
Morphological and Morphometric Variations in Foramen Transversarium: A Cross-sectional Study in Dried Cervical Vertebrae of Western Odisha Origin
Correspondence Address :
Dr. Sarita Behera,
Assistant Professor, Department of Anatomy, Veer Surendra Sai Institute of Medical Sciences and Research, Burla, Sambalpur-768017, Odisha, India.
E-mail: drsaritabehera81@gmail.com
Introduction: Foramen transversarium refers to bilateral foramina found lateral to the vertebral body in the transverse process of the cervical vertebrae. Many variations are observed in these foramina which may lead to vertebrobasilar insufficiency, labyrinthine or hearing disturbances along with neurological symptoms due to compression or tortuosity of vertebral artery as it passes through the foramen.
Aim: To study the morphological and morphometric variations of the foramen transversarium in cervical vertebrae.
Materials and Methods: This cross-sectional study was conducted in Department of Anatomy, Veer Surendra Sai Institute of Medical Sciences and Research, Burla, Odisha, India, from June 2022 to August 2022. A total of 367 human cervical vertebrae were procured from the anthropology section of Department of Anatomy. Vertebrae with any damage to foramen transversarium were discarded. Each vertebra was observed for shape, size, symmetry, number of foramen transversarium and osteophytic encroachment. Distance of foramen transversarium from the medial margin of uncinate process was measured bilaterally in C3 to C7 vertebrae. Data collected was tabulated and analysed by Microsoft Excel software 2019.
Results: Mean anteroposterior diameter and transverse diameter in left-side were 5.45 mm and 5.42 mm, respectively and in right-side the measurements were 5.29 mm and 5.23 mm, respectively. Double foramen transversarium was observed in 40 (10.9%) vertebrae. Among them 18 (4.9%) were bilateral and 22 (6.0%) were unilateral. In 2 (0.54%) vertebrae there was triplication of foramen transversarium. In 34 vertebrae (9.26%) there was incomplete duplication of which 9 (2.45%) were bilateral and 25 (6.81%) were unilateral. Six different shapes of foramen transversarium were observed out of which round shape (62.1%) was the most common finding. In 261 (71.1%) of vertebrae the main foramen transversarium was symmetrical in both sides but in 106 (28.9%) it was asymmetrical. Osteophytic encroachment was found in 14 (3.81%) vertebrae. The mean distance of the foramen from medial margin of uncinate process was 5.32 mm on the left and 5.42 mm on the right-side.
Conclusion: The morphological data like very narrow foramina and such a high number of accessory foramina produced through the present study definitely points towards the variations of vertebral vessels.
Foramina, Morphometry, Osteophyte, Spine, Vertebrobasilar
Foramen transversarium refers to bilateral foramina found lateral to the vertebral body in the transverse process of the cervical vertebrae. It is ventrally by ventral bar and dorsally by dorsal bar. Each of the bars end in a tubercle laterally which are connected by intertubercular or costal lamella that forms the lateral boundary of the foramen. Developmentally, it is formed between vestigeal costal element anteriorly and true transverse process posteriorly (1).
These foramina are found only in cervical vertebrae and serve as a good way to identify them. Vertebral artery, vertebral vein and sympathetic plexus arising from inferior cervical ganglion pass through these foramina. Vertebral vein passes through all the seven foramina transversaria whereas the vertebral artery does not pass through the foramen transversarium of the seventh cervical vertebra as it mostly enters at the 6th cervical vertebra level for its vertebral course. Ideally, each cervical vertebra should have two foramen transversaria. But many variations are observed in these foramina. Congenital absence of the transverse foramen and osteophyte formation are reported to be one of the causative factors for vertebrobasilar insufficiency caused by rotation of the head. Vertebrobasilar insufficiency is characterised by headache, migraine and fainting attack. Also, inner labyrinthine or hearing disturbances along with neurological symptoms (2),(3).
