European Annals of Otorhinolaryngology, Head and Neck diseases 132 (2015) 265269 [627811]
European Annals of Otorhinolaryngology, Head and Neck diseases 132 (2015) 265–269
Available online at
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Original article
Recurrent laryngeal nerve landmarks during thyroidectomy/H22845
A.-R. Ngo Nyekia,∗, L.-R. Njockb, J. Miloundjac, J.-E. Evehe Vokwelyd, G. Bengonoe
aService d’oto-rhino-laryngologie et de chirurgie cervico-faciale (ORL-CCF), hôpitaux universitaires de Genève, 4, rue Gabrielle-Perret-Gentil, 1211 Genève
14,
Switzerland
bService d’ORL et de chirurgie cervico-faciale, hôpital Général, Douala, Cameroon
cService d’ORL et de chirurgie cervico-faciale, hôpital d’instruction des armées Omar Bongo Ondimba, Libreville, Gabon
dService d’ORL et de chirurgie cervico-faciale, centre hospitalier d’Essos, Yaoundé, Cameroon
eService d’ORL et de chirurgie cervico-faciale, centre hospitalier universitaire, Yaoundé, Cameroon
a r t i c l e i n f o
Keywords:Recurrent laryngeal nerve
ThyroidectomyInferior thyroid artery
African
populationa b s t r a c t
Objective: This study was designed to describe the various anatomical relations of the recurrent laryngeal
nerve (RLN) during thyroid surgery in a Central African population.
Patients and methods: A prospective study was conducted between January 2012 and December 2012
in 5 otorhinolaryngology and head and neck surgery departments in Cameroon and Gabon. All patients
undergoing total or subtotal thyroidectomy or loboisthmectomy with recurrent laryngeal nerve dissec-
tion, with no history of previous thyroid surgery, RLN dissection or tumour infiltration of the RLN, were
included.Results: Fifty-six patients were included, corresponding to 36 loboisthmectomies and 20 total or subtotal
thyroidectomies. A total of 62 recurrent laryngeal nerves were identified: 32 on the right and 30 on the
left. The course of the recurrent laryngeal nerve in relation to branches of the inferior thyroid artery (ITA)
was retrovascular in 53.1% of cases on the right and 76.6% of cases on the left; transvascular in 15.6% of
cases on the right and 13.4% of cases on the left. The course of the recurrent laryngeal nerve was modified
by thyroid disease in 12.9% of cases. Six cases (9.7%) of extralaryngeal division of the recurrent laryngeal
nerve were observed. No case of non-recurrent nerve was observed in this series.
Conclusion: The anatomical relations of the recurrent laryngeal nerve with the inferior thyroid artery
were very inconstant in this series and were predominantly retrovascular or transvascular in relation
to the branches of the artery. The presence of extralaryngeal branches and modification of the course
of the nerve by thyroid disease also introduced additional difficulties during recurrent laryngeal nerve
dissection. The anatomical relations of the right recurrent laryngeal nerve in this African population differ
from the classically described prevascular course.
©
2015 Elsevier Masson SAS. All rights reserved.
1. Introduction
Thyroid surgery is one of the most commonly performed proce-
dures in head and neck surgery. It represents 11.3% of all head and
neck procedures in Yaoundé, Cameroon [1] and 12.72% in Libreville,
Gabon [2].
Nevertheless, one of the major risks of this surgery is recurrent
laryngeal nerve (RLN) palsy, which, when it is bilateral, induces
laryngeal diplegia with major respiratory consequences sometimes
requiring tracheotomy or segmental posterior cordectomy. The
/H22845Subject of the article presented to the 120th congress of the Société franc ¸ aise
d’ORL
et de chirurgie de la face et du cou (SFORL) Paris-France, 12–14 October 2013.
∗Corresponding
author. 46, avenue de Miremont, 1206 Genève, Switzerland.
E-mail address: adelerose nyeki@yahoo.fr (A.-R. Ngo Nyeki).incidence of recurrent laryngeal nerve complications in the African
and international literature currently ranges between 2 and 6%
[3,4] .
