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Anatomical and Clinical Relevance of the Thyroid Foramen

Authors:
  • University of Health Sciences, Gulhane Faculty of Medicine
  • Seattle Science Foundation

Abstract

Objective: The thyroid foramen (TF) is an opening on the lamina of the thyroid cartilage. It may be located on the posterosuperior part of the lamina or below the superior tubercle. The aim of the present study was to determine the incidence of the foramen in an adult Turkish population and the morphometry, topography, and structures within it, thereby aiding surgeons working in this area.Methods: In 57 formalin-fixed cadaveric laryngeal specimens, 113 (56 right and 57 left) sides were dissected using a surgical microscope.Results: The TF was observed in 6 out of 57 (10.5%) specimens. It was bilateral in 3 (5.3%) specimens; thus, it was observed in 9 sides. It was located at (33.3%) or posterior to (66.7%) the oblique line and below the superior tubercle. It was crossed by only a nerve in 2 (22.2%) left sides, an artery with a vein in 2 (22.2%) sides, or a neurovascular bundle in 5 (55.6%) sides.Conclusion: The TF is a variation located on the lamina of the thyroid cartilage with an incidence of 2% to 57% in adults. Neurovascular structures can pass through it. It is important in two aspects: surgical exposure and spread of laryngeal tumors.
DOI: 10.5152/EurJTher.2018.487
European Journal of Therapeutics
Anatomical and Clinical Relevance of the Thyroid
Foramen
Bülent Yalçın1 , Sedat Develi1 , R. Shane Tubbs2 , Necdet Kocabıyık1 ,
Selda Yıldız1 , Nurcan Ercıktı1
1Department of Anatomy, University of Health Sciences, Gülhane School of Medicine, Ankara, Turkey
2Division of Pediatric Neurosurgery, Children’s Hospital of Alabama, Birmingham, AL, USA
ABSTRACT
Objective: The thyroid foramen (TF) is an opening on the lamina of the thyroid cartilage. It may be located on the posterosuperior
part of the lamina or below the superior tubercle. The aim of the present study was to determine the incidence of the foramen in an
adult Turkish population and the morphometry, topography, and structures within it, thereby aiding surgeons working in this area.
Methods: In 57 formalin-fixed cadaveric laryngeal specimens, 113 (56 right and 57 left) sides were dissected using a surgical mi-
croscope.
Results: The TF was observed in 6 out of 57 (10.5%) specimens. It was bilateral in 3 (5.3%) specimens; thus, it was observed in 9
sides. It was located at (33.3%) or posterior to (66.7%) the oblique line and below the superior tubercle. It was crossed by only a
nerve in 2 (22.2%) left sides, an artery with a vein in 2 (22.2%) sides, or a neurovascular bundle in 5 (55.6%) sides.
Conclusion: The TF is a variation located on the lamina of the thyroid cartilage with an incidence of 2% to 57% in adults. Neurovas-
cular structures can pass through it. It is important in two aspects: surgical exposure and spread of laryngeal tumors.
Keywords: Thyroid cartilage, thyroid foramen, superior laryngeal nerve
The study has been presented in 7th International Symposium of Clinical and Applied Anatomy (ISCAA) meeting hold on 17-20
September 2015 in Bratislava.
ORCID IDs of the authors: B.Y. 0000-0003-1653-3701; S.D. 0000-0002-3712-7510; R.S.T.0000-0003-1317-1047; N.K. 0000-
0003-2164-9231; S.Y. 0000-0002-7324-7165; N.E. 0000-0002-7836-0095.
