Journal of Morphological Sciences Original Article

J Morphol Sci J Morphol Sci 2021;38:70-74

Brazilian Society of Anatomy

Morphometric Analysis of The Accessory Transverse Foramen

in a Population in Northeastern Brazil
João Pedro Maia Medeiros,1 Jamil Dieb Santana,1 Fábio Antônio Serra de Lima Júnior,1 Jonathan Barros Cavalcante,1 Desiré
Dominique Diniz de Magalhães,1 André de Sá Braga Oliveira,1 Cecília de Lima Leite,2 Sandy Costa Gonçalves,2 Gilberto
Santos Cerqueir,2 Jalles Dantas de Lucena3
1
Federal University of Paraiba – UFPB. João Pessoa, PB, Brazil
2
Federal University of Ceara – UFC. Fortaleza, CE, Brazil
3
Faculty Santa Maria- FSM. Cajazeiras, PB, Brazil

Disclose and conflicts of interest: none to be declared by all authors

ABSTRACT
Introduction: vertebral arteries (VA) are the formation factors of the Transverse Foramens (TF) and the largerst anatomical
structures that occupy them. Variations in the presence, size and course of VAs affect the morphology of TFs considerably,
besides being the probable cause of formation of the accessory transverse foramen (ATF). Knowledge of the presence of the
ATF and its variations are important for a safe surgery.
Material and Methods: the present study has analyzed 165 cervical vertebrae. The ATF has been classified as unilateral or
bilateral, complete or incomplete and anterior, posterior or lateral regarding the transverse foramen of the respective cervical
vertebrae analyzed. Quantitative data was collected through a digital caliper.
Results: significant differences were found between relative amount of black pixels in the region of the branch (R) of the
mandibular canal (P < 0.05) and mean values of the groups, whereas no significant differences were found for the regions of
the mandibular canal near the mental foramen (MF) and angle region (A).
Conclusion: 36 (21.82%) of the vertebrae presented the ATF, with 25 (15.15%) of them carrying the ATF unilaterally, while the
remaining 11 (6.67%) had the foramen bilaterally. 28 (59.57%) ATF were classified as incomplete and 19 (40.43%) were classified
as complete. 44 (93.62%) were identified as posterior and 3 (6.38%) were anterior to the TF. Regarding the morphometric data,
there was no difference between the longitudinal measurement (LM) and transverse measurement (TM) on the right and left
sides of the vertebrae analyzed. Conclusion. It has been shown for the first time the prevalence of ATF in individuals in a
population of Northeastern Brazil. The morphological knowledge can be surgical and clinically important as it may suggest
alterations in the vertebral artery and in the venous plexuses that surround it in its vertebral segment of passage in the
transverse foramina.
Keywords: Anatomy; Clinical anatomy; Spine; Transverse foramen.

Introduction Thus, the anatomical relations described in this

The transverse foramen (TFs) are located bilaterally region explain why during prolonged head rotations,
in the transverse processes of the cervical vertebrae, such as when driving in reverse, there may be dizziness
which are the smallest among the mobile vertebrae. and other symptoms, since there is interference in
They are filled by the spiral path of the vertebral the blood supply of the brainstem that comes from
arteries (AVs).1 branches of the VA.
The vertebral artery, which comes up at the The vertebral arteries are the factors that form FTs,
initial portions of the subclavian arteries, medially and the largest anatomical structures that occupy
to the anterior scalene muscle, can be divided into them. In about 88% of cases, VA can enter the cervical
four segments: cervical, vertebral, suboccipital spine through the sixth vertebra, but occasionally
and intracranial. The vertebral portion starts with it can emerge in the fourth, fifth or seventh cervical
the penetration of the vessel in the TF of the sixth vertebra. 3 In the 7th cervical vertebra, the foramen is
cervical vertebra in an ascending path to the atlas (C1 smaller and give way to only small accessory vertebral
vertebrae). Next to the roots of the spinal nerves there veins, which are sometimes absent. Variations in
is the emergence of spinal branches of this artery, the presence, size and course of the VAs affect the
which go towards the spinal cord and contribute to its morphology of the TFs considerably, in addition to
irrigation. It is noteworthy that in this segment the VA being the probable cause of formation of the accessory
is surrounded by a venous plexus.2 transverse foramen (ATF).

DOI: 10.51929/jms.38.12.2021
70 Journal of Morphological Sciences Vol. 38/2021 ISSN 2177-0298
Morphometric Analysis of The Accessory Transverse Foramen in a Population in Northeastern Brazil Medeiros JPM et al.

