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Turkish Journal of Medical Sciences Turk J Med Sci(2013) 43: 711-717© TÜBİTAKdoi:10.3906/sag-1209-103

Variations of transverse foramens of cervical vertebrae: a 3-dimensionalmultidetector CT study

Bumin DEĞİRMENCİ*, Ömer YILMAZDepartment of Radiology, Faculty of Medicine, Süleyman Demirel University, Isparta, Turkey

* Correspondence: [email protected]

1. IntroductionThe vertebral artery, vein, and accompanying sympathetic plexuses pass through the transverse foramens (TFs) of cervical vertebrae. Vertebral arteries do not pass from the transvers foramina of the seventh cervical vertebra (C7). Vertebral arteries enter the TF at the C6 level (1). In previous studies, the size, number, and form variations of TFs were observed and morphometric measurements were done on dry cadaveric materials (2–6). In the previous studies, it was reported that multidetector computed tomography (MDCT) with 3-dimensional (3D) volume rendering (VR), multiplanar reconstruction (MPR), and maximum intensity projection (MIP) techniques has a very high sensitivity in evaluating anatomic (bony and vascular) variations and anatomic localization (7–21). To the best of our knowledge, this is the first study in the literature that evaluates the variations of TFs by MDCT. MDCT evaluation of TFs in patients with cervical trauma and cervical spine degenerative disease could be used as a guide for surgical interventions.

2. Materials and methodsIncluded in this study were 127 subjects comprising 63 women and 64 men (aged between 8 and 85 years; mean:

46.4 ± 16.5; female mean: 47.3 ± 15.6; male mean: 45.9 ± 17.4). Subjects’ data were collected from patients referred to the radiology department between November 2008 and June 2010 for the evaluation of cervical trauma and other cervical pathologies through CT examinations. No additional CT procedure was needed for this study beyond the routine referral examination. This study conformed to the Helsinki Declaration. A 6-slice multidetector CT scanner (Philips Brilliance 6, Philips Medical Systems, Amsterdam, the Netherlands) was used, and images were transferred to a workstation that had direct connection with the CT console. CT examinations of all chosen subjects had been performed with high-resolution parameters (6 × 1.5 mm detector collimation, 2-mm slice section thickness, 120 kV); therefore, they were suitable for excellent VR and MPR processes. Measurements were done on VR images and checked with MPR and curved planar reformatted (CPR) (Figure 1) images synchronously. The entire study was performed by review of CT data at the computer workstation.

Each cervical vertebra was extracted separately by a cut on the appropriate horizontal planes in the VR images. If the acquired images were not suitable for the evaluation

Aim: The objective of this study was to display the transverse foramens (TFs) of cervical vertebrae with multidetector computed tomography (MDCT) and to identify their variations.

Materials and methods: This study included 127 (63 women and 64 men) patients. The mean age was 46.4 years. MDCT images of cervical vertebrae were formed with volume rendering (VR) and multiplanar reconstruction. VR images were formed for each cervical vertebra between C1 and C7 and they were examined for the shape, diameter, and congenital variations of TFs. The TF diameters of each cervical vertebra were measured from MDCT images.

Results: The widest TF diameters were measured at the C1 level and the narrowest at the C7 level. TF diameters were wider on the left side. The most frequent variation was the duplication of TF, which was noted in 117 (13.1%) cervical vertebrae in total. Hypoplasia of TF was seen in 93 (10.4%) cervical vertebrae. Diameter asymmetry of right and left TFs were other frequent variations.

Conclusion: TF variations can be easily assessed in cervical MDCT examinations. Determination of foraminal variations before surgical interventions on cervical vertebrae could be an important guide for surgeons.