Corresponding Author: Bülent Yalçın E-mail: bulent.yalcin@sbu.edu.tr
Received: 13.02.2018 • Accepted: 04.04.2018
©Copyright by 2018 Gaziantep University School of Medicine - Available online at www.eurjther.com
Original Research
168
INTRODUCTION
The thyroid cartilage is the most prominent cartilage of the lar-
ynx. It consists of two hyaline cartilage flats called laminae. The
apparent protrusion of the anterior fusion of these laminae is
called laryngeal prominence. On the lateral side of each lamina,
a slight crest extending from the superior thyroid tubercle to the
inferior thyroid tubercle is called the oblique line. The posterior
borders of the laminae do not fuse and deviate laterally. The su-
perior and inferior extensions seen on the posterior border are
called superior and inferior cornu (1).
The thyroid foramen (TF) is an opening located in one or both
posterosuperior parts of the lamina of the thyroid cartilage and
below the superior tubercle. Its presence over the thyroid carti-
lage lamina becomes apparent from the middle of the first tri-
mester and closes during the subsequent trimesters. If there is a
problem at the conjunction point of the cartilage tissue between
the 4th and the 6th pharyngeal arches, the foramen can remain
open (2, 3). The incidence of the TF has been variously reported,
ranging from 2% to 57% in adults (4, 5). It is sometimes double
but is more often seen in single form (3, 6, 7). Its location has
been reported as posterior or anterior to the oblique line and
below the superior tubercle. The foramen might contain only a
nerve or vessel or house a neurovascular bundle. The nerve anas-
tomoses between the external branch of the superior laryngeal
nerve (ebSLN) and the internal branch of the superior laryngeal
nerve (ibSLN) (3, 6–8) or between the ebSLN and the recurrent
laryngeal nerve (9, 10). The arterial branch is usually an aberrant
superior laryngeal artery (SLA) (3, 6, 9). The foramen is rarely cov-
ered only by the connective tissue with no content.
The TF is generally found incidentally during imaging examina-
tions, larynx surgery or dissection of the neck. Its presence and
content can be clinically important. Surgeons should be careful
to avert from iatrogenic damage to the nerve or bleeding of the
vessel when they place a surgical retractor or reflect the soft tis-
sue around the larynx.
The aim of the present study was to determine the incidence
of the TF in an adult Turkish population and the morphometry,
topography, and structures within it, thereby aiding surgeons
working in this area.
METHODS
The study was conducted with 57 formalin-fixed cadaveric laryn-
geal specimens. A total of 113 (56 right and 57 left) sides were
investigated. Dissections were made using a Zeiss OpM1 surgical
microscope (OpM1; Carl Zeiss, Oberkochen, Germany). One right
side was not suitable for dissection. After the soft tissue around the
larynx was removed, the strap muscles were exposed. The muscle
parts attaching to the thyroid cartilage were incised to expose the
lamina of the cartilage and TF clearly. The soft tissue occupying
the outer and inner openings of the foramen and surrounding
its content was also cleaned to measure its dimensions and to
follow the contents to their origin points. The inferior constrictor
muscle was subsequently incised at the midline to view inside the
lamina of the thyroid cartilage. This enabled us to follow the con-
tents throughout their length. The incidence, location, contents,
and diameters of the TF were recorded. Finally, the structure was
documented using a high-resolution photography. The vertical
length of the TF was regarded as the widest site of the foramen.
The horizontal length of the foramen was considered as the lon-
gest distance between the superior and the inferior edges of the
foramen. Measurements were made using a digital vernier caliper
(D&W Measuring-1kds15, China). The local ethics committee ap-
proved the study (University of Health Sciences, Gülhane School of
Medicine-2016-16), patient approval was not necessary since the
current study was conducted on cadaveric specimens.
Statistical Analysis
Descriptive analyses were made for all variables. Statistical re-
sults represented as mean ± standard deviation. Statistical anal-
yses of data were performed using Statistical Package for the
Social Sciences for Windows, version 16.0. (SPSS Inc.; Chicago, IL,
USA), at a statistical significance set at p<0.05.