The accessory transverse foramen (ATF) or double foramen, including the verifications of the longitudinal
transverse foramen, according to some publications, is measurement (LM) and transverse measurement (TM)
characterized by being a considerably smaller structure of the diameters of the ATF. For proper analysis of these
than the TF, and may be absent in most individuals. It is data, the Kolmogorov-Smirnov test was used to verify
also located in the transverse processes of the cervical its normal distribution and, immediately afterwards,
vertebrae and is defined by its spatial relationships parametric or non-parametric tests were applied to
with the TF of the respective vertebra. Unlike the TF, assess the difference between the right and left sides
it can appear due to changes in venous circulation of the analyzed morphometric parameters. The results
in the region. Knowledge of the presence of the ATF were considered significant when p≤0.05.
and its variations are important for a safe surgery.4,5
Changes in the embryological process of formation of Results
vertebral vessels are the most suggestive causes of the As shown by the analysis of the 165 vertebrae
formation of ATF. This relation is corroborated to the present in the study, we have identified the presence of
extent that, as reported in most of the literature on 44 (26.67%) atlas vertebrae, 58 (35.15%) axis vertebrae
the topic, the presence of ATF is more common in low and 63 (38.18%) typical cervical vertebrae (C3-C7).
cervical vertebrae (C5, C6, C7), especially at the exact Among them, two axis vertebrae were excluded from
C6 level where there is penetration of the VA in most
the study because they had damaged structures that
individuals.6
compromised the analysis.
Segmenting the analysis by vertebrae type, 4 (2.43%)
Material and Methods atlas vertebrae with the ATF were identified, while
The present study has analyzed 165 dry cervical 40 (24.24%) did not have this structure. Moreover,
vertebrae from a population of Northeastern Brazil, 8 (4.84%) axis vertebrae presented the ATF, while 48
with unknown ages and genders, belonging to the (29.09%) did not have it and 2 were damaged (1.21%).
morphology department, more specifically to the Finally, 24 (14.54%) of the typical cervical vertebrae
human anatomy laboratories at the Federal University were identified with this foramen, with the remaining
of Paraíba (UFPB). Vertebrae with important 39 (23.64%) were identified without this structure
degradation were excluded from the study, once they (Table 1).
made their specific analysis impossible. Regarding the presence of the accessory transverse
As qualitative parameters, the accessory transverse foramen, 36 (21.82%) of the vertebrae presented this
foramina have been classified as unilateral or bilateral, structure, with 25 (15.15%) of them having unilateral
complete or incomplete, and anterior, posterior or ATF, while the remaining 11 (6.67%) had the foramen
lateral, in relation to the transverse foramen of the bilaterally. Thus, a total number of 47 accessory
respective cervical vertebrae analyzed (Figure 1). transverse foramen was found in the vertebrae
A 150 mm capacity digital caliper (Eccofer®, João included in the study.
Pessoa, Paraíba, Brazil) was used to collect the Furthermore, according to the qualitative analysis
morphometric data of the accessory transverse

Figure 1. Qualitative analysis of the accessory transverse foramen: (A) ATF bilateral, incomplete and posterior, (B) ATF unilateral, complete and anterior.

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Medeiros JPM et al. Morphometric Analysis of The Accessory Transverse Foramen in a Population in Northeastern Brazil

of the 47 accessory accessory foramens identified, 28 of the ATF in dry cervical vertebrae in a population in
(59.57%) were classified as incomplete and 19 (40.43%) Northeastern Brazil.
as complete. According to the anatomical relationship The presence of the accessory transverse foramen
with the transverse foramen, 44 (93.62%) were was reported in 36 of the 165 vertebrae analyzed,
identified as posterior and 3 (6.38%) as anterior to this corresponding to a percentage of 21.82%. The
other prominent structure. No ATF was identified in a values presented
​​ are similar to those described by
lateral position to the TF (Table 2). Esakkiammal and Chauhan (2016)7, who reported the
Finally, as shown in the linear dimensions of the ATF presence of 37 (27.6%) ATF in 134 analyzed vertebrae.
analyzed, the mean transverse diameter was 3.11 ± 0.51 Only simple cervical vertebrae were considered by
mm (range 1.86 to 4.30 mm) and 3.13 ± 0.52 mm (range this study, since the analysis did not identify the
1.84 to 4.30 mm) on the right and left, respectively. presence of ATF in C1 or C2. In addition, Chaudhari et
The longitudinal diameter was 2.49 ± 0.41 mm (range al. (2013)1 also described a prevalence of 31 (23.15%) in
from 1.90 to 3.47 mm) and 2.47 ± 0.49 mm (range 133 vertebrae analyzed, thus bringing an analysis close
from 1.59 to 3.45 mm), also on the right and left sides, to that identified in this study.
respectively. There were no differences between the On the other hand, Murlimanju et al. (2011)8
linear parameters verified in the accessory transverse described the presence of only 6 (1.6%) ATF in 363
foramen between two sides of the vertebrae (p<0.05) vertebrae analyzed, contrasting with the proportion
(Table 3). analyzed in the present study. Also, Murlimanju et al.

