7 mm and 35.7 mm [4].Lang J et al–measured the length of the Vv part (axoatlantal part) of VA to be 38.91 ± 5.53 mm (ranged from 29mm to 56mm) and the length of Vh / horizontal part of VA from its atlas entry (foramen transversarium) to its exit into dura mater was measured to be 44.3 ± 6.27mm (ranged from 27mm to 60mm)[12]. Our current study measured the length of 3 parts of VA. 1st (V) part- was the vertical length of VA between second cervical and first cervical transverse foramen. 2nd (H) part – was the horizontal length of VA from its C1 transverse foramen entrance till the dural entry point. 3rd (atlas posterior arch, corresponding to the foramen transversarium of C1) part –was the length of transverse process measured between superior and inferior margin of foramen transversarium of atlas. The mean length of V part on right side (LVR) was found to be 23.72mm (ranged from 17mm-32mm) and the mean length of V part on left side (LVL) was 23.45mm (ranged from 16mm-30.5mm). Similarly, the mean length of H part on right side (LHR) was found to be 38.937mm (ranged from 26mm- 50.5mm) and the mean length of H part on left side (LHL) was 40.237mm (ranged from 27mm-55mm). The mean length of 3rd part (posterior arch / transverse process of C1) on right side (LPR) was 6.400mm (ranged from 4mm- 11.5mm) and the mean length of 3rd part on left side (LPL) was 6.725mm (ranged from 4mm-11mm). The total length (LTR and LTL) of VA on both right and left sides was also noted by adding 3 parts together and it was found to be 66.810mm (range 24mm-88mm) on right and 70.350mm (range 51.5mm-88.5mm) on left. It can be noted that the length of left sided VA was more than that of right. The value of V part and H part found in this study fall in between the values found in other studies. These values of current study shows that the mean length of each part was separately measured for right and left sides unlike the other cited studies. The right- left values for each part of VA was also compared and the p value represented that all comparisons between them were insignificant. The morphometric measurement of length of each part helps the surgeons to get an approximate total length value prior to the surgeries.

Few studies that measured the diameter of V3 / atlantal segment of VA. A retrospective study using MDCT cerebral angiography scans of 120 patients was done by Binit Sureka et al. This study measured the diameter of VA and it was found that the largest diameter of VA measured (3.5 ± 0.8mm) was at level C7 vertebrae on the right and on left side, the largest diameter measured was (3.7 ± 0.4mm) at fifth cervical vertebrae level. The diameter of the VA was statistically significant between males and females and it was noted that the diameter was more in females than males[17]. Khanfour AA et al did the anatomical measurements in relation to VA portions from first to second cervical vertebrae of right and left side. The diameter of C1-C2 segment of VA on right side was measured to be 3.4 ± .42mm (ranged from2.11mm- 4.6mm). On left side, the mean diameter was 3.3 ± 0.26mm (ranged from 2.3mm- 4.6mm). At C1 level, the mean diameter of extradural segment of VA was 4.9 mm and 4.5 mm on the right and left side[11]. Another author Duan et al. found the diameter of a part of VA which passes through foramen magnum to be 2.41 mm on the right side and 2.88 mm on the left side[7]. An study done by Abd El Gawad Fal et found mean diameter between C4 and C5 pedicles - the second segment of VA to be higher on left side (3.67 ± 1.07 mm) than compared to that of right side (3.36 ± 0.93 mm) and the difference in the mean diameter of the VA between both right and left sides was found to be statistical significant p value p = 0.038 [1].The results from S. Muralimohan et al mentioned that the mean diameter of vertical (Vv) segment was 4.8mm [14]. An study on intracranial part of VA by Patel Z et al showed the mean external diameter was 3.72mm and 3.79 mm on left and right side [16] .Nourbakhsh Aet al measured at the midline of C2, the average diameter of the VA was 4.66 ± 0.51 mm on the right and on left side was 5.2 ± 0.49 mm (P = 0.002) [15]. While our study uniquely measured the diameter in 3 different regions of atlantal (V3) part of VA. The diameter was measured both on right and left sides, in the following 3 regions -at the mid-length of vertical (V) part (DVR-right and DVL- left), mid-length of horizontal (H) part (DHR and DHL) and at dural entry / V3 exit (E) part (DER and DEL).The mean diameter of DVR was 3.550 ± 1.161mm and DVL was 3.547 ± 0.972mm, DHR was 3.630 ± 1.408mm and DHL was 3.695 ± 1.407mm, DER was 3.415 ± 1.256mm and DEL was 3.458 ± 1.366mm. Finally, an average diameter of all these 3 parts was calculated both on right and left sides – DAR was 3.698 ± 1.287mm and DAL was 3.564 ± 1.125mm. All the mean diameter values ranged between 4.95mm-5.7mm and the maximum diameter among all is 6.0mm. These right and left pairs of diameters measured was compared using paired t-test and it was seen statistically insignificant with the p value > 0.05. In addition to these measurements, a correlation between total length and average diameter of both sides was taken (Graph 1 and 2) and this study resulted that the correlation was statistically insignificant and the Pearson’s r value was very weakly positive. The correlation manifests that as the length of the aimed part of the VA increases, the diameter also increases slightly. These mean values of diameter measured and the correlation test done will assist the surgeons to acquire better approach during skull base surgeries.