RESULTS
The TF was observed in 6 out of 57 (10.5%) specimens. It was bi-
lateral in 3 (5.3%) specimens, suggesting that it was observed in
9 out of 113 (7.9%) sides. Table 1 shows the mean values of the
horizontal and vertical diameters of the outer and inner open-
ings of the TF and the distance between the superior tubercle
and the TF.
The TF was located at (33.3%, Figure 1a) or posterior to (66.7%,
Figure 1b) the oblique line and below the superior tubercle in
all nine sides.
The foramen was crossed by only a nerve originating from the
ebSLN. This was observed in 2 (22.2%, Figure 2a) sides. After pass-
ing, it anastomosed with the ibSLN in all 9 sides (Figure 2b). The
foramen was also crossed by an artery with a vein observed in 2
(22.2%, Figure 3a) sides. The artery originated directly from the
superior thyroid artery (STA). No SLA was observed. After passing
through the foramen, the artery spread to the area supplied by
the SLA (Figure 3b). Finally, the foramen was crossed by a neuro-
vascular bundle observed in 5 (55.6%, Figure 4a) sides. The nerve
of the bundle emerged from the ebSLN and anastomosed with
the ibSLN in all cases. The artery of the bundle originated from the
STA directly or from its glandular branches. After passing through
the foramen, the artery anastomosed with the SLA. If no SLA was
observed (in two sides), the area normally supplied by the SLA was
supplied by the artery passing through the TF (Figure 4b).
Yalçın et al. Thyroid Foramen in Turkish PopulationEur J Ther 2018; 24(3): 168-72
169
Table 1. Mean values of the measurements of the TF (mm)
Vertical distance of Horizontal distance Vertical distance Horizontal distance Distance between
the outer side of the of the outer side of the inner side of the inner side the superior tubercle
foramen of the foramen of the foramen of the foramen and the TF
2.3±1.0 2.2±0.9 3.1±0.9 2.4±0.7 6.7±2.9
a b
Figure 1. a, b. Right laminae of the thyroid cartilage. The thyroid foramen (white arrow) was located at (a) or posterior (b) to the
oblique line. It was below the superior tubercle
TC: thyroid cartilage; OL: oblique line; SH: superior horn
DISCUSSION
The embryological development of the TF is controversial. The
embryonic draft of the thyroid laminae begins to develop in
the first trimester as quadrilateral plates with a foramen. In the
following stages of embryogenesis, the TF closes. However, hes-
itation or distortion of the fusion of the cartilaginous tissue be-
tween the fourth and the sixth pharyngeal arches may lead to
the foramen to remain open (2, 3). Other studies have indicated
that the shape of the TF is formed due to the content of the fora-
men, affecting the proper chondrification of the thyroid lamina
(6). This satisfactorily explains why the TF is almost always locat-
ed on the posterosuperior aspect of the laminae, in the neigh-
borhood of the superior thyroid tubercle (3, 6). Muller et al. (11)
reported that the descent of the ebSLN over the thyroid cartilage
during the development of the larynx results in the formation of
the foramen.
This incidence of the TF has been variously reported as ranging
from 2% to 57% in adults and from 12.5% to 76.9% in fetuses. Its
incidence differs greatly among the adult population: 33%–57%
170
Yalçın et al. Thyroid Foramen in Turkish Population Eur J Ther 2018; 24(3): 168-72
a
Figure 2. a, b. (a) Outer and (b) inner surface of the right lamina of the thyroid cartilage. The thyroid foramen (white arrow) was
crossed by only a nerve originating from the external branch of the superior laryngeal nerve. After passing, the nerve anastomo-
sed with the internal branch of the superior laryngeal nerve
TC: thyroid cartilage; n: nerve; ebSLN: external branch of the superior laryngeal nerve; ibSLN: internal branch of the superior laryngeal nerve; SH: superior horn
b
a
Figure 3. a, b. (a) Outer and (b) inner surface of the left lamina of the thyroid cartilage. The thyroid foramen (white arrow) was
crossed by an artery with a vein. The artery originated directly from the superior thyroid artery
TC: thyroid cartilage; a: artery; v: vein; STA: superior thyroid artery; SH: superior horn
b
in the USA, 2%–55% in Europe, 10%–16% in India, 27.3%–50% in
Japan, and 7.5%–17.3% in South Africa (3). Ortug et al. (12) ob-
served the TF in 12% of 50 Turkish cadavers, and it was found in
10.5% of 57 cadaveric laryngeal specimens in the present study.