It has been reported that vertebral vessels are responsible for formation of foramen transversarium. So variations in the course of the vertebral vessels may be one of the causative factors for variations in foramen transversarium. It is also noted that tortousity of vertebral artery may cause bone erosion or obstruct the complete formation of the foramen transversarium (4). Now-a-days transpedicular screw fixation of cervical spine is preferred surgery for instability due to trauma, tuberculosis, neoplasia or degenerative conditions and screw is placed just medial to foramen transversarium, so the vertebral artery is at risk of injury (5).
As per literature, most of the earlier studies have focused either on morphology or morphometry of foramen transversarium in different populations (6),(7),(8),(9),(10). Study by Nayak G et al., which included the bones of eastern part of Odisha also describes only about the incidence of accessory foramen transversarium (11), they have not studied the morphometric details. Hence, the present study was undertaken to study both the morphological and morphometric variations of foramen transversarium in dry bones of western Odisha population in a comprehensive way, which will definitely be helpful for the neuro and orthopaedic surgeons and the radiologists of this part of India to increase the effectiveness of the surgical and diagnostic procedures and decrease the complications related to injury of vertebral artery.
This cross-sectional study was conducted from June 2022 to August 2022 in Department of Anatomy, Veer Surendra Sai Institute of Medical Sciences and Research, Burla, Odisha, India. Study was commenced after obtaining approval from the Institutional Ethics Committee (IEC) (IEC no 009-2022/I-F-O/43/Dt.17-05-2022).
Inclusion criteria: Both typical and atypical cervical vertebrae were included in the study.
Exclusion criteria: Vertebrae with damaged foramen transversarium were excluded from the study.
Data collection: A total of 367 human cervical vertebrae of unknown age and sex, were procured from the anthropology section of Department of Anatomy, VIMSAR, Burla. Each vertebra was observed for shape, size, symmetry, osteophytic encroachment and number of foramen transversarium. In vertebrae having accessory foramen transversarium the larger foramen was taken as the main foramen and smaller one as accessory foramen.
The shapes of the foramina were classified into six categories using the criteria by Ambali MP and Jadhav SD with little modifications (12).
• Type-1 round,
• Type-2 elliptical with main diameter (length) anteroposterior,
• Type-3 elliptical with main diameter transverse (breadth),
• Type-4 elliptical with main diameter oblique, from right to left,
• Type-5 elliptical with main diameter oblique from left to right,
• Type-6 as irregular.
The widest anteroposterior and transverse diameters of main transverse foramina taken on the inner side were measured bilaterally using digital Vernier caliper (Table/Fig 1). In C3-C7 vertebrae distance of medial margin of foramen transversarium from the medial margin of uncinate process was measured.
Statistical Analysis
Data collected was tabulated and analysed by Microsoft Excel software 2019. The range, mean and standard deviation of all the measurements like anteroposterior diameter, transverse diameter, mean diameter and distance of medial margin of the foramen transversarium from the uncinate process were calculated. The scatter chart for the mean diameters of foramen transversarium of the right and left-side was plotted.
Mean anteroposterior diameter and transverse diameter in left-side were 5.45±0.81 mm and 5.42±0.79 mm, respectively and in right-side the measurements were 5.29±0.81 mm and 5.23±0.75 mm, respectively. The mean distance of the medial margin of the foramen from the uncinate process was 5.32±1.18 mm on the left and 5.42±1.33 mm on the right-side (Table/Fig 2). Mean diameter of transverse foramen of individual vertebra showed wide range of variation ranging from 1.17-6.95 mm in the right-side and 1.05-6.95 mm in left-side (Table/Fig 3),(Table/Fig 4).
Double foramen transversarium was observed in 40 (10.9%) vertebrae. Among these 18 (4.9%) was bilateral and 22 (6.0%) was unilateral. In 2 (0.54%) vertebrae there was triplication of foramen transversarium. In 261 (71.1%) of vertebrae the foramen transversarium was symmetrical in both sides but in 106 (28.9%) it was asymmetrical. In 34 vertebrae (9.26%) there was incomplete duplication out of which 9 (2.45%) was bilateral and 25 (6.81%) was unilateral. Osteophytic encroachment was found in 14 (3.81%) vertebrae (Table/Fig 5),(Table/Fig 6),(Table/Fig 7). Six different shapes of foramen transversarium were observed. Type-1 or round shape was the most common finding bilaterally (Table/Fig 8),(Table/Fig 9).
