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ARTICLE IN PRESS

Motor function of the recurrent


laryngeal nerve: Sometimes
motor fibers are also located in
the posterior branch
Mehmet Uludag, MD,a Nurcihan Aygun, MD,a and Adnan Isgor, MD,b Istanbul, Turkey

Background. The function of the extralaryngeal branches of the recurrent laryngeal nerve (RLN) has yet
to be described precisely. The goal of this study was to evaluate the incidence and motor function of the
extralaryngeal branches of the RLN.
Methods. Our study group consisted of 335 consecutive patients undergoing thyroid and parathyroid
operations in whom the branches of the RLNs (n = 200) were evaluated with intraoperative nerve
monitoring and by measuring the distance from the point of branching of the RLN into anterior and
posterior branches and the entry of the individual branches into the larynxdefined as the branching
distance. Anterior and posterior branches of the RLN were assessed separately by electromyography (using
a standard electromyography endotracheal tube) for adduction and by finger palpation for abduction.
The RLNs were classified as having motor function only in the anterior branches (Group 1) or function
both in the anterior and posterior branches (Group 2).
Results. There were 185 RLNs in Group 1 and 15 RLNs in Group 2, assessed by intraoperative nerve
monitoring. Motor function was detected in all anterior branches of the RLN (100%) and in 8% of the
posterior branches. The mean branching distance was greater in Group 2 compared with Group 1
(24.1 13.6 mm, 17.3 8.5 mm, respectively, P = .045).
Conclusion. Although the anterior branch of RLN always has motor function, the posterior branch also
has motor function in about 8% of patients. The probability of detecting motor function in the posterior
branch was greater among early branching RLNs, which have a greater branching distance. The surgeon
should remember that posterior branches may contain motor fibers and protect these branches to avoid
postoperative vocal cord dysfunction. (Surgery 2016;j:j-j.)
From the General Surgery,a Sisli Hamidiye Etfal Education & Research Hospital, and General Surgery,b
Bahcesehir University, Istanbul, Turkey

RECURRENT LARYNGEAL NERVE (RLN) palsy is one of


the main problems after thyroid and parathyroid
operations.1 Although exposure and visualization
The authors declare that this study received no financial support. There was no financial or professional association between
the authors and the commercial company supplying the nervemonitoring product.
Author contributions: conception and design, MU, AI; acquisition of data, MU, NA; analysis and interpretation of data, MU,
NA; writing article, MU, NA; and critical revision, AI, MU.
Presented at the First World Congress of Neural Monitoring in
Thyroid and Parathyroid Surgery on September 17-19, 2015,
Krakow, Poland.
Accepted for publication February 3, 2016.
Reprint requests: Mehmet Uludag, MD, General Surgery, Sisli
Hamidiye Etfal Education & Research Hospital, Istanbul,
Turkey. E-mail: drmuludag@hotmail.com.
0039-6060/$ - see front matter
2016 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.surg.2016.02.003

of the RLN is the gold standard for prevention of


injury to the RLN,2 visual integrity alone of the
RLN does not guarantee preservation of motor
function, because the RLN has been noted to be
structurally intact in 72%88% of patients who
have evidence of RLN injuries postoperatively.3,4
Anatomic variations in the RLN are a wellknown risk factor for RLN injury.5 Furthermore,
RLNs that branch into anterior and posterior
branches farther away from the larynx are more
likely to be associated with RLN palsy.6,7 Therefore,
recognizing and protecting the extralaryngeal
branches of the RLN is important in preserving
the motor function of the RLN; inadvertent transection, compression, and traction of a branch
can lead to postoperative palsy, despite the surgeon assuming that the RLN was preserved.
The function of each extralaryngeal branch of
the RLN has yet to be well described. Most prior
studies describing the anatomy of the anterior
SURGERY 1

