Anatomical variations of the superior thyroid and superior laryngeal

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ORIGINAL ARTICLE
ANATOMICAL VARIATIONS OF THE SUPERIOR THYROID
AND SUPERIOR LARYNGEAL ARTERIES
Teresa Vázquez, PhD,1 Rosana Cobiella, MD, PhD,1 Eva Maranillo, MD, PhD,1
Francisco Jose Valderrama, PhD,1 Stephen McHanwell, PhD,2 Ian Parkin, MD, PhD,3
Jose Ramon Sañudo, MD, PhD1
1
Department of Human Anatomy and Embryology, I. School of Medicine, Complutense University of Madrid,
Madrid, Spain. E-mail: tvazquez@med.ucm.es
2
Oral Biology, School of Dental Sciences, Dental School, Newcastle University, Framlington Place,
Newcastle upon Tyne NE2 4HH, United Kingdom
3
Cuschieri Surgical Skills Centre, Ninewells Hospital, Dundee, United Kingdom
Accepted 30 October 2008
Published online 1 April 2009 in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/hed.21077
Abstract: Background. There are known to be variations in
the origins of the superior thyroid artery (STA), an important
surgical landmark, and 1 of its branches, the superior laryngeal artery (SLA).
Methods. Three hundred thirty human embalmed heminecks were dissected. The results of previous studies were
reviewed, and a meta-analysis is presented.
Results. Four different origins for the STA were found. The
most frequent was type I, from the carotid bifurcation (49%).
Four different origins were also found for the SLA being the
most frequent the type I in which the artery arose from STA
(78%). The mean external diameters of STA and SLA were
0.26 and 0.20 cm, respectively, with no statistically significant
differences by side or sex.
Conclusion. Variations in the origin of STA and SLA from
the carotid arterial tree and the similarity of their diameters
mean that there is a significant possibility of their misidentified
C 2009 Wiley Periodicals, Inc. Head Neck
during surgery. V
31: 1078–1085, 2009
Keywords: superior thyroid artery; superior laryngeal artery;
external carotid artery; carotid arterial axis; arterial variations
Correspondence to: T. Vázquez
C 2009 Wiley Periodicals, Inc.
V
1078
Superior Thyroid Artery Variations
Clinical diagnosis and surgical procedures
require a thorough knowledge not only of the
normal gross anatomy of the structures within a
region but also of the common and less-common
anatomical variations of the structures located
within it. Recent and continuing advances in surgical procedures have made the need for such
detailed knowledge ever-more important. This
article describes variations in the normal anatomy of the superior thyroid artery (STA) and 1 of
its main branches, the superior laryngeal artery
(SLA). The STA is frequently used as a recipient
vessel for microvascular free tissue transfer in
head and neck surgery, for selective embolization
of thyroid and head and neck tumors, and as a
landmark for identifying the superior laryngeal
nerve in thyroid surgery.1–4 Consequently, it is
important to have a clear understanding of the
variations in the anatomy of this artery and to
be able to distinguish it from 1 of its key
branches in situations in which normal anatomical variation could lead to them being confused.
HEAD & NECK—DOI 10.1002/hed
August 2009
Table 1. Types of origin of superior thyroid artery based on incidence.
No. of cases/total sample (%)
Author
Type I
8
Quain
Livini10
Poynter11
Adachi12
Aaron and Chawaf14
(anatomical sample)
Poissel and Golth15
Lucev18
Our results
Meta-analysis
81/300 (27)
82/187 (44)
37/156
9/40
102/207
311/890
(24)
(22)
(49)
(35)
Type II
41/292
18/200
14/200
39/300
24/187
10/156
19/40
55/207
220/1582
Type III
(14)
(9)
(7)
(13)
(13)
177/300 (59)
80/187 (43)
(6)
(47)
(26.6)
(14)
103/156
12/40
48/207
420/890
(66)
(30)
(23)
(47)
Type IVa
2/302
3/200
1/200
6/300
11/187
Type IVb
(1)
(1)
(1)
(2)
(6)
(0)
5/156 (3)
(1)
2/300 (1)
30/1645 (2)
1/300 (0)
(0)
Comparison with consulted bibliography. Type I, origin from carotid bifurcation; type II, origin from common carotid artery; type III, origin from external
carotid artery; type IVa, thyrolingual trunks; type IVb: thyrolinguofacial trunks.
origins of the STA or SLA from the carotid arterial tree. We consider these earlier classifications difficult to apply in a clinical setting, and
so have attempted to devise a simple classification that is easier and more useful to employ in
surgical practice.