Table 1. Distribution of the Accessory Transverse foramen (ATF) in the analyzed vertebrae (N = 165).

Vertebrae With FTA Without FTA Total

Atlas 4 (2.43%) 40 (24.24%) 44 (26.67%)
Axis 8 (4.84%) 48 (29.09%) 58 (35.15%)
Typical (C3-C7) 24 (14.54%) 39 (23.64%) 63 (38.18%)
Total 36 (21.82%) 129 (78.18%) 165 (100%)

Table 2. Qualitative analysis of ATF laterality, shape and position. N = 47.

Laterality Shape Position
Unilateral Bilateral Incomplete Complete Anterior Posterior Lateral
25 (15.1%) 11 (6.7%) 28 (59.6%) 19 (40.4%) 3 (6.4%) 44 (93.6%) -

Table 3. Mean (mm) ± standard deviation (SD) values ​​of the morphometric parameters analyzed in the accessory transverse foramen (ATF) of the cervical vertebrae.
N = 47.

Right side Left side

Parameters Min - Max Mean (SD) Min - Max Mean (SD)
TD 1.86-4.30 3.11±0.51 1.84-4.30 3.13±0.52
LD 1.59-3.47 2.49±0.41 1.59-3.45 2.47±0.49
TD: Transverse diameter of ATF; LD: longitudinal diameter of ATF; N: number; Min: Minimum; Max: Maximum; SD: Standard Deviation.

Discussion (2011)8 described the presence of ATF only on cervical

Changes in the embryological process of vessel vertebrae. In this same perspective, Das S et al. (2005)9
formation in the cervical region are the main causes published a study in which the presence of the ATF was
of the appearance of accessory transverse foramen. described in 2 (1.5%) of 132 vertebrae analyzed. Sharma
Although there is still no consensus regarding its et al. (2010)10 described the presence of 16 (8%) ATF in
clinical manifestations, it is extremely important that 200 vertebrae, notably at the C6 level. Finally, Taitz
its morphological knowledge is analyzed in surgical et al. (1978)11 used a sample space of 480 vertebrae, in
approaches, as to fix vertebrae fractures, for example, which the ATF was identified in only 34 (7%) (Table 4).
and imaging exams in the region. This literature review on the subject has shown a
Hence, believing in the importance of identifying higher prevalence of the ATF in the vertebrae of this
morphometric distinctions between epidemiological study in contrast to a considerable part of the existing
groups analyzed, enabling a more precise knowledge publications, although some authors demonstrate
for the professionals working with this specific area of similar values.1,7 It is notorious, however, to emphasize
the body, the present study analyzed the prevalence that there are very few reports about the presence

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Morphometric Analysis of The Accessory Transverse Foramen in a Population in Northeastern Brazil Medeiros JPM et al.