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and posterior branches of the RLN were cadaver


dissections or surgical series with only intraoperative visual evaluation of the nerve.6-10 With intraoperative nerve monitoring (IONM) gaining
more widespread acceptance as an adjunct to visual identification of the RLN, IONM allows the
determination of neural function and the location of the motor branches of the RLN.11-15 Using
IONM, Serpell et al12 and Kandil et al13 reported
the presence of motor fibers in the anterior
branch but not in the posterior branch of
the RLN.
We have used IONM in our clinics since January
2010 and have observed in some patients both
positive evoked electromyography (EMG) waveforms and audio tones when stimulating the posterior branch of the RLN. Consequently, our
hypothesis is that the posterior branch of the
RLN may contain motor fibers. Thus, the goal of
the present study was to evaluate the incidence and
motor function in vivo of the extralaryngeal
branches of the RLN.
PATIENTS AND METHODS
We investigated prospectively 335 consecutive
patients (279 female, 56 male) undergoing thyroid
or parathyroid operations with IONM. Two surgeons (MU, AI) specializing in endocrine surgery
performed the operations. All operations were
conducted between January 2012 and September
2014 involving 593 RLNs deemed at-risk. The
study was approved by the Institutional Review
Board of Sisli Etfal Training and Research Hospital
and ClinicalTrials.gov (ID: NCT02493881). All procedures performed in studies involving human
participants were in accordance with the ethical
standards and with the 1964 Helsinki Declaration
and its later amendments or comparable ethical
standards. Written, informed consent was obtained
from all of the patients.
Exclusion criteria included the preoperative
presence of an RLN palsy, intentional transection
of the RLN because of cancer invasion, failure to
assess RLN functioning due to equipment issues
with the IONM setup, and any parathyroidectomy
operations where the RLNs were not fully dissected
(eg, unilateral focused parathyroidectomy).
Each operational side of the neck was considered a separate entity. One side of each of the 10
patients who underwent bilateral neck exploration (4 right, 6 left) was excluded from the study.
Nine patients who underwent a parathyroidectomy were excluded, because the RLN was not
dissected fully. One patient was excluded due to

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preoperative vocal cord paralysis secondary to a


transected RLN during a previous operation. The
583 remaining, fully dissected RLNs (303 right,
280 left) were included in this study.
IONM technique. We used the NIM 3.0 Nerve
Monitoring System (Medtronic Xomed, Jacksonville, FL), which included a surface electrode on
the endotracheal tube, to test the adductor muscle function of the RLN intraoperatively. Each
patient was administered general anesthesia with
a low-dose, short-acting neuromuscular blockade
and rocuronium (0.3 mg/kg). Patients were
intubated with a Medtronic Xomed Nerve Integrity Monitor Standard Reinforced EMG Endotracheal Tube (size 6.0, 7.0, or 8.0). After neck
extension with a thyroid pillow and patient
positioning, the tube was secured with tape. A
sterile, single-use, pulse-generated monopolar
stimulator probe (Medtronic Xomed) was used
for nerve stimulation in the operative field. The
IONM setup, applications, and data interpretation were in compliance with International Neural Monitoring Guidelines.3,11 Stimuli were
generated from a monitor and set to 1.0 mA for
nerve stimulation. Stimulation duration was set
to a 100 ms current with a frequency of 4 Hz
and an event threshold of 100 mV. Standard
IONM was performed as a 4-step procedure
(V1, R1, R2, V2). The EMG waveform amplitude
defined motor function of the adductor muscles
of the vocal cords.
The method of laryngeal palpation has been
used to evaluate abductor function of the vocal
cords via contraction of the posterior cricoarytenoid muscle (PCA) during routine stimulation of
the vagus nerve or the RLN since January 2013. By
inserting a finger deep into the posterior lamina of
the cricoid cartilage between the posterior lamina
and the fascia overlaying the vertebral column and
palpating the posterior lamina of the cricoid
through the wall of the hypopharynx, a palpable
response, referred to as a laryngeal twitch, could
be appreciated, indicative of contraction of the
PCA16 (Fig 1, A and B).
Operative technique. The anterior approach
was used while performing primary thyroidectomy
and/or central neck dissection and bilateral parathyroid exploration. The back door lateral
approach was used for unilateral parathyroid
exploration, revision thyroidectomy, and/or central
neck dissection. The RLN was identified near the
inferior thyroid artery. The thyroid gland was
dissected meticulously from the anterior and medial
surface of the RLN up to the entry point of the
nerve, into the larynx under the cricopharyngeus

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Uludag, Aygun, and Isgor 3

Fig 1. (A) Method for laryngeal palpation. Evaluation of the laryngeal twitch by inserting the soft tissue pad of the volar
side of the index finger deep into the posterior lamina of the cricoid cartilage. (B) The posterior view of the posterior
cricoarytenoid muscle (PCA) in the laryngeal palpation method. CC, Cricoid cartilage; CPM, cricopharyngeal muscle;
CTM, cricothyroid muscle; ES, esophagus; IAM, interarytenoid muscle; ICM, inferior pharyngeal constrictor muscle;
ITA, inferior thyroid artery; RLN, recurrent laryngeal nerve; TC, thyroid cartilage.