A good knowledge of the anatomy of the thyroid region is
essential to avoid RLN lesions. It has now been clearly established
that visualization of the RLN remains the main factor determining
preservation of nerve function and a decreased incidence of postop-
erative recurrent laryngeal nerve palsy [5–8] . Systematic dissection
of the RLN has therefore become the standard technique to reduce
the risk of recurrent laryngeal nerve palsy [7]. Visualization of the
anatomical relations of the recurrent laryngeal nerve with branches
of the inferior thyroid artery (ITA) remains essential for preserva-
tion of recurrent laryngeal nerves. Classically, the right recurrent
laryngeal nerve more frequently presents a prevascular course than
the left recurrent laryngeal nerve, as it arises higher than the left
nerve and has a more oblique course.
http://dx.doi.org/10.1016/j.anorl.2015.08.002
1879-7296/© 2015 Elsevier Masson SAS. All rights reserved.
266 A.-R. Ngo Nyeki et al. / European Annals of Otorhinolaryngology, Head and Neck diseases 132 (2015) 265–269
Several studies of the anatomy of the recurrent laryngeal nerve
and the anatomical relations with the ITA have been conducted in
Africa [9,10] . These studies demonstrated that the RLN has a pre-
dominantly posterior course in relation to the ITA. The objective of
this study was to describe the various anatomical relations of the
RLN during thyroid surgery in a Central African population.
2. Patients and methods
A prospective and descriptive study was conducted in the
otorhinolaryngology and head and neck surgery departments in
five hospitals in Cameroon and Gabon: Yaoundé university hospital,
Yaoundé general hospital, Douala general hospital, Essos Hospi-
tal in Yaoundé, and Omar Bongo Ondimba military hospital in
Libreville. This study was conducted over a 12-month period, from
January 2012 to December 2012.
2.1. Patients
All patients undergoing total or subtotal thyroidectomy or
loboisthmectomy with recurrent laryngeal nerve dissection were
included and patients with a history of thyroidectomy or RLN dis-
section, and patients with tumour infiltration of the RLN were
excluded.
2.2. Operative technique
All operations were performed under general anaesthesia. The
operative technique was performed according to 9 main steps:
•Kocher neck incision and creation of platysma skin flaps;
•exposure
of the thyroid gland;
•primary or final isthmectomy;
•dissection
of the lateral surface of the lobe with ligation of middle
thyroid veins;
•dissection of the inferior pole with ligation of inferior thyroid
veins;
•ligation of the superior vascular pedicle as close as possible to the
superior pole;
•identification and dissection of the RLN;
•lobectomy;
•closure.
The
same technique was performed on the other side in the case
of total thyroidectomy. The sequence of operative steps sometimes
differed according to the department in which the thyroidectomy
was performed and the approach used to identify the RLN. Pho-
tographs of the various steps of identification and dissection of
recurrent laryngeal nerves were taken to illustrate the operative
reports.
Various characteristics were reported for each patient: the type
of operation performed and its indication, the method of identifi-
cation of the RLN, the various anatomical relations of the recurrent
laryngeal nerve especially with the ITA, variations of the course of
the RLN due to thyroid disease, the presence of any extralaryngeal
divisions and the presence of a non-recurrent laryngeal nerve.
2.3. Statistical analysis
All data were recorded on a predefined form comprising all
intraoperative data and a description of the various steps. Data
analysis was performed with Statistical Package for Social Sciences
(SPSS) version 19.0 and Excel 2010 for Windows software. Data
were compared between groups, especially left and right sides,by Fisher’s exact test. A P-value <0.05 was considered statistically
significant.
2.4. Ethical considerations
Informed consent was obtained from all patients before the
operation and approval was obtained from the Yaoundé School of
Medicine Ethics Committee (Cameroon), and the Department of
Medical Affairs and Quality of the Omar Bongo Ondimba military
hospital in Libreville (Gabon).
3. Results
3.1. Population
A total of 56 patients were included in this study: 52 women
(92.86%) and 4 men (7.14%) with a sex ratio of 0.08 and a mean
age of 40.89 years (range: 16 to 62 years). Surgery consisted of 36
loboisthmectomies and 20 total or subtotal thyroidectomies. A total
of 62 recurrent laryngeal nerves were identified.
3.2. Methods of identification of the RLN
The approach most commonly used to identify the RLN was a lat-
eral approach in 59.7%, allowing postero-anterior thyroidectomy.
The distribution of surgical approaches to the RLN is reported in
Table 1.
3.3. Anatomical relations of the RLN with the ATI and its
branches( Table 2)
3.3.1. Anatomical relations with the trunk of the ITA
3.3.1.1. Right. Thirteen recurrent laryngeal nerves crossed the ITA
(40.6%): 7 anteriorly (21.9%) and 6 posteriorly (18.7%).