Anatomically foramen transversarium has been described to be divided by fibrous or bony ridge, separating artery and vein, the smaller posterior part that encloses a branch of vertebral nerve and vein is called accessory foramen transversarium. Separate area in the form of complete accessory foramen transversarium for vertebral vein and nerve offers limited space. Any irritation or inflammation of nerve causes pressure effect on nerve and vein as well. Such duplication of foramen transversarium or accessory foramen transversarium may be suggestive of duplication of vertebral artery or separate area for vertebral vein and nerve. Awareness of such variation and its incidence is clinically important for spine surgeons to prevent intraoperative complications by damaging vertebral artery and vein (4).
Duplication of foramen transversarium may be associated with developmental anomalies of vertebral artery, such as duplication and fenestration or due to abnormality during formation of vertebra itself. Vertebral arteries are formed by fusion of the longitudinal anastomosis, connecting the cervical intersegmental arteries. The intersegmental arteries regress during the embryonal development except the 7th intersegmental artery, which forms the proximal portion of the subclavian artery and initial part of the vertebral artery. Persistence of a portion of primitive dorsal aorta with two intersegmental arteries results in duplication of vertebral artery. This may lead to accessory foramen transversarium (2).
Accessory vertebral arteries if present may potentially be protective against ischaemic attacks to the brain by providing collateral blood flow to the basilar artery. However, fenestrated vertebral arteries have been demonstrated histologically to be weak with irregular elastic fibres in the vessel wall. There may be a higher risk of thrombus development and embolisation leading to a severe transient ischaemic attack in people with fenestrated or duplicated vertebral arteries (13).
During development of vertebra, double rib bone element may fuse to the original transverse process resulting in unusual number of foramen transversarium (12). Study by Gupta M and Agarwal S on 319 foramen transversarium of 161 cervical vertebrae at Lady Hardinge Medical College, Delhi in 2019 found accessory foramen transversarium in 26.09% where majority were at C6 level and nil at C1 and C2 level (14). Similar report was made by Patil NP et al., in a study on 175 cervical vertebrae at Ambjogai, Maharashtra in 2014 that the accessory foramen transversarium was more common in lower cervical vertebrae (15). Present study found it to be 54.7% in C6 and nil in C1 and C2.
Vasuki AKM et al., in their study on 300 cervical vertebrae at Coimbatore in 2018 found triple foramen in right-side in one (0.003%) vertebra (4). In the present study, in two (0.54%) vertebrae there was triplication of foramen transversarium.
Anatomical variations in the vertebral artery, embryological factors and functional conditions may play an important role in the formation of incomplete transverse foramen. It was noted that the tortousity of vertebral artery may cause bony erosion or obstruct the complete formation of foramen transversarium (4),(16). Vasuki AKM et al., found unilateral incomplete duplication in 3% and bilateral incomplete duplication in 2% out of 125 vertebrae showing variation (4). Shah ST et al., in their study on 210 vertebrae at Gujarat in 2014 found unilateral incomplete duplication in 3.8% (6). In the present study, in 34 vertebrae (9.26%) there was incomplete duplication out of which 9 (2.45%) was bilateral and 25 (6.81%) was unilateral.
Size of transverse foramen is directly proportional to the calibre of vertebral artery. Size of transverse foramen carries clinical significance as vertebrobasilar insufficiency may be seen in case of narrowing of foramen transversarium. During the development of bone, new layers are added to the pre-existing surfaces. Reduced foramen area of some cervical vertebrae may be attributed to periosteal growth at foramen margins to fit around their neurovascular and other contents (4).