Key words: Cervical vertebra, transverse foramen, multidetector CT, variation

Received: 30.09.2012 Accepted: 06.11.2012 Published Online: 26.08.2013 Printed: 20.09.2013

Research Article

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DEĞİRMENCİ and YILMAZ / Turk J Med Sci

of TFs, the process was repeated with different plane cuts. MPR and CPR images of cervical vertebrae were acquired by using slabs having thicknesses of 1–3.5 mm. Diameters of the TFs were measured on VR, MPR, and CPR images. VR images were used for the assessment of shape, number, and agenesis. To examine the existence of bony lamella on TFs, the MPRs acquired by the thinnest slabs were evaluated using different windowing levels. Anterior-posterior (A-P) and transverse diameters of TFs were measured bilaterally (Figure 1). In levels with double TFs, the bigger one was measured. Any marked diameter difference of right-left TFs (bigger-smaller) was assumed as asymmetry (Figure 2). When no TF was seen uni- or bilaterally, this was assumed as agenesis (Figure 3). If the TF was smaller than 2 mm in diameter, it was assumed to be a case of hypoplasia (rudimentary) (Figure 3). In some cases, smooth indentations that had

separate contours and no bony septa from the main TF, especially in the posterior aspects of TFs, were seen. This appearance was taken as a “sulcus” formation (Figure 4). A double-TF appearance with bony lamella was assumed as duplication (Figure 5). Partial absence of bone structure forming a TF was accepted as “incomplete TF” (Figure 6). If the TF appearances were not suitable for measurement on standard VR images, images were formed again using different angles. Diameter differences of right-left TFs were evaluated for each cervical vertebra. Diameter differences of TFs were observed between the sexes. The patients were divided into 3 age groups (group 1: 8–39 years, group 2: 40–59 years, group 3: 60–85 years). Diameter differences of TFs were observed between groups.

Patients with complete TF fracture or advanced bony degeneration at cervical level were excluded.

Figure 1. A-P and transverse diameter measurements (calibers) of TF in 3D VR (A) and axial MPR (B) images.

Figure 2. Various levels of cervical vertebrae (A: C4, B: C5, C: C6, and D: C3 level) with 3D VR images showing TF asymmetry.

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Statistical analysis was done using SPSS 10.0. Data were analyzed statistically by one-way ANOVA and t-tests. All parametric results were expressed as mean ± standard deviation (SD) for each group. Local statistical significance was assumed as P < 0.05 for all parameters.

3. ResultsIn total 127 cervical spines, comprising 889 vertebrae and 1778 transverse processes from C1 to C7, were evaluated. The means and SDs of the diameters of the TFs were calculated at each level for all subjects (Table 1). The

Figure 3. The 3D VR images show bilateral TF hypoplasia bilateral (A) and right TF (B) of C7 vertebra, and agenesis left TF of C7 vertebra (C) (arrows).

Figure 4. The 3D VR images show unilateral (A and B) and bilateral (C) sulcus formation in TFs (arrows).

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widest TF diameters (right-left) were measured at the C1 level (A-P, 6.57 ± 0.89 mm, transverse, 6.16 ± 0.96 mm; left A-P, 6.65 ± 0.96 mm, left transverse, 6.28 ± 1.08 mm) and the narrowest was at the C7 level (right A-P, 3.97 ± 1.15 mm, transverse, 4.18 ± 1.05 mm; left A-P, 3.99 ± 1.00 mm, left transverse, 4.39 ± 1.15 mm). Although it was

not statistically significant at all levels, TF diameters were wider on the left side than the right side (Table 2). The transverse diameters at all levels excluding C1 were slightly wider than the A-P diameters, although the difference was statistically insignificant (Table 1). The most frequent asymmetrically wide foramen was observed in 15 cases at

Table 1. Minimal and maximal diameters of the transverse foramina in both sides of the C1–C7 levels of cervical vertebrae.