3.3.1.2.
Left. The recurrent laryngeal nerve crossed the ITA in 11
cases (36.6%): 10 posteriorly (33.3% of the overall sample). Only
one laryngeal nerve crossed in front of the ITA.
3.3.2.
Anatomical relations with branches of the ITA
3.3.2.1. Right. Of the 32 RLNs dissected, 19 crossed branches of the
ITA (59.4% of the overall sample); 11 RLN (34.4%) crossed behind
branches of the inferior thyroid artery (retrovascular course); 8 RLN
(15.6%) passed between branches of the ITA (transvascular course).
Table 1
Various
approaches to recurrent laryngeal nerve (RLN) dissection.
Approaches to RLN dissection Number of patients %
Lateral 37 59.7
Anterograde
or inferior 20 32.2
Retrograde or superior 5 8.1
Total
62 100
Table 2
Position
of the recurrent laryngeal nerve (RLN) in relation to the trunk and branches
of
the inferior thyroid artery (ITA).
Right RLN Left RLN
n % n %
Anterior to the trunk of the ITA 7 21.9 1 3.3
Posterior
to the trunk of the ITA 6 18.7 10 33.3
Anterior to branches of the ITA 3 9.4 2 6.7
Posterior
to branches of the ITA 11 34.4 13 43.3
Between
branches of the ITA 5 15.6 4 13.4
Total
32 100 30 100
P = 0.054: no statistically significant difference.
A.-R. Ngo Nyeki et al. / European Annals of Otorhinolaryngology, Head and Neck diseases 132 (2015) 265–269 267
3.3.2.2. Left. Of the 30 RLNs dissected: 19 crossed branches of the
ITA (63.3% of the overall sample); 13 (43.3%) dissected RLN passed
behind branches of the ITA; 4 RLN (13.4%) passed between branches
of the ITA.
Among the 6 patients in whom bilateral dissection was per-
formed, one half presented different anatomical relations with the
ITA and its branches on each side.
The majority of RLNs in this series had a retrovascular course
(with respect to the ITA or its branches): 53.1% on the right and
76.6% on the left (Table 3).
3.4. Anatomical relations with the suspensory ligament of Berry
The course of 58 (93.6%) of the dissected nerves was posterolat-
eral to the suspensory ligament of Berry, while the other 4 nerves
(6.4%) passed between the fibres of this ligament. Arteriolar bleed-
ing during dissection of the RLN was frequently observed in this
zone (51/62, 82.25%).
3.5. Anatomical relations with the inferior horn of the thyroid
cartilage
All RLNs penetrated into the larynx by passing posteriorly to the
inferior horn of the thyroid cartilage on both the left and right sides.
3.6. Variations of the course of the RLN due to thyroid disease
Eight (12.9%) cases of RLN adherent to the posterolateral surface
of the thyroid were observed (Fig. 1). Five cases were observed in
a context of very large multinodular or plunging goitres and the
other 3 cases were observed in a context of simple nodules.
Table 3
General
relations of the recurrent laryngeal nerve (RLN) with the inferior thyroid
artery
(ITA).
Course of the RLN Right RLN Left RLN
n % n %
Passes in front of the ITA (trunk and
branches; prevascular course)10 31.3 3 10
Passes behind the ITA (trunk and
branches; retrovascular course)17
53.1 23 76.6
Passes between the branches of the
ITA
(transvascular course)5 15.6 4 13.4
Total 32 100 30 100
P = 0.07: no statistically significant difference.
Fig. 1. Left recurrent laryngeal nerve (white arrows) adherent to the lateral surface
of
a multinodular goitre.
Fig. 2. Extralaryngeal bifurcations of the left recurrent laryngeal nerve. Arrows indi-
cate
2 nerve branches.
3.7. Anatomical variants of the RLN
No case of non-recurrent laryngeal nerve was observed in our
series. Six cases (9.7%) of extralaryngeal divisions of the RLN were
observed, all corresponding to bifurcations (Fig. 2) and all situ-
ated distal to the passage of the RLN with the ITA. Five cases were
observed on the left and one case was observed on the right, includ-
ing a bilateral variant in one patient.
Nine cases of transient recurrent laryngeal nerve palsy and no
case of permanent RLN palsy were observed in this series of 62 RLN
dissections.