Bow hunter’s stroke is a symptomatic vertebrobasilar insufficiency caused by stenosis or occlusion of the vertebral artery with head rotation (7). Ambali MP and Jadhav SD in their study on 163 cervical vertebrae at Maharashtra in 2016 observed the average diameter of the foramen transversarium on the right-side to be 5.46 mm and on the left to be 5.80 mm (12). In present study, the largest diameter was 7.30 mm and smallest was 1 mm. Previous studies had shown that the two vertebral arteries are not equal in size in 75% of people and of these,10% have quite narrow vertebral arteries in right-side (7). Agrawal D et al., conducted a study on 160 cervical vertebrae of eastern Odisha in 2012 and reported asymmetrical foramen transversarium only in one specimen in typical vertebrae (17). Ambali MP and Jadhav SD, observed symmetrical foramen transversarium in 91 (55.82%) out of 163 vertebrae (12). In the present study asymmetrical foramen transversarium were found in 106 out of 367 vertebrae (28.9%).
As per literature, osteophytes are more common along the medial or lateral margins of the foramen transversarium reducing the transverse diameter, type 2 where the main diameter is along the anteroposterior direction is most likely to be involved in compression of the vertebral artery whereas type 3 where main diameter is along the transverse axis is at minimal risk [18,19]. Ambali MP and Jadhav SD, found seven different shapes of foramen transversarium. Out of them oval and tilted to right was the most common shape (44.78%) (12). Vasuki AKM et al., found five different shapes out of which Type-1 or round shape was the most frequent (43.6%) (4). Patra A et al., in their study on 200 cervical vertebrae of south central Asian cadavers in 2022 observed type 1 or round shape (27.13%) to be the most common in right-side and type-4 or elliptical with main diameter from right to left (27.63) in left-side (18). In present study, six different shapes were observed and round shape was the most common (62.1%) in both sides. Most of the studies describe unilateral accessory foramen to be more common than bilateral which was consistent with present study (Table/Fig 10) (2),(4),(6),(7),(8),(9),(10),(11),(12),(20),(21),(22),(23),(24),(25),(26).
Ambali MP and Jadhav SD, found bony spicules in 12 (7.36%) out of 163 vertebrae (12). Sangari SK et al., observed osteophytic encroachment in 21.3% of vertebrae studied (7). Patra A et al., observed osteophytes in 21.3% (18). In present study, authors observed osteophytic encroachment in 14 (3.81%) out of 367 vertebrae. The osteophytes encroaching the transverse foramina are potential sites of trauma to the vertebral artery which may also compress it resulting in its narrowing leading to vertebrobasilar insufficiency.
To avoid vertebral artery injury during anterior cervical disc surgery, the medial margin of the uncovertebral joint may be the safe landmark. The distance of foramen transversarium from uncinate process found in the present study which was consistent with findings of previous studies (Table/Fig 11) (7),(14),(16),(18),(23). The risk of vertebral artery laceration may be increased, especially when osteophytes are removed from uncinate process by lateral decompression. So, it is better to perform this procedure under direct visualisation with opening of the anterior walls of the transverse foramen and retracting the vertebral artery laterally (7).
Limitation(s)
As the study was done in dried vertebrae collected from the anthropology section, age and sex correlation could not be done.
Finding of extremely narrow foramen transversarium as small as 1 mm in diameter and accessory foramina in such a good number of vertebrae in the present study raises questions about the integrity of the contained structures. This factor leading to vertebral artery compression should not be ignored while searching for the differential diagnosis of complaints like headache, migraine and fainting attacks. So, the results generated through this osteological study should be correlated by undertaking radiological studies to confirm the variations of the vertebral vessels. Further, though the other morphometric details of foramen transversarium have been studied in different populations of India, the distance of uncinate process from its medial margin generated through this study will be first of its kind.
DOI: 10.7860/JCDR/2023/63927.18035
Date of Submission: Mar 09, 2023
Date of Peer Review: Apr 04, 2023
Date of Acceptance: May 23, 2023
Date of Publishing: Jun 01, 2023
AUTHOR DECLARATION:
• Financial or Other Competing Interests: None
• Was Ethics Committee Approval obtained for this study? Yes
• Was informed consent obtained from the subjects involved in the study? No
• For any images presented appropriate consent has been obtained from the subjects. No
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