muscle. If the RLN bifurcated before crossing the


inferior thyroid artery, the nerve was dissected
proximally to its branching point.
The distance between the point of bifurcation
of the RLN and the entry point of the branches
into the larynx was measured in millimeters with a
digital vernier caliper, with a resolution of 0.1 mm;
this distance was defined as the branching distance. Additionally, the diameter of both the RLN
and its branches were measured and recorded.
Only RLNs with branches both entering the larynx
at a distance of 5 mm or greater were considered
branched nerves. Some RLNs had 2 branches
arising from the main trunk that then also
branched before entering the larynx. The RLNs
were defined as bifurcating RLNs, and their secondary branches are detailed below.
The main trunk and each branch were stimulated and evaluated separately by both an EMGevoked waveform (Fig 2, A and B) for adduction
and finger palpation for abduction. When RLN
branches ran close together (within a distance of
less than 2 mm), or there were small- to mediumsized arterial branches crossing the RLN, a false
EMG signal could be induced via a shunt stimulus. The stimulation level was decreased to
0.5 mA in that situation, as is suggested in the
literature.5,11
Patients underwent routine pre- and postoperative (within 2 days) direct laryngoscopy, conducted by an independent laryngologist. RLN palsy was
determined to be permanent when there was no
evidence of recovery within 6 months
postoperatively.

Demographic, anatomic, and IONM data were


documented at the end of each operation and
entered into a prospective database. The RLNs
that branched were divided into 2 groups; Group 1
consisted of nerves having motor function in the
anterior branch alone, whereas Group 2 consisted
of nerves having motor function from both the
anterior and posterior branches.
Statistical analyses. Differences between continuous and categorical variables were assessed with a
Mann-Whitney U test and Fisher exact test or v2
test, respectively. Spearman rank correlation was
used for the parameters that were not normally
distributed. Continuous data (distance of branching and nerve diameter) are presented as
mean standard deviation as well as range.
RESULTS
A total of 335 patients (279 women, 56 men)
were assessed. Mean age was 49.4 13.5 years
(range, 1881 years). Indications for operation
were benign thyroid disorders (n = 195: euthyroid = 142; hyperthyroid = 53), thyroid cancer
(n = 52), undetermined or suspicious cytology for
malignancy after fine needle aspiration biopsy
(n = 49), and parathyroid disorders (n = 39: 11
with a concomitant thyroid operation). There
were 244 total thyroidectomies (with central lymph
node dissection in 26, and parathyroidectomy in
11 patients), 14 parathyroidectomies with bilateral
neck exploration, 67 lobectomies (with a parathyroidectomy in 4 patients), and 10 parathyroidectomies with a unilateral approach. RLNs were

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Fig 2. EMG waveforms of stimulation of the RLN. (A) Stimulation of the anterior branch of the RLN. (B) Stimulation of
the posterior branch of the RLN.

evaluated in 87 patients unilaterally and 248 patients bilaterally (Table I).


Anatomy of the branches of the RLN. Two
hundred RLNs (98 right, 102 left; 34.3%) of 583
RLNs (303 right, 280 left) showed extralaryngeal
branching; these 200 branching RLNs were divided
into 2 groups, including 185 in Group 1 with motor
function only in the anterior branch and 15 in
Group 2 with motor function also in the posterior
branch (see below---Motor function of branches of
RLN) (Fig 3, A and B). There was no significant difference between groups in terms of sex (P = .258).
Eleven of 98 (11%) branching nerves on the right
and 4 of 102 (4%) branching nerves on the left
had motor function of the posterior branches
(P = .06). When comparing Group 1 with Group 2,
the distance of branching was greater in
Group 2: 17.3 8.5 mm (range, 550 mm) vs
24.1 13.6 mm (range, 1560 mm) (P < .045)
(Table II). There were no differences in the diameters of the main trunks of the RLN (1.9 0.5 mm vs
2.0 0.5 mm) nor in the diameters of the anterior
branch (1.1 0.3 mm vs 1.2 0.5 mm) or the
posterior branch (1.0 1.9 mm vs 0.9 0.4 mm)
(Table II). The 200 branched RLNs consisted of
189 bifurcated, 10 trifurcated, and 1 4-branched
nerves (Fig 3, A and B).
Motor function of the branches of the RLN.
The motor functions of the branches are displayed