Furthermore, some angiographic procedures
require more complete quantitative information
about certain parameters, including the diameters of their branches and distances of the origins of these arteries from carotid bifurcation.
In the previous literature surveyed, these data
are largely absent, with only 1 study providing
data on the endoluminal diameter of the STA,
which it gives as 2.5 mm.17 There have been no
studies that provide information on the diameter of SLA.
The aim of this study was to evaluate, in a
large, statistically reliable sample of human
cadavers, the normal anatomical variation in
In the standard textbooks of anatomy or surgery, the STA is considered to have a relatively
constant origin from the anterior surface of the
external carotid artery (ECA); with the SLA
originating from the STA as 1 of its major
branches.5–7 However, within the literature,
many different variations in origin have been
reported for both arteries, including their arising from either of the other carotid arteries or
arising from carotid arterial tree in common
with other arterial trunks8–18 (Tables 1 and 2).
Although some classifications of the variations
in the anatomy of these arteries have been published, they are complex and elaborate, being
based either on either the number of collateral
branches arising from the STA or, more frequently, on the number and relative position of
the collateral branches of the ECA.10,14 We have
not found, in the literature surveyed, any classifications that are based exclusively on specific
Table 2. Types of superior laryngeal artery origins based on incidence.
No. of cases (%)
Author
8
Quain
Schwalbe and Pfitzner9
Livini10
Adachi12
Terracol and Guerrier13
Andrea16
Our results
Meta-analysis
Total sample
292
132
200
215
42
247
142
1270
Type I
266
92
175
198
29
232
111
1103
(91)
(70)
(72)
(92)
(69)
(94)
(78)
(87)
Type II
24
32
25
9
11
13
13
127
(8)
(24)
(12)
(4)
(26)
(5)
(9)
(10)
Type III
Type IV
2 (1)
1 (1)
–
–
2 (5)
–
7 (5)
12 (1)
–
–
–
–
–
–
6 (4)
–
Comparison with consulted bibliography. Type I, origin from the superior thyroid artery; type II, origin from external carotid artery; type III, origin from
common carotid artery.
Superior Thyroid Artery Variations
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FIGURE 1. Anterior views of isolated carotid arterial systems that show the superior thyroid artery possible origins. (A) Type I from
the carotid bifurcation (49.3%); (B) Type II from the common carotid artery (26.6%); and (C) Type III from the external carotid artery
(23.2%). ap, ascending pharyngeal artery; cc, common carotid artery; ec, external carotid artery; fa, facial artery; ic, internal carotid
artery; la, lingual artery; oa, occipital artery; st, superior thyroid artery.
the origins of the STA and SLA from the carotid
arterial tree, 2 arteries that are of surgical importance. The rationale for this study been the
lack of reliable information from previous studies. This study also reviewed the results of those
earlier studies, performed a meta-analysis of
their results, and compared them with the
results obtained in this study.
made using the chi-square test, with a value of
p < .05 taken as a statistically significant one.
Previous published results were carefully
reviewed and compared to present a meta-analysis, and from the results in the present study, a
unified and simple classification is proposed.
RESULTS
MATERIALS AND METHODS
A total sample of 165 human cadavers (330
heminecks) embalmed at the Department of
Anatomy, University of Cambridge, UK, was
examined over a period of 4 years. The sex distribution was 74 men and 91 women cadavers,
with an age range of 60 to 103 years. Clinical
histories were available, and in no case contained any reference to vascular surgical intervention. Based upon the completeness of the
neck structures after dissection, 3 different samples of the available cadavers were taken to
study the following parameters: the origin and
external diameter of the STA—207 heminecks
(95 women and 112 women); the occurrences of
the STA arising in common with other
arteries—330 heminecks (148 men and 182
women); the origin and external diameter of the
SLA—142 heminecks (63 men and 79 women).