4. Discussion
4.1. Approaches to identification of the recurrent laryngeal nerve
(RLN)
Several approaches to RLN dissection can be are used. The
approach most commonly used in our series was the lateral
approach in 59.7% of cases, corresponding to the most frequently
used incision. Its main landmark is the inferior thyroid artery (ITA)
at the middle or lower third of the posterolateral surface of the
thyroid lobe. It requires identification of the recurrent laryngeal
nerve in the middle third of the lateral lobe. This approach is rec-
ommended for simple cervical goitres and thyroid nodules [11,12] .
However, this approach can be difficult or even impossible in
the presence of a very large and/or plunging goitre, short neck or
limited morphological neck extension, in which the lateral or infe-
rior approach to the RLN [11] may be advantageously replaced by
a superior approach with preliminary dissection of the superior
vascular pedicle followed by craniocaudal dissection of the RLN. A
superior approach to the RLN was used in our series in 8.1% in cases
of plunging or very large goitres. According to some authors [13,14] ,
this retrograde approach allows good exposure of the nerve and
limits the risk of recurrent laryngeal nerve damage in the presence
of a large goitre.
4.2. Anatomical relations of the RLN and the ITA
The anatomical relations between the RLN and ITA constitute
a classical landmark for recurrent laryngeal nerve dissection Sev-
eral authors have therefore studied the value of this landmark, since
the meta-analysis by Flament et al. [14] until the most recent series
published by Kulekci et al. [15] . In the present series of 62 dissected
nerves, the relations between the RLN and the ITA essentially con-
cerned especially branches of the ITA (59.4% on the right and 63.4%
on the left), with a predominantly retrovascular course (34.4% on
the right and 43.3% on the left). These results are similar to those of
268 A.-R. Ngo Nyeki et al. / European Annals of Otorhinolaryngology, Head and Neck diseases 132 (2015) 265–269
operative series reported by several authors [10,16] . However, the
various relations of the RLN with the ITA observed in our series did
not present any significant differences according to the side.
We observed a considerable percentage of RLNs passing
between branches of the ITA (transvascular course, 15.6% on the
right and 13.4% on the left). According to some authors, this
transvascular pattern is predominant and would expose the RLN to
an increased risk of intraoperative injury, especially during exces-
sive medial traction of the gland designed to improve visibility of
the nerve, ranging from simple stretching to complete section of
the nerve [10,17] .
Various positions of the RLN in relation to the ITA have been
described over the decades, either in the context of intraoperative
dissections or on anatomical specimens [9,14,16–18] . However,
many authors consider that the “classical position” of the RLN
would be anterior to the ITA on the right and posterior to the ITA
on the left in more than 50% of cases [19,20] . Extreme caution is
therefore necessary when ligating branches of the ITA. In our series,
in the 6 patients in whom bilateral dissection was performed, one
half of patients had a different course of the RLN of each side, as also
reported by Sturniolo et al., who also demonstrated differences in
the anatomical relations of the RLN with the ITA on either side in
the same patient [16] . These findings therefore suggest that the ITA
should not be used as the sole landmark for RLN dissection.
Bleeding from branches of the ITA during dissection also high-
lights the need for other important anatomical landmarks to guide
RLN dissection, especially the suspensory ligament of Berry and the
inferior horn of the thyroid cartilage.
4.3. Anatomical relations with the suspensory ligament of Berry
The suspensory ligament of Berry or lateral thyrohyoid ligament
is a fibrous structure between the posterior surface of the lateral
lobes of the thyroid and the cricoid cartilage and the lateral sur-
faces of the first three tracheal rings. It constitutes an important
landmark of the course of the RLN before its enters the larynx.
In this study, 93.6% of RLNs had a posterolateral course with
respect to this ligament and 6.4% of nerves crossed the fibres of
this ligament. These findings are in agreement with the data of the
literature [9,18] .
However, passage of the nerve through the fibres of the sus-
pensory ligament of Berry still remains very controversial. The RLN
is generally posterolateral to the ligament, but some authors have
reported that the RLN can penetrate the ligament [12] . This has
been challenged by other authors [21,22] , who consider that the
RLN has a more medial course with respect to the ligament, giving
an impression of transfixing the ligament.
We observed arterial bleeding in the distal segment of the RLN
in 82.25% of cases in our series, corresponding to the zone of the
suspensory ligament of Berry. This bleeding is due to damage of the
posterior arterial branch of the ITA that follows the course of the
RLN [23] . This bleeding interferes with final dissection of the nerve
and haemostasis must be meticulously ensured by bipolar cautery
[18,22] .