of ATF in atlas or axis vertebrae (C1 and C2 levels, of 24 complete ATFs against only 7 in their incomplete
respectively), with the descriptions being very morphology. Such data are correspondent with the
restricted to typical cervical vertebrae only. description of Gonsai et al. (2015)13, whose sample
Esakkiammal and Chauhan (2016)7 and Murlimanju presented 40 vertebrae that had the ATF in complete
et al. (2011)8 published that the presence of ATF was shape, while only 22 were incomplete, and with the
only described in typical cervical vertebrae, whereas analysis of Kumari et al. (2015)15, in which 22 ATF were
Akhtar et al. (2015)12 cites the presence of ATF in 9 complete and only 9 were incomplete.
atypical vertebrae. However, the author does not These data contrast with those identified by
mention any axis vertebrae on his report with this Esakkiammal and Chauhan (2016)7, who described the
structure. In contrast, this present study identified prevalence of 19 complete morphology ATF and 24 in
4 C1 vertebrae and 8 C2 vertebrae that had the ATF. its incomplete presentation, and with those exposed in
Although it is still mostly described in typical cervical
the present analysis, since it has described only 19 ATF
vertebrae (24 in the present study), the fact that the
in its complete morphology and 28 of the accessory
ATF is identified in atypical cervical vertebrae, both C1
transverse foramen as being incomplete. Therefore, the
and C2 is a highly innovative finding in the area.
innovative character of the study is again perceived, as
Additionally, Akhtar et al. (2015)12 describes 20
unilateral and 5 bilateral ATFs, just like Gonsai et al. it brings relevant information with divergent outcomes
(2015)13 does, identifying 31 unilateral and 9 bilateral, in the literature (Table 6).
being in correspondence with the findings in the Finally, the quantitative analysis described in the
present study (25 vertebrae with unilateral ATF and 11 results of the present study is more complete than
with bilateral ATF). On the other hand, Esakkiammal the existing records in the literature, considering that
and Chauhan (2016)7 and Mishra et al. (2015)14 reported the articles that mention the size of the ATF do so in
a more frequent bilaterality in their analysis, with 18 a brief way, only highlighting the fact of presenting
unilateral and 19 bilateral for the first and 10 unilateral smaller diameters than the foramen transverse itself,
and 21 bilateral for the second one (Table 5). without going deeper into the measurements made
Other studies have also classified their analysis as and described here previously, with emphasis on the
to whether the ATF is complete or incomplete. The fact that there is no differences between the right and
prevalence identified by Mishra et al. (2015)14 consisted left sides of ATF.

Table 4. Comparison of the percentage of ATF in different populations.

Population Total Vertebrae Vertebrae with ATF

Taitz et al. 1978,11 Tel-Aviv, Israel 480 34 (7%)
Das S et al. 2005, Bangi, Malaysia
9
132 2 (1.5%)
Sharma et al. 2010, India 10
200 16 (8%)
Murlimanju et al. 2011,8 India 363 6 (1.6%)
Chaudhari et al. 2013,1 Bhuj, India 133 31 (23.15%)
Esakkiammal and Chauhan. 2016,7 Delhi, India 134 37 (27.6%)
Present study 165 36 (21.82%)

Table 5. Comparative analysis of ATF laterality.

Population Unilateral ATF Bilateral ATF

Akhtar et al. 2015,12 India 20 5
Gonsai et al. 2015,13 Ahmedabad, India 31 9
Mishra et al. 2015,14 Lucknow, India 10 21
Esakkiammal and Chauhan, 2016, Delhi, India 7
18 19
Present study 25 11

Table 6. Comparative analysis of ATF shape.

Population Complete ATF Incomplete ATF

Gonsai et al. 2015, Ahmedabad, India
13
40 22
Mishra et al. 2015,14 Lucknow, India 24 7
Kumari et al. 2015,15 Kishanganj, India 22 09
Esakkiammal and Chauhan, 2016, Delhi, India 7
19 24
Present study 19 28

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Medeiros JPM et al. Morphometric Analysis of The Accessory Transverse Foramen in a Population in Northeastern Brazil

Conclusion of the study, bringing significant contributions to

For the first time, the prevalence of the accessory the anatomy field in Brazil and serving as a basis for
transverse foramen was demonstrated in a population neurosurgeons, head and neck surgeons, orthopedists,
in Northeastern Brazil, along with a complete analysis radiologists and physiotherapists. Morphological
of the morphometric parameters of this structure, knowledge is clinically important, as it can suggest
such as location in relation to the transverse foramen, changes in the vertebral artery and in the venous
unilateral or bilateral character and complete or plexuses that surround it in its vertebral segment
incomplete shape. The presence of the accessory passing through the transverse foramen.
transverse foramen was observed in 21.82% of the The presence of the accessory transverse foramina
cases, with the unilateral presence being more frequent may suggest fenestrations or duplications in the
than the bilateral and all cervical vertebrae (Atlas, Axis
vertebral artery or in important veins. Variations
and Typical C3 to C7) being affected by this variation.
in their location, shape and quantity can increase
Incomplete morphology prevailed and the posterior
relationship with FT was more frequent. The study the risk of injury to these vessels during surgical
found no significant differences in transverse and access to the cervical spine, which can produce
longitudinal diameters when laterality was considered. clinical complications and iatrogenic injuries. Finally,
These identifications contrasted to several findings compression of the vertebral artery during neck
in the literature, such as the higher prevalence of the movement can cause basilar failure, characterized by
ATF in this analysis, evidencing the innovative character headache, fainting and hearing problems.

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Received: January 30, 2019 Corresponding author

Accepted: July 25, 2020 André de Sá Braga Oliveira
andre.sboliveira@gmail.com

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