Distances and external diameters were measured with calipers. Statistical comparisons were
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Superior Thyroid Artery Variations
The results show that the origins of the STA
from the carotid arterial tree showed could be
classified into 4 different types (see Figures 1
and 2). In 102 of the 207 cases with an incidence
of 49%, the STA was found to arise at the level
of the carotid bifurcation; this was classified as
type I. In 55 of the 207 cases with an incidence
of 27%, the STA was found to arise from the
common carotid artery; this was classified as
type II. Our data showed a statistically significant difference in type II origins between sides,
with the frequency of occurrence being much
higher on the left than the right (p ¼ .03). In
contrast, there was no statistically significant
difference in type II origins between men and
women. In type III, the STA arose from ECA,
and this was found to occur in 48 of the 207
cases; an incidence of 23%. A type IV origin for
the STA was defined as being when the artery
arose as a common trunk with 1 of more of the
other branches of the carotid arterial tree. It
was subdivided into type IVa, where the STA
HEAD & NECK—DOI 10.1002/hed
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FIGURE 2. Superior thyroid artery combined origins (type IV). (A) Left hemineck. Thyrolingual trunk from external carotid artery (type
IVa). (B) Right hemineck. Thyrolingual trunk from common carotid artery (type IVa). (C) Left hemineck. Thyrolingualfacial trunk (type
IVb), cb, carotid bifurcation; cc, common carotid artery; eln, external laryngeal nerve; ec, external carotid artery; fa, facial artery; h,
hyoid bone; ic, internal carotid artery; iln, internal laryngeal nerve; la, lingual artery; oa, occipital artery; s, sympathetic trunk; sla, superior laryngeal artery; slv, superior laryngeal vein; st, superior thyroid artery; tc, thyroid cartilage; tg, thyroid gland; th, thyrohyoid muscle; tlt, thyroid-lingual trunk; XII, hipoglossal nerve. [Color figure can be viewed in the online issue, which is available at
www.interscience.wiley.com.]
arose with the lingual artery to form a common
thyrolingual trunk. This was infrequent, occurring in just 2 of 330 cases; an incidence of 0.6%.
In 1 type IVa case, the thyrolingual trunk arose
from the ECA in a left hemineck (see Figure
3A), while in the other, it arose from the common carotid artery in a right hemineck (see Figure 3B). In type IVb origin was defined as
where the STA arose in common, with the lingual and facial arteries forming a common thyrolinguofacial trunk. This was found in a single
case (see Figure 3C). In those cases in which
the STA originated from the carotid arterial tree
as a single independent branch, it was found
that there was a statistically significant difference between that originating from the carotid
bifurcation (type I) compared to types II and III
(p < .03)
For the meta-analysis, incidences were calculated simply by dividing the number of cases of
each origin by the number of cases. In calculating total incidences for types I and III, the
results from some authors were excluded.8,10,11
This was because they failed to distinguish
between arteries that arose from the carotid
bifurcation and those that arose from the ECA
itself. Also, the anatomical results of Aaron and
Chawaf14 were included in the analysis (see Table 1).
Superior Thyroid Artery Variations
For the cases classified as type II origins,
where the STA arose from the common carotid
artery the distance from the origin of the STA to
the carotid bifurcation was found to vary
between 0.1 and 2.1 cm. In type III in which the
artery originated from the ECA, the distance
FIGURE 3. Distances to carotid bifurcation. ‘‘y’’ axis represents
distance intervals in centimeters (cm); ‘‘x’’ axis represents percentages of cases belonging to each interval. Cases in which
SLA arose from STA are not represented. Values under 0
include origins from common carotid artery: STA type II and
SLA type III. Values below 0 include origins from external carotid artery: STA type III and SLA type II. Percentage corresponding to value 0 represents STA and SLA origins at carotid
bifurcation level.