in Fig 3, A and B. Adductor muscle function was


present when stimulating the anterior branches
in all nerves in both Groups 1 and 2 (200,
100%), but was only present in the posterior
branches of Group 2 (15 of 200, 8%). Additionally,
adductor muscle function was detected in some of
the secondary branches of the RLNs. Adductor
function was detected in the medial branch of 1
nerve and both the anterior and medial branches
of another nerve due to secondary bifurcation of
their anterior branches in Group 1. One nerve
had adductor motor function in the anterior and
medial branches of the secondary bifurcated posterior branch in Group 2. The mean EMG amplitudes that define adductor muscle function
obtained during anterior branch stimulation were
greater than the amplitudes for posterior branches
in Group 2 (909 686 mV [range, 3042474 mV] vs
453 286 mV [range, 119981 mV]; P = .026).
The abductor muscle function of the RLNs that
bifurcated close to the entry point of the larynx
and have branches running closely to each other,
could not be evaluated. Abductor muscle function
was evaluated for only 95 of 185 RLNs from Group
1 and 10 of 15 RLNs from Group 2. Abductor
muscle function was present in only the anterior
branches of all the tested 95 RLNs from Group 1.
In Group 2, abductor muscle function was found
in only the anterior branch in 3, only the posterior

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Table I. The branching properties of 583 nerves of


335 patients on the right and left sides
Bilateral exploration
Right branching + left nonbranching
Left branching + right nonbranching
Bilaterally branching
Bilaterally nonbranching
Unilateral exploration
Right side
Branching
Nonbranching
Left side
Branching
Nonbranching
Total

40
50
39
119

19
36
13
19
335

Table II. Anatomic properties of RLN


Parameter*
Diameter
Main RLN
Anterior branch
Posterior branch
Branching distance

Group 1
(n = 185)
1.9
1.1
1.0
17.3

0.5
0.3
1.9
8.5

Group 2
(n = 15)
2.0
1.2
0.9
24.1

0.5
0.5
0.4
13.6

P value
.553
.450
.99
.045

*Data presented as mean (SD) mm.

branch in 4, and in both the anterior and posterior


branches in 3 of 10 RLNs. Abductor muscle
function was present in the anterior branch in
101 (96%) and in the posterior branch in 7 (7%)
of 105 RLNs tested.
Postoperative RLN palsy. The rate of temporary
RLN palsy was 5.5% (n = 32) of 583 RLNs at risk,
whereas permanent RLN palsy was detected in 5
of 583 RLNs at risk or (0.9%) patients. When
comparing branched and nonbranched nerves,
there were no statistical differences for temporary
RLN palsies (6% vs 5%) or for permanent RLN
palsies (1% vs 1%).
DISCUSSION
Branching of the RLN prior to entry into the
larynx is one of the most common anatomic
variations of the RLN. RLN branching in surgical
studies has been reported widely in the literature
as 18.5%72%.6,7,12-15,17-22 The overall RLN bifurcation rate of 34.3% in the present study by overdefinition (branching distances >5 mm) is similar to
what
has
been
observed
in
previous
reports.14,15,19,23
Previous studies have observed a distance of
619 mm as the mean branching distance.12-14,23
We found the mean branching distances of the

RLN to be 17.9 9.0 mm (range, 560 mm).