The foramen appears solitary and unilateral in 0% to 42.9% of
cases but bilateral in 0% to 31.3% (4, 9, 13). An equal incidence
of the unilateral and bilateral TFs was also reported (3). There are
few studies of double TFs in the literature (6, 7). There were bilat-
eral TFs in 5.3% of specimens in the present study, but no double
ones were observed.
The foramen was located posterior to the oblique line in 60%
and 61.9%, at the oblique line in 14.3% and 20%, or anterior to it
in 20% and 23.8% (3, 14). Ramsaroop et al. (7) stated that it was
most often located anterior to the linea obliqua. It has also been
reported as located below the oblique line in 68.29%, above it
in 21.95%, and right at the upper end in 9.76% of cases (6). In
the present study, it was found to be at the oblique line in 33.3%
and posterior to it in 66.7%. It was located below the superior
tubercle in all nine sides. The distance between the foramen and
the superior tubercle was reported as 10 mm (9) and found to be
6.7±2.9 mm in the present study.
The diameter of the TF ranged from 0.5 to 9 mm (3, 9). It was
reported as 0.5–6 mm in males and 0.45–6.5 mm in females (15).
The mean horizontal and vertical diameters were reported as 2.8
and 3.3 mm on the right side and 3.1 and 3.4 mm on the left side,
respectively (14). According to our results, the outer vertical and
horizontal diameters were 2.3±1.0 and 2.2±0.9 mm, respectively,
whereas the inner vertical and horizontal diameters were 3.1±0.9
and 2.4±0.7 mm, respectively.
The TF passed by neurovascular structures 6.5% to 83.3% was
crossed by only a nerve originating from the ebSLN and anas-
tomosing with the ibSLN inside the larynx (8, 12). In the present
study, the same variation was observed in 2 (22.2%) sides. The
TF passed by neurovascular structures 7% to 33% was crossed
by only an artery, usually a communicating branch between
the SLA and the cricothyroid vessels or an aberrant SLA (3, 6, 12,
16). In contrast, the TF was crossed by an artery with a vein in 2
(22.2%) sides. The artery originated directly from the STA. No SLA
was observed. Since the artery spread to the area supplied by the
SLA, it was regarded as an aberrant SLA. The TF passed by neuro-
vascular structures 16.7% to 100% was crossed by a neurovascu-
lar bundle (4, 6–9, 12, 13). In the present study, a neurovascular
bundle coursing through the TF was observed in 5 (55.6%) sides.
Its nerve originated from the ebSLN and anastomosed with the
ibSLN in all cases. Its artery originated from the STA directly (ab-
errant SLA) or from its glandular branches.
Partab et al. (10) reported an interesting case of double neural
anastomosis running through the TF. In this case, two neural
loops were observed. The proximal loop was reported to be be-
tween the ebSLN and ibSLN, whereas the distal loop was report-
ed to be between the ebSLN and the recurrent laryngeal nerve.