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1081
FIGURE 4. Superior laryngeal artery possible origins. (A) Right hemineck. Type I; (B) Left hemineck. Type II, (C) Right hemineck.
Type III. cb, carotid bifurcation; cc, common carotid artery; eln, external laryngeal nerve; ec, external carotid artery; fa, facial artery; h,
hyoid bone; iln, internal laryngeal nerve; oh, omohyoid muscle; sh, sternohyoid muscle; sla, superior laryngeal artery; sm, sternothyroid muscle; smg, submandibular gland; st, superior thyroid artery; tc, thyroid cartilage; th, thyrohyoid muscle; tt, trunk formed by junction of thyroid, lingual, pharyngeal, and facial veins (Farabeuf trunk); XII, hipoglossal nerve; jv, jugular vein. [Color figure can be
viewed in the online issue, which is available at www.interscience.wiley.com.]
from origin to the carotid bifurcation varied
between 0.1 and 1.5 cm (see Figure 3). In 1 case
of the common thyrolingual trunk that originated, the ECA was found to arise just 0.3 cm
above the bifurcation while the common thyrolingual trunk that arose from the common carotid artery did so 2 cm below the bifurcation.
In the majority of cases for all types, the origin of the STA was found to be from the anterior
face of the carotid arterial tree (95%, p ¼ .01).
The external diameter of the STA was found
to range from 0.1 to 1.5 cm, with a mean of 0.26
cm and a standard deviation of 0.12 cm. There
were no statistically differences by sex or side.
In a similar manner, the results on the
origins of the SLA showed that these could be
classified into 4 different types (see Figure 4). A
type I origin was defined as where the SLA
arose from the STA. This was by far the commonest type occurring in 111 of the 142 cases,
an incidence of 78%. In this type, the distance
between the origin of the SLA and the origin of
the STA varied between 0 and 3.4 cm; but in
most cases, the artery was found to arise 0.5 cm
from the STA. In type II, the SLA arose from
the ECA, and this was found in 13 of 142 cases
(9%). In type III, the SLA arose from the common carotid artery, and this was found in 7 of
142 cases (5%). In type IV, the SLA arose from
the carotid bifurcation, and this was found in 6
of 142 cases (4%). In a further 5 cases, the SLA
was absent (4%). Type II and II origins were
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Superior Thyroid Artery Variations
found to occur more frequently on the left than
the right (p ¼ .06%). The distance of the origin
of the artery from the carotid bifurcation ranged
between 0.2 and 2.5 cm. Figure 1 shows the frequencies of distribution.
The external diameter of the SLA was found
to range from 0.1 to 1.5 cm, with a mean of 0.20
cm and a standard deviation of 0.19 cm. There
were no statistically differences by sex or side.
DISCUSSION
Variations in the origins of the superior thyroid
and superior laryngeal arteries have been
reported by many authors,8–18 but there have
been no previous studies that have attempted to
classify the origins of these arteries that have
been based exclusively upon their origins from
the carotid arterial tree.
From our own results and from our review of
the literature, the origins of STA and SLA could,
in each case, be classified into 4 patterns depending upon their site of origin from the carotid arterial tree. These classifications have enabled us
to determine incidences for each origin, and this
has enabled us to compare our results with those
of previous authors and thus to present a metaanalysis of those studies with similar methodologies to our own (Tables 1 and 2).
The normally reported pattern of origin of
the STA describes it as arising from the ECA,
HEAD & NECK—DOI 10.1002/hed
August 2009
with the SLA arising as a collateral branch of
the STA. This pattern is equivalent in our classification to a type III origin for the STA and a
type I origin for the SLA. This accepted normal
arrangement differs from our own observations
on the origins of the STA, probably because earlier authors failed to distinguish clearly between
an origin of the artery from the carotid bifurcation and an origin from ECA.8,10,11 We consider
that this increased the incidence of reported
origins from the ECA (type III in our classification). Although the meta-analysis shows a
higher incidence of STA type III origin even
when these earlier authors8,10,11 were excluded,
the results of our work show that type III is the
least frequently observed. From our results, the
highest incidence is of type I, in which STA
arises from carotid bifurcation (49%), while the
frequency of occurrence of types II and III is
almost equally distributed (26% and 23%,
respectively).