Our results (with the distance being close to the
upper mean range observed in the literature)
may be related to our routine use of the thyroid
pillow in order to extend the neck, which could
cause nerve stretching. Nevertheless, our results
seem more compatible with the clinical approaches, because most thyroid operations are performed through a neck extention. Several factors
could contribute to differences in branching distances, however, including variable study samples,
racial disparity, sex, and body habitus.13,14,23
The adductor muscles of the vocal cords (thyroarytenoid, interarytenoid, lateral cricoarytenoid)
and the abductor muscle of the vocal cord (PCA)
are supplied by the RLN.24 Data regarding motor
function of the RLN are not as clear as the
anatomic course of the RLN. Some authors suggest
that both the anterior and posterior branches
contain a blend of sensory and motor fibers,8 while
others argue that the anterior branch contains
only motor fibers and the posterior branch consists
of only sensory fibers.9,25,26 In contrast, others suggest that adductor fibers are located in the anterior
branch and abductor fibers in the posterior
branch.27,28 Up until now, this latter suggestion
has been the most accepted theory.11,24
The use of IONM provided an opportunity for
evaluating RLN and the function of its branches
in vivo. Previous studies have provided limited
information on this subject. Serpell et al12 reported that motor fibers of both the adductor
and abductor muscles were located in the anterior
branch and detected no sign of motor fibers in any
of the posterior branches. Kandil et al13 detected
the presence of motor fibers only in the anterior
branches and not in the posterior branches. The
last 3 studies from the literature describe motor fibers to the vocal cords in all anterior branches and
in 1.1%11.5% of posterior branches.14,15,29 Barcyzynski et al29 detected motor activity in 8 (1.3%)
posterior branches from 613 branched RLNs,
and revealed only abductor function in 4 and
both abductor and adductor function in 4.
Adductor muscle function was determined in
the anterior branches of all 200 branched RLNs in
our study, similar to the literature.12-15 In contrast,
we also detected adductor function in the posterior branches of 15 RLNs (8%). Furthermore,
adductor function was observed in the medial
branch of 1 RLN and both the anterior and medial
branches of 2 RLNs, which had more than 2
branches as a result of secondary branching (Fig
3, A and B). Abductor muscle function was found
in the anterior branch in 101 (96%) and in the

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Fig 3. Schematization of the branching pattern and motor function of branches of the recurrent laryngeal nerve
(RLN). (A) Group 1; (B) Group 2. M, main trunk; CPM, Cricopharyngeal muscle; CTM, cricothyroid muscle; A, anterior
branch; P, posterior branch; Am, anteromedial branch of the anterior branch after secondary branching; Aa, anterior
branching of the anterior branch after secondary branching; Pm, posteromedial branch of the posterior branch after
secondary branching; Pp, posterior branching of the posterior branch after secondary branching.

posterior branch in 7 (7%) of 105 RLNs tested.


The functional results of our study support the
complex and variable branching pattern observed
between different branches of the RLN, as have
been reported in recent anatomic studies.30-32 Maranillo et al30 did not find any RLN abductor or
adductor division in their autopsy study. They
observed that adductor muscles also received
branches from other laryngeal nerves, except the
anterior branch of the RLN. Maranillo et al31

also revealed that PCA muscles were supplied by


the anterior branch of the RLN; additionally, 4%
of the PCA muscles received a branch from the
ramus anastomoticus, deriving from the posterior
branch of the RLN. Communication has also
been observed between the muscular branches of
the larynx (under the deep surface of the PCA)
in approximately 65% of the cases,31 and the thyroarytenoid muscle is innervated by a complex nerve
plexus.32

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Despite the low number of cases evaluable in


the present study, the mean branching distance for
RLNs with motor function both in the anterior
and posterior branches tended to be greater than
for nerves with motor functioning only in the
anterior branches (24.1 13.6 mm vs
17.3 8.5 mm, P # .045). Although the probability
of detecting motor functioning in the posterior
RLN branch appears to be greater among early
branching RLNs, we also found similar branching
diameters of the RLNs with motor function in
only the anterior branch. Thus, it is not accurate
to presume motor function among branches based
only on anatomic information. During the operation, the probability of branching of the RLN
must be considered if there is a nerve with a #1mm diameter.
The presence of motor function in the posterior
branch of RLN is important clinically. Any true
extralaryngeal RLN branches not recognized during an operation are in theory at risk for injury.
Visual identification of the RLN has been the gold
standard for RLN preservation. During a thyroidectomy and some parathyroidectomies with wide
exploration, all extralaryngeal branches of the
RLN should be identified in order to preserve
laryngeal motor function. Limited exploration
may be sufficient for the majority of parathyroidectomies; thus a full dissection of the RLN and its
branches may increase injury risk. If the anterior
branch of the RLN is misidentified as a single
trunk nerve, the posterior branch with its motor
function may be divided unintentionally, leading
to an unexpected, postoperative vocal cord
dysfunction. Therefore, any nervelike structure
confronted during the operative dissection should
be considered an extralaryngeal branch.
If IONM is being used during a thyroid operation, motor function of all identified branches
should be evaluated. The distance for the risk of an
electrical shunt to adjacent tissues is <1 mm, when
using 1-mA intensity; thus, motor function may be
misinterpreted due to the proximity between
branching nerves. This situation may cause a
change in the operative strategy due to the potential for false positives, which could lead to loss of
vocal cord function on the surgical side.
Even though all RLN branches are identified,
the second branch (with motor functioning) may
be evaluated as sensorial after identifying the first
motor branch. Any injury to this second branch
may cause unexpected substantial vocal cord
dysfunction, which may explain prior false negative results observed previously with IONM. Thus,
adequate EMG responses could be obtained