Previously, a morphometric cadaveric study was conducted by Patel Z et al in the intracranial part of VA using 10 formalin fixed brain specimens. This study was to determine the correlation / dependency between the external diameter differences in the left and right VA with the angle formed between them, for which a Pearson correlation was conducted. Here the LVA and RVA represented the intracranial part of VA at the level of inferior margin of pons, where the VA of both sides joins to form the basilar artery. The external diameter of LVA ranged from 2.82mm − 4, while that on right ranged from 2.41mm-4. The difference between the LVA and RVA external diameters was taken and it ranged from 0.39mm- 4.44mm. It was found that, 60% had larger external diameter on the right VA and 40% of them had larger external diameter on the left VA. The angle between the left and right VA ranged from 51° degrees to 91° degrees. After the Pearson correlation test was performed, it resulted that the correlation was statistically significant between the differences in the right and left VA’s external diameter and the angle found between them. The Pearson’s r value was − 0.6560 for n = 10 and the p value 0.0394 (p < 0.05) showed significant correlation. This study mentions that the large sample size was necessary to understand the correlation between the right and left VAs and their angulation [16]. Another study was conducted both in 7 (14 sides) cadavers and 24 (48 sides) CT images focusing only to the horizontal part of VA (V3h). 2 lengths (A and B) were measured in the V3h part of VA. Length A was the distance from the medial end of V3h part to the midpoint of atlas, posterior tuberculum. The length B was the distance from the medial tip to the Dural entrance point. The angle formed between these 2 lengths (A and B) was considered as alpha. The alpha mean angle in cadaver was 82.42 ± 10.34º and 83.21 ± 10.81º on the right- left side and in CT scan was 81.6 ± 10.15 º on the right and 83.77 ± 10.65º on the left side [5]. Our present study stands distinctive, by measuring the angulation between vertical (V) part and horizontal (H) part of V3 (atlantal) segment of VA. An imageJ software was used to measure the angle unlike other studies where protractor (25) was used. This software was used to maintain high accuracy of the angle measured. It was found that the angle on right side (AR) ranged from 34.644° to 129.634° and on the left side (AL) ranged from 30.103° to 117.241°. The mean and standard deviation of angle between 2 parts of VA on right side was 80.8 ± 24.45° while that on left side was 24.45 ± 22.43°. The AR and AL was compared using paired t test and the p value 0.345 (> 0.05) was statistically insignificant. The angles measured, AR and AL were correlated using Pearson correlation test. The Pearson’s r value was 0.911 and the p value in correlation was < 0.001, this value represents that the correlation between AR and AL was significant (Graph3). This can be interpreted as to maintain the equivalent blood supply to brain from both sides, the angulation on right and left are dependent (i.e. when one side angulation increases the other side also increases and vice versa). Along with this, correlation between the difference in diameter of V and H part of VA (DDVR, DDVL, DDHR and DDHL) with the angle (AR and AL) between these 2 parts was made. The correlation between all had Pearson’s r value weakly positive with the correlation p value being insignificant. Thus, this correlation clearly shows that the 2 variables are not depend on each other like that of intracranial part of VA, as mentioned in [16]. One of the limitations of the current study is it is done on cadavers and there might be slight change in morphometric values while compared to living individual.

In contrast to earlier studies elaborated, the current morphometric investigation precisely evaluated the length, diameter, and angle pertaining to each of the 3 parts separetly of the atlantal/ V3 segment of VA. This will also be of a great importance to neurosurgeons who intend to operate a limited part (any of the 3 parts) of V3 segment of VA. The mean values of parameters resulted in this study gives an average measurements or safe limits to the surgeons for the safe surgical procedures like occipital condyle screw technique, C1 laminectomy etc.

Author Contributions:

RP and AK conceived and designed the study, conducted research, provided research materials, collected and organized data, wrote the initial draft of article. MH and GM were involved in revising it critically for important intellectual content and the final approval of the version. All authors have critically reviewed and approved the final draft and are responsible for the content and similarity index of the manuscript

Funding: None

Data Availability: RP and MH have full access to all of the data used in this study and take responsibility for the integrity and accuracy of the data analysis. Data are available upon request to the corresponding author.

Code Availability: None

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Graphs 1 to 3 are available in the Supplementary Files section.

No competing interests reported.

G1.png
Graph 1- correlation between total length of right (LTR) with average diameter of right (DAR)
G2.png
Graph 2- correlation between total length of left (LTL) with average diameter of left (DAL)
G3.png
Graph 3- represents the correlation between AR and AL

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An Exploratory Morphometric Study of the Atlantal Part of Vertebral Artery

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