Cases in which STA originates in common
with 1 or more arteries forming either a common thyrolingual or thyrolinguofacial trunk
have been classified as type IV in our study.
These have been described with a variable incidence by previous authors.7,8,12,14,15,17 Our
results for these combined origins have been
compared with those previously reported (Table
1) and are in disagreement with those obtained
from our meta-analysis, in which previously a
higher incidence has been reported. One of the
thyrolingual trunks (type IVa) observed in the
present study arose from the common carotid
artery 2 cm below carotid bifurcation; such an
origin has been only reported twice previously,19,20 in each case the origin being located 3
cm below the carotid bifurcation. A type IVb origin for the STA has been described only in sporadic cases.9,12,15 One report14 describes this
situation in occurring in 2% of cases in a radiological sample, which is higher than we
observed in our cadaveric sample (0.30%),
although this could be due to the different methodology. This study14 as well as other studies
relying upon data derived from radiological
studies were excluded in the calculation of total
incidence in meta-analysis for type IVa. There
have been no previously reported data on type
IVb cases to allow us to perform a metaanalysis.
In the case of the SLA, all authors agree
that its most frequent origin is from the STA,
and the results of the systematic literature
Superior Thyroid Artery Variations
review show incidences only slightly different
from those of our own observations of type I and
II origins (see Table 2). There is, however, a
much greater discrepancy in the reported frequencies of type III origin, which has only previously been reported by a few authors.8,9,13 Our
results are similar to those of Terracol and
Guerrier.13 A type IV origin, in which the SLA
arises from carotid bifurcation, has not been
previously described; previous authors may
have considered this to have been a type II or
III origin.
There have been a few reports describing an
origin for the SLA from the lingual artery or
another, unspecified, artery,9,10,12,13,16 giving frequencies of occurrence between 0.7% and 5.10%.
In our study, no cases were found in which the
SLA arose from the lingual or any other
arteries. In 5 cases, we found the SLA to be
absent (3.5%), which represents the lowest
reported incidence of this situation.10,16
Differences in origin for sex and side have
only been described previously for the STA. The
origin of the left STA was described as being
located at a lower level than on the right,10 and
the origin of the artery from the common carotid
artery was described with a higher frequency on
the left side and in women, though this study
provides no quantitative results to support these
statements.12 In our results, only statistically
significant differences in origin with respect to
side have been observed, the main differences
we observe are that the STA arises from a common carotid artery with a higher frequency in
the left side (p ¼ .03), and type II and III origins
for the SLA are more frequent also on the left
side (p ¼ .06).
Only 1 report mentions the position of the origin of the STA in relation to the carotid axis,10
with this study describing its most frequent
position as being at the internal face of carotid
axis. However, in our study, the origin of the
STA was located more frequently at the anterior
face (95.2%).5,6
Although the origin of the superior thyroid
artery has usually been described as being
located very close to the carotid bifurcation,5,6
the exact value of this distance has been only
once reported and with the reported distance
ranging from between 1.5 cm below the bifurcation to 2.5 cm above it.10 In our study, we found
that the origin of the STA varied from between
2 cm below the carotid bifurcation to 1.5 cm
above it. In the case of type II origin for the
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STA, this was found to be at a mean distance of
0.7 cm, whereas that for the type III was found
to be at a mean distance of 0.45 cm from the carotid bifurcation in each case (see Figure 1).
The exact position of SLA on the carotid arterial axis, in cases in which the artery arises
from ECA (type II), has been reported previously only once.10 Our results partially agree
with that study in which the mean distance to
the carotid bifurcation was very similar to the
previously reported one (1.1 cm). In our sample,
cases in which SLA arose from ECA (type II),
did so at a distance 0.5 cm from the bifurcation, which means that the SLA arose in a similar area to that which might be expected for the
origin of the type III STA (see Figure 1).