Diameters (mm)Right Left

N Mean ± SD Range N Mean ± SD Range

C1A-P

1276.5 ± 0.89 4.8–8.9

1276.6 ± 0.96 4.1–8.7

Transverse 6.1 ± 0.96 3.9–8.7 6.2 ± 1.05 3.9–9.1

C2A-P

1275.8 ± 0.86 3.6–8.1

1275.9 ± 0.81 3.3–8.3

Transverse 6.1 ± 0.94 3.9–8.7 6.1 ± 0.98 3.8–8.5

C3A-P

1274.9 ± 0.55 3.5–6.2

1275.1 ± 0.65 3.7–7.2

Transverse 5.9 ± 0.76 3.8–8.1 6.0 ± 0.87 3.7–8.4

C4A-P

1275.1 ± 0.79 3.5–7.5

1275.1 ± 0.70 3.8–8.5

Transverse 5.8 ± 0.76 3.8–8.5 6.0 ± 0.87 4.0–8.0

C5A-P

1275.1 ± 0.86 2.7–7.4

1275.4 ± 0.88 3.1–7.9

Transverse 5.6 ± 0.77 2.0–0.7 5.9 ± 0.83 3.7–8.0

C6A-P

1275.6 ± 1.2 1.9–9.1

1275.7 ± 1.0 2.6–8.5

Transverse 5.9 ± 1.0 2.0–8.0 6.1 ± 1.0 2.7–8.6

C7A-P

1273.9 ± 1.1 2.0–6.8

1273.9 ± 1.0 2.2–5.6

Transverse 4.1 ± 1.0 2-5–7.0 4.3 ± 1.1 2.3–7.1

Figure 5. Various levels of cervical vertebrae (A: C6, B: C5, C: C6, and D: C4 level) with 3D VR images showing unilateral (A) and bilateral (B, C, and D) TF duplication.

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the C6 level. The most frequent TF agenesis was observed at the C7 level; in 2 cases it was on the right, in 1 case it was on the left, and it was bilateral in 2 cases. The most common TF hypoplasia was seen at the C7 level in 93 cases (bilaterally in 81 cases). The most common TF duplication was seen at the C6 level, bilaterally in 34 and unilaterally in 13 cases. Sulcus formation in TFs was at the C5 level mostly (n = 31). In 1 case, incomplete TF was observed at the C7 vertebra. The observed TF variations and their cervical levels are presented in Table 2.

There was no significant difference of TF diameters between age groups.

4. Discussion The most frequent cervical vertebral abnormalities are fusion or arch defect of the second or third vertebra (2,17). In the literature, TF variations were studied in dry materials in several previous studies (2,3,5). Erbil et al. (2) and Taitz et al. (3) evaluated variations of the cervical vertebral TF. Variations of TFs were studied by MDCT in only one study in the literature. In that study, Evangelopoulos et al. (4) evaluated the variations in diameter and in shape, but congenital variations (agenesis, duplication, hypoplasia, or occurrence of sulcus) were not evaluated. In another

MDCT study, Duan et al. (6) studied the variations of bone and vertebral artery at the craniocervical junction. Our study seems to be the first study in the literature evaluating the TFs of C1–C7 with MDCT. In agreement with other studies (3,4), the largest A-P and transverse diameters were measured at the C1 level. On the other hand, the smallest diameters of foramens were measured at the C7 level. An answer to the question of why the narrowest diameter was measured at the level of C7 in our study and in previous studies (3–5) could be the fact that no VA is passing through at this level. In the normal population, the left TF is generally larger than the right TF (left dominancy). Taitz et al. (3) found that in most of the cases, the diameters of the left TF were larger than those of the right foramens, and they explained their findings by the fact that the left VA is larger than the right VA. Evangelopoulos et al. (4) have shown that diameters of the left TFs were statistically larger than those of right foramens in A-P projections at the level of C3–C6 and in transverse projections at the level of C3–C4. In our study, diameters of the left TF in both A-P and transverse projections at the C1–C7 level were found to be minimally larger than those of the right side, with no statistical difference.