intraoperatively with postoperative vocal cord paralysis noted postoperatively. When evaluating the
function of the individual branches of the RLN,
the stimulator probe must be in direct contact with
the branch, and other branches should not be
close to each other, which will help minimize false
negatives and false positives. Laryngeal palpation
can evaluate PCA abductor function and should be
applied to the branching nerves as a complementary method to IONM.
In our study, the amplitudes of the anterior
branch wave were greater than those of the posterior branches, which was similar to other
studies.14,15 Although the anterior branch contains
substantially more motor fibers, the number of fibers in the branches may differ individually. The
clinical findings of suggesting injury to the anterior or posterior branch may be unpredictable
and variable. These findings may vary due to the
number of motor fibers of the injured branch
regardless of its being an anterior or posterior
branch.
In conclusion, extralaryngeal branching is
observed in approximately one third of RLNs.
The anterior RLN branch always has motor function; the posterior branch may also have adductor
and/or abductor motor function in 7%8% of
such branches. Although the probability of detecting motor function in the posterior branch appears to be greater for early branching RLNs, it is
not accurate enough to predict laryngeal branch
functioning based solely on branching distance.
All posterior branches of the RLN should be
preserved and may be a potential risk factor for
postoperative vocal cord dysfunction.
REFERENCES
1. Jeannon JP, Orabi AA, Bruch GA, Abdalsalam HA, Simo R.
Diagnosis of recurrent laryngeal nerve palsy after thyroidectomy: a systematic review. Int J Clin Pract 2009;63:624-9.
2. Hermann M, Alk G, Roka R, Glaser K, Freissmuth M. Laryngeal recurrent nerve injury in surgery for benign thyroid
diseases: effect of nerve dissection and impact of individual
surgeon in more than 27,000 nerves at risk. Ann Surg 2002;
235:261-8.
3. Chiang FY, Lu IC, Kuo WR, Lee KW, Chang NC, Wu CW.
The mechanism of recurrent laryngeal nerve injury during
thyroid surgery---the application of intraoperative neuromonitoring. Surgery 2008;143:743-9.
4. Snyder SK, Lairmore TC, Hendricks JC, Roberts JW. Elucidating mechanisms of recurrent laryngeal nerve injury during thyroidectomy and parathyroidectomy. J Am Coll Surg
2008;206:123-30.
5. Chiang FY, Lu IC, Chen HC, Chen HY, Tsai CJ, Hsiao PJ,
et al. Anatomical variations of recurrent laryngeal nerve
during thyroid surgery: how to identify and handle the variations with intraoperative neuromonitoring. Kaohsiung J
Med Sci 2010;26:575-83.