Regarding the diameter of the STA, our
results (mean value ¼ 0.26 cm) are in agreement with those of Czerwinski,17 who measured
the STA endoluminal diameter in 240 cases.
From the literature consulted, there appears to
be no data about external diameter of the SLA,
although a descending order for the diameter of
the 16 collateral branches of the ECA has been
previously described. In this previous report,
the diameter of the STA was the third largest in
size after the facial and lingual arteries,10 and
SLA the smallest together with that of the sternocleidomastoid artery. In our results, STA was
found to be the fourth largest vessel in diameter, after the facial, lingual, and occipital
arteries. The range of diameters of the superior
thyroid and superior laryngeal arteries were
identical, and the mean diameters were similar,
which means that it would be quite possible to
confuse these 2 arteries in situations in which
their origins are variable.
Variations in the origin of the superior thyroid and superior laryngeal arteries could have
important surgical repercussions. The STA is
normally considered to be the first branch arising from the ECA and is used as a surgical
landmark for differentiating the external from
the internal carotid artery, since no cervical
branches normally arise from the latter or from
the carotid bifurcation.5–7 Our results show,
however, that the possibility that the first artery
arising from ECA or from carotid bifurcation is
the SLA rather than STA always needs to be
borne in mind.
The accepted site of ECA ligation is inferior
to the origin of the STA. However, its closeness
to the carotid bifurcation may make this surgically difficult, and it is accepted that ligating
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Superior Thyroid Artery Variations
above the STA may still preserve a good collateral circulation.5,21 Again, our results show that
the variable origin of the STA and the fact that
the SLA usually arises less than 1 cm from the
ECA means that the STA is neither a reliable
landmark for the identification of ECA nor to
identify a safe point for its ligation. The only
reliable method to identify ECA is that it would
always be safer to identify several collateral
branches of the ECA before carrying out this
procedure on it.22
A further comment should also be made
about the incidence of thyrolingual or thyrolinguofacial trunks (STA, types IVa and IVb).
Although they are rare anatomical variations,
they are yet further examples of variation in the
expected pattern of branches of the ECA that
may be encountered during surgery.
Our proposed classification provides a means
of classifying simply how the superior thyroid
and superior laryngeal arteries arise in relation
to carotid bifurcation, a site involved in many
surgical procedures. Awareness of these variations and a careful examination is necessary
before performing any invasive procedure and
will allow the surgeon to define the vascular
pattern and so avoid unexpected injuries. This
study also highlights that the STA may not be
considered as a constant surgical landmark for
these procedures as may have been previously
thought.
CONCLUSIONS
In the majority of cases (75%), the STA does not
arise from ECA but from the common carotid artery, with this occurring more frequently on the
left than on the right (p ¼ .03). A common thyrolingual trunk was present in 0.9% of cases
and thyrolinguofacial trunks in 0.3% of cases. In
95.2% of cases (p < .01), the STA was found to
arise from anterior aspect of the carotid arterial
tree.
The SLA was found to originate more frequently from STA (78.2%), although it was also
observed arising from either the external or the
common carotid arteries. Superior laryngeal
arteries arising directly from either of these carotid arterial branches was observed more
frequently on the left (p ¼ .06). When SLA was
observed arising from ECA in most of the cases,
it did so from an area where the STA might
normally be expected to occur, and since both
HEAD & NECK—DOI 10.1002/hed
August 2009
arteries have similar external diameters, they
could in such situations be easily confused.
These results underline the importance for
surgical practice of understanding these patterns of variation in situations where the STA is
being used as a landmark, a recipient vessel or
for selective embolization and emphasize the
unreliability of the commonly accepted criteria
for identifying this artery.
Acknowledgment. Authors thank
León for his valuable statistical advice.
Dr.
X.
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HEAD & NECK—DOI 10.1002/hed
August 2009
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