The existence of the TF is most likely to be asymptomatic, but it
is very significant in surgeries of the larynx, such as partial lar-
yngectomy or partial reconstruction. Its location and contents
Yalçın et al. Thyroid Foramen in Turkish PopulationEur J Ther 2018; 24(3): 168-72
171
a b
Figure 4. a, b. (a) Outer and (b) inner surface of the left lamina of the thyroid cartilage. The thyroid foramen (white arrow) was
crossed by a neurovascular bundle. The nerve of the bundle emerged from the external branch of the superior laryngeal nerve
and anastomosed with the internal branch of the superior laryngeal nerve. The artery of the bundle originated from the superior
thyroid artery directly or from its glandular branches
TC: thyroid cartilage; n: nerve; ebSLN: external branch of the superior laryngeal nerve; ibSLN: internal branch of the superior laryngeal nerve; a: arter y; STA:
superior thyroid artery; SH: superior horn
are important for surgeons performing laryngeal procedures
(3). Since the artery passing through the TF supplies the area of
the SLA when the SLA is absent, surgeons should remember the
aberrant artery to avoid injury. Another way in which the TF is
important concerns the spread of tumors: a TF containing neu-
rovascular structures is a possible pathway for tumor spread (12).
CONCLUSION
The TF was observed in 6 out of 57 (10.5%) specimens. It was bi-
lateral in 3 (5.3%) specimens. It was situated at (33.3%) or poste-
rior to (66.7%) the oblique line and below the superior tubercle.
The foramen was crossed by only a nerve (22.2%), only a vessel(s)
(22.2%), or a neurovascular bundle (55.6%). The nerve extended
between the ebSLN and the ibSLN in all cases. The artery origi-
nated from the STA directly or from its glandular branches. Sur-
geons should be aware of the unusual course of the neurovas-
cular structures on the surface of the thyroid cartilage to avoid
injuring the nerve and artery passing through the TF.
Ethics Committee Approval: Ethics committee approval was received for
this study from the ethics committee of University of Health Sciences,
Gülhane School of Medicine (No: 2016-16).
Informed Consent: Informed consent was not necessary since the cur-
rent study was conducted on cadaveric specimens.
Peer-review: Externally peer-reviewed.
Author Contributions: Concept – B.Y., S.D.; Design – B.Y., S.D.; Supervi-
sion – R.S.T., N.K.; Resources – N.K., S.Y., N.E.; Materials - N.K., S.Y., N.E.; Data
Collection and/or Processing – B.Y., S.D., R.S.T.; Analysis and/or Interpre-
tation – B.Y., S.D., R.S.T.; Literature Search – N.K., S.Y., N.E.; Writing Manu-
script – B.Y., S.D., R.S.T.; Critical Review – R.S.T., N.K.
Conflict of Interest: The authors have no conflicts of interest to declare.
Financial Disclosure: The authors declared that this study has received
no financial support.
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How to cite:
Yalçın B, Develi S, Tubbs RS, Kocabıyık N, Yıldız S, Ercıktı N.
Anatomical and Clinical Relevance of the Thyroid Foramen.
Eur J Ther 2018; 24(3): 168-72.
172
Yalçın et al. Thyroid Foramen in Turkish Population Eur J Ther 2018; 24(3): 168-72
... Its existence and composition can hold clinical significance. Surgeons must exercise caution to prevent inadvertent damage to the nerve or vascular bleeding when positioning a surgical retractor or manipulating the soft tissue surrounding the larynx [45]. Previously, a systematic review was conducted more than a decade ago to provide a review of the available literature, comment on the demographics, frequency, and morphometry [33]. ...
... [3] 2.5 mm Grüber [12] 0.5-0.9 mm Kirchner et al. [23] 2.5 + 1.6 mm (less than 1 mm to 6 mm) Lang et al. [25] 2.5-4 mm Ortuğ et al. [31] 1.1-6 mm Ramsaroop et al. [34] Horizontal diameter: 2.9 mm (right), 2.8 mm (left) Vertical diameter: 3.1 mm (right), 2.6 mm (left) Roncallo [35] 'Very small' (2 cases) and 'about 5 mm' (1 case) Sharada et al. [40] Horizontal diameter: 2.29 mm (right), 2.73 mm (left) Vertical diameter: 3.34 mm (right), 3.9 mm (left) Tanaka et al. [42] 3-4 mm Yalçın et al. [45] Outer width: 2.2 + 0.9 mm Inner width: 2.4 + 0.7 mm Zemlin et al. [48] 0.45-6.5 mm (females), 0.5-6 mm (males) ...