The dense and richly vascular suspensory ligament of Berry, the
presence of this arteriole supplying the RLN and its intimate rela-
tionship with thyroid tissue make dissection of the RLN particularly
delicate at the almost final phase of release of the lobe [23] .
4.4. Anatomical relations with the inferior horn of the thyroid
cartilage
In this series of 62 dissections, all recurrent laryngeal nerves
penetrated the larynx by passing posteriorly to the inferior horn
of the thyroid cartilage. The inferior horn of the thyroid cartilage,
considered in the literature to be the most reliable landmark of therecurrent laryngeal nerve, indicates the point of entry of the nerve
into the larynx.
The constancy of this anatomical landmark has been demon-
strated for several decades in the majority of dissection studies
[9,24] . This landmark is situated 0.8 cm ± 4 mm inferiorly and pos-
teriorly to the inferior horn of the thyroid cartilage and is easily
palpable [21,24] . The point of laryngeal penetration of the RLN is a
very important anatomical landmark, especially when inferior and
lateral surgical approaches are difficult, as in the case of very large
or plunging goitres or in the presence of a non-recurrent laryngeal
nerve [11,13] .
4.5. Variations of course of the RLN caused by thyroid disease
The RLN was adherent to the thyroid gland in 8 cases, i.e. 12.9%
of the sample. This anomaly is observed in the presence of thy-
roid nodules arising from the lateral lobes, but especially in the
context of multinodular goitres, as these tumours displace the RLN
and therefore modify its normal course [16] . This modification of
the course of the RLN has rarely been reported in series in which
recurrent laryngeal nerve dissection was performed on anatom-
ical specimens, as the exclusion criteria for most of these studies
included the presence of thyroid tumour or a history of thyroid dis-
ease [18,19] . In these studies, the anatomy of the RLN was therefore
not altered by the presence of a nodule or by the size or type of
goitre, in contrast with the population of the present series.
4.6. Anatomical variants of the RLN
4.6.1. Non-recurrent laryngeal nerve
No case of non-recurrent laryngeal nerve was observed in
our series, as reported by other authors [16,21] . This anatomical
anomaly remains rare, representing less than 1% of cases in many
series [9,25] . It is generally observed on the right, except in patients
with situs inversus, with a retro-tracheo-oesophageal course of the
left subclavian artery. This anomaly is usually an incidental finding,
with a risk of intraoperative nerve injury.
4.6.2.
Extralaryngeal divisions of the RLN
Six (9.7%) of the 62 nerves dissected in this series presented
extralaryngeal divisions of the recurrent laryngeal nerve, all corre-
sponding to bifurcations distal to the inferior thyroid artery.
Extralaryngeal divisions are reported to be fairly frequent in
the literature, with rates ranging between 24 and 70% [22,25] . The
low rate observed in our study could be explained by the fact that
extralaryngeal divisions were not systematically investigated in
this study and were often incidental findings.
In five of these six patients, bifurcation of the RLN was observed
on the left side, as reported in the majority of publications [18,25] ,
which have sometimes reported as many as 5 branches of the recur-
rent laryngeal nerve. These branches remain very variable and may
differ from one side to the other in the same patient. Extralaryn-
geal divisions generally give 2 branches: an anterior motor branch
and a posterior sensory branch. The discovery of an abnormally
thin nerve must alert the surgeon to the possibility of a second
branch coursing towards the larynx. The current use of intraoper-
ative nerve monitoring is particularly useful to identify the nerves
in these complex situations [6–8] .
5. Conclusion
In contrast with the classical data reported in the literature, this
preliminary study illustrates the numerous anatomical variants of
the RLN with respect to the ITA and its branches. The RLN mainly
has a retrovascular course on both the right and the left sides. The
presence of extralaryngeal branches and modification of the course
A.-R. Ngo Nyeki et al. / European Annals of Otorhinolaryngology, Head and Neck diseases 132 (2015) 265–269 269
of the nerve as a result of thyroid disease constitute additional dif-
ficulties for recurrent laryngeal nerve dissection. Thyroid surgery
training requires repeated procedures on anatomical preparations.
The hypothesis of anatomical specificities of the RLN related to a
specific population of Central Africa must be confirmed by studies
on a larger series of patients.
Disclosure of interest
The authors declare that they have no conflicts of interest con-
cerning this article.
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