The fact that no difference in TF diameters was found among the different age groups (groups 1, 2, and 3) may be due to the full development of TFs in all the patients. No difference between sexes was detected in the present study, either.

Erbil et al. (2) found 4% asymmetric TFs in their study evaluating adult cervical vertebrae. On the other hand, Taitz et al. (3) did not evaluate variations; however, they divided TFs into groups according to their shape. In the present study, asymmetric appearance was detected in 29 cervical vertebrae (3.2%), which can be accepted as morphological variation. The most frequent morphological variations were found at the C6 level (n = 15). In 10 out of those 15 cases, the left TF was detected as very large. Erbil et al. (2) found double foramens in 5 cases (2%) in their study. On the other hand, Taitz et al. (3) reported double

Table 2. Variation types and their levels and numbers of transverse foramina. R; right, L; left, NA; not applicable.

Vertebrae

Variation types of transverse foramina

Agenesis Hypoplasia(rudimentary) Double foramen Asymmetry Sulcal type indentation

R L Bilaterally R L Bilaterally R L Bilaterally R L Bilaterally R L BilaterallyC3 - - - - - - - - - 2 1 NA - - -C4 - - - - - 5 1 1 2 3 NA - - -C5 1 - - 1 - - 11 13 16 2 2 NA 15 9 7C6 1 1 - 2 2 - 13 13 34 5 10 NA 8 6 6C7 2 1 2 2 5 81 - - - 1 1 NA - - -

Figure 6. C7 cervical vertebra’s 3D VR image shows bilaterally “incomplete” TF formation.

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foramens in 34 vertebrae (13.4%). The level at which the double foramens were detected was not mentioned in either of those studies (2,3). In our study, double foramen variations were found in 117 vertebrae (13.1%). Double foramen variations were most frequently detected at the level of C6 (n = 70; in 34 cases, they were bilateral). Taitz et al. (3) reported triple foramens in one vertebra at the level of C7. No triple foramens were seen in our study.

Taitz et al. (3) reported hypoplasia (rudimentary) of TFs in 8 cases (3.1%, 4 cases at C7 level, 3 cases at C6, and 1 case at C5 level). In our study, hypoplasia of TFs was found in 93 (10.4%) vertebrae (mostly at the C7 level; n = 88). In addition, bilateral TF hypoplasia was found in 81 cases at the C7 level. Taitz et al. (3) reported agenesis of TF in 4 cases (3 cases at the C4 level and 1 case at C6 level). On the other hand, Erbil et al. did not report any agenesis. In the present study, agenesis of TFs was found in 8 (0.9%) vertebrae (mostly at the C7 level; n = 5). In addition, bilateral TF agenesis was found in 2 cases at the C7 level. No VA passage at the C7 level may be the cause of agenesis or hypoplasia of foramens at this level.

We detected a dilation that looked like an indentation in the anterior or posterior portion of foramens in 31 cases at the C5 and in 20 cases at the C6 level (in total

51 cases, 5.7%). This finding has not been reported before in the literature and we termed this as “sulcus”. Vertebral vessels have been defined as a factor in the development and formation of TFs (3,22). Vertebral arterial pressure has also been reported as important in the formation of foramens and Kovacs et al. (23) reported that VA pressure causes bony excavation in the superior articular process. We speculated that the configurations and pressure changes of the vessels passing through the foramens may cause the appearance of a sulcus. Other speculations about the development of sulcus formation include that it may be incomplete duplication of a TF.

Partial absence of bony structure of the TF was termed as “incomplete TF”. This TF variation has not been reported in the literature. We detected an incomplete TF in one case in our study.

The present study appears to be the first study in the literature evaluating the variations of TFs with MDCT. Configurations, diameters, and variations of the foramens can be easily and effectively evaluated with 3D VR, MPR, and CPR images of MDCT. This evaluation may provide important information for spinal surgeons that may help in preoperative planning and may prevent VA trauma during tissue dissection and instrument application.

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