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... Ortug et al. (2005) found a foramen thyroideum in 12% of cases, exclusively males [12]. However, the incidence of the foramen thyroideum has been reported in various ways, ranging from 2 to 57% in adults and 12.5% to 76.9% in foetuses [17]. Vazquez et al. (2009) classified the origin of the SLA into four types: type I-SLA leaves the STA (78%), type II-SLA leaves the ECA (9%), type III-SLA from the common carotid artery (5%), and type IV-SLA leaves the carotid bifurcation (4%) [16]. ...
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The superior laryngeal artery supplies blood to the larynx and has important implications for neck surgery. We report a unilateral, anomalous continuation of this superior laryngeal artery in an elderly male cadaver. The superior laryngeal artery was enlarged from its origin down to the lateral lamina of the thyroid cartilage. At this point, the artery passed through the lamina and continued as an internal branch that supplied the larynx. No other vascular anomalies were noted. Although this anatomical variation is uncommon, the possibility of its occurrence should be kept in mind by clinicians and surgeons who manipulate this anatomical area. CASE REPORT INTRODUCTION The superior laryngeal artery (a. laryngea superi-or) accompanies the internal laryngeal branch of the superior laryngeal nerve beneath the thyreohyoideus muscle and pierces the hyothyroid membrane to sup-ply the muscles, mucous membrane, and glands of the larynx before anastomosing with the branch from the opposite side [4,7,10,13]. The presence of an anomalous foramen in the thyroid cartilage lamina is rare [2,5,6,14], as are anomalies of the superior laryngeal artery [2]. However, variations in the nerves and arteries of this region has been documented [1,2,8] including the inferior thyroid artery and its branches [2,11,12]. Aberrant branches of the superior laryngeal nerve passing through the thyroid foramen have been reported [3,9]. Here, we describe a rare variation of the superior laryngeal artery that passes through the lateral lamina of the thyroid cartilage. MATERIAL AND METHODS This study was approved by the ethics committee for human research at the Federal Fluminense University and complied with the declaration of Helsinki (as revised in Edinburg, 2000) and with the guidelines of an internal review board. REPORT OF CASE During gross anatomical dissection of the right neck of a male cadaver fixed in 10% formalin, the right superior laryngeal artery was found to be slightly enlarged from its origin down to the lateral lamina of the thyroid cartilage. At this point, the artery passed through the lamina and continued as internal branch that supplied the larynx (supraglotic region) (Figs.1 and 2). The anomalous artery originated from the superior thyroid artery and had abnormal course only in the opening for the larynx. No other vascular anomalies were noted. DISCUSSION This anomaly was an interesting finding be-cause of its uncommon nature [2,4,7,10,13], partic-ularly since most reports only mention the possible presence of a foramen in the thyroid cartilage lamina [2,5,6,10,14]. Anomalous branches of the superior la-ryngeal artery are uncommon [2]. However, the supe-rior laryngeal nerve has been reported to run through the thyroid cartilage [3,9]. The surgical implications of these variations have been discussed by Kirchner et al. [6] and Espinoza et al. [3]. Bergman et al. [2] pointed out that the superior la-ryngeal artery may occasionally traverse the thyroid car-tilage through an anomalous foramen, but these authors did not comment on the possibility of an aberrant superi-or laryngeal artery passing through the thyroid foramen. Indeed, this variation has been reported only by Adachi [1] in Japanese cadavers. Hence, the present report is one of the few cases in the literature. This anatomical vari-ation should be kept in mind by clinicians and surgeons who may manipulate this anatomical area. ACKNOWLEDGMENTS The authors thank Mr. Rafael L.R. Maciel for performing the schematical drawings.
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