ARTICLE IN PRESS
8 Uludag, Aygun, and Isgor

6. Casella C, Pata G, Nascimbeni R, Mittempergher F,


Salerni B. Does extralaryngeal branching have an impact
on the rate of postoperative transient or permanent
recurrent laryngeal nerve palsy? World J Surg 2009;33:
261-5.
7. Sancho JJ, Pascual-Damieta M, Pereira JA, Carrera MJ,
Fontan
e J, Sitges-Serra A. Risk factors for transient
vocal cord palsy after thyroidectomy. Br J Surg 2008;
95:961-7.
8. Sunderland S, Swaney WE. The intraneural topography of
the recurrent laryngeal nerve in man. Anat Rec 1952;114:
411-6.
9. Schweizer V, Dorfl J. The anatomy of the inferior laryngeal
nerve. Clin Otolaryngol Allied Sci 1997;22:362-9.
10. Rustad WH. Revised anatomy of the recurrent laryngeal
nerves: surgical importance, based on the dissection of
100 cadavers. J Clin Endocrinol Metab 1954;14:87-95.
11. Randolph GW, Dralle H, International Intraoperative Monitoring Study Group, Abdullah H, Barczynski M,
Bellantone R, Brauckhoff M, et al. Electrophysiologic recurrent laryngeal nerve monitoring during thyroid and parathyroid surgery: international standards guideline
statement. Laryngoscope 2011;121:S1-16.
12. Serpell JW, Yeung MJ, Grodski S. The motor fibers of the
recurrent laryngeal nerve are located in the anterior extralaryngeal branch. Ann Surg 2009;249:648-52.
13. Kandil E, Abdelghani S, Friedlander P, Alrasheedi S,
Tufano RP, Bellows CF, et al. Motor and sensory branching
of the recurrent laryngeal nerve in thyroid surgery. Surgery
2011;150:1222-7.
14. Fontenot TE, Randolph GW, Friedlander PL, Masoodi H,
Yola IM, Kandil E. Gender, race, and electrophysiologic
characteristics of the branched recurrent laryngeal nerve.
Laryngoscope 2014;124:2433-7.
15. Gurleyik E. Location of motor fibers within branches of the
recurrent laryngeal nerve with extralaryngeal terminal
bifurcation: functional identification by intraoperative neuromonitoring. Surgery 2015;158:1339-44.
16. Randolph GW, Kobler JB, Wilkins J. Recurrent laryngeal
nerve identification and assessment during thyroid surgery:
laryngeal palpation. World J Surg 2004;28:755-60.
17. Ardito G, Revelli L, DAlatri L, Lerro V, Guidi ML, Ardito F.
Revisited anatomy of the recurrent laryngeal nerves. Am J
Surg 2004;187:249-53.
18. Cernea CR, Hojaij FC, De Carlucci D Jr, Gotoda R,
Plopper C, Vanderlei F, et al. Recurrent laryngeal nerve: a
plexus rather than a nerve? Arch Otolaryngol Head Neck
Surg 2009;135:1098-102.

Surgery
j 2016

19. Beneragama T, Serpell JW. Extralaryngeal bifurcation of the


recurrent laryngeal nerve: a common variation. ANZ J Surg
2006;76:928-31.
20. Makay O, Icoz G, Yilmaz M, Akyildiz M, Yetkin E. The recurrent laryngeal nerve and the inferior thyroid artery
anatomical variations during surgery. Langenbecks Arch
Surg 2008;393:681-5.
21. Katz AD. Extralaryngeal division of the recurrent laryngeal
nerve: report on 400 patients and the 721 nerves measured.
Am J Surg 1986;152:407-10.
22. Yalcin B, Tu
gcu H, Cant
urk N, Ozan H. Laryngeal branching pattern of the inferior laryngeal nerve, before entering
the larynx. Surg Radiol Anat 2006;28:339-42.
23. Kandil E, Abdel Khalek M, Aslam R, Friedlander P,
Bellows CF, Slakey D. Recurrent laryngeal nerve: significance of the anterior extralaryngeal branch. Surgery 2011;
149:820-4.
24. Randolph GW. Surgical anatomy and monitoring of the
recurrent laryngeal nerve. In: Randolph GW, editor. Surgery of the thyroid and parathyroid glands. 2nd ed. Philadelphia: Elsevier Saunders; 2013. p. 306-30.
25. Williams AF. The recurrent laryngeal nerve and the thyroid
gland. J Laryngol Otol 1954;68:719-25.
26. Pichler H, Gisel A. The clinical significance of the ramification of the recurrent laryngeal nerves; a critical anatomical
study. Laryngoscope 1957;67:105-17.
27. King BT, Gregg RL. An anatomical reason for the various
behaviors of paralyzed vocal cords. Ann Otol Rhinol Laryngol 1948;57:925-44.
28. Rustad WH, Morrison IF. Revised anatomy of the recurrent
laryngeal nerves. Surgical importance based on the dissection of 100 cadavers: a preliminary report. Laryngoscope
1952;62:237-49.
29. Barczy
nski M, Stopa M, Konturek A, Nowak W. The overwhelming majority but not all motor fibers of the bifid
recurrent laryngeal nerve are located in the anterior extralaryngeal branch. World J Surg 2016;40:629-35.
30. Maranillo E, Leon X, Orus C, Quer M, Sanudo JR. Variability in nerve patterns of the adductor muscle group supplied by the recurrent laryngeal nerve. Laryngoscope 2005;
115:358-62.
31. Maranillo E, Le
on X, Iba~
nez M, Or
us C, Quer M,
Sa~
nudo JR. Variability of the nerve supply patterns of the
human posterior cricoarytenoid muscle. Laryngoscope
2003;113:602-6.
32. Sanders I, Wu BL, Mu L, Li Y, Biller HF. The innervation of
the human larynx. Arch Otolaryngol Head Neck Surg 1993;
119:934-9.

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