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Superior Laryngeal Nerve Identification and Preservation in Thyroidectomy
Michael Friedman, MD;
Phillip LoSavio, BS;
Hani Ibrahim, MD
Arch Otolaryngol Head Neck Surg. 2002;128:296-303.
ABSTRACT
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Background Injury to the external branch of the superior laryngeal nerve (EBSLN)
can result in detrimental voice changes, the severity of which varies according
to the voice demands of the patient. Variations in its anatomic patterns and
in the rates of identification reported in the literature have discouraged
thyroid surgeons from routine exploration and identification of this nerve.
Inconsistent with the surgical principle of preservation of critical structures
through identification, modern-day thyroidectomy surgeons still avoid the
EBSLN rather than identifying and preserving it.
Objectives To describe the anatomic variations of the EBSLN, particularly at the
junction of the inferior constrictor and cricothyroid muscles; to propose
a systematic approach to identification and preservation of this nerve; and
to define the identification rate of this nerve during thyroidectomy.
Materials and Methods A retrospective review of thyroid lobectomies and total thyroidectomies
performed between 1978 and 1997 was carried out. A total of 884 patients were
included, with 1057 EBSLNs explored. Intraoperative findings of identification
of the EBSLN were recorded and compared on an annual basis for both benign
and malignant disease. Overall results were also compared with those found
in previous series identified through a 50-year literature review.
Results The 3 anatomic variations of the distal aspect of the EBSLN as it enters
the cricothyroid were encountered and are described. The total identification
rate over the 20-year period was 900 (85.1%) of 1057 nerves. Operations performed
for benign disease were associated with higher identification rates (599 [86.1%]
of 696) as opposed to those performed for malignant disease (301 [83.4%] of
361). Operations performed in recent years have a higher identification rate
(over 90%).
Conclusions Understanding the 3 anatomic variations of the distal portion of the
EBSLN and its relation to the inferior constrictor muscle allows for high
rates of identification of this nerve. The EBSLN should be explored during
thyroid surgery and identification is possible in most cases. Preservation
of the EBSLN maintains optimal function of the larynx.
INTRODUCTION
THE CLINICAL significance of the superior laryngeal nerve (SLN) has
been clearly overshadowed by emphasis on the recurrent laryngeal nerve. The
principles of head and neck surgery are based on identification and preservation
as opposed to avoidance of important structures. These principles would set
identification and preservation of the SLN as standard in all thyroid surgery.
The nerve is clearly at risk, and injury is clearly detrimental to the patient.
Despite these facts, the SLN is not routinely identified by most surgeons,
and some physicians have presented studies to justify this apparent inconsistency
in optimal surgery.1-3
Many articles deal with the variable anatomy of the superior laryngeal
nerve.3-11
Most of these articles focus on the anatomic relationship of the SLN to the
superior thyroid artery. They discuss the likelihood of the SLN being at risk
for injury and the probability of identifying the SLN during surgery; they
suggest that the SLN often cannot be identified. Very little has been written
on the anatomy of the distal portion of the SLN as it enters the cricothyroid
muscle.3
This study was undertaken to review the experience of the senior surgeon
(M.F.) with the SLN in more than 1000 thyroid lobectomies over a 20-year period.
The study reviews the anatomy of the distal end of the SLN as it relates to
the practical aspect of surgical identification. It also reviews the percentage
of cases in which the SLN was actually identified. It presents a reliable
technique for practical identification and preservation of the SLN in thyroid
surgery in a high percentage of cases.
MATERIALS AND METHODS
This nonrandomized retrospective study reviews a 20-year experience
of thyroid lobectomies from the year 1978 to 1997. The charts of all patients
who underwent thyroidectomy and/or lobectomy were reviewed to assess if the
external branch of the SLN (EBSLN) was identified and preserved or not identified
at surgery. Cases were categorized into benign or malignant as determined
by pathology reports at the time of surgery, and the percent identification
was compared for each calendar year. Overall, 884 patient cases were reviewed
with a total of 1057 EBSLNs put at risk (696 nerves [65.8%] in cases with
benign tumors and 361 nerves [34.2%] with malignant tumors). A full literature
search was performed on the OVIDWEB-MEDLINE database looking for all relevant
articles since 1950 that comment on the identification, preservation, anatomy,
surgical technique, and injury rate to the EBSLN.
SURGICAL ANATOMY
The SLN is classically described as originating from the middle of the
nodose ganglion. In addition, it receives contributions from the superior
cervical sympathetic ganglion. Its path of descent initially begins posteriorly
and proceeds medially to the internal carotid artery where it bifurcates into
an internal (sensory and autonomic) and external laryngeal branch (motor).12-13 The internal branch proceeds to pierce
the thyrohyoid membrane with the superior laryngeal artery and subsequently
divides into an upper and lower branch. The external branch continues to travel
inferiorly, passing superficially to the inferior constrictor and then piercing
it to finally reach the cricothryoid muscle.12
While this level of description can suffice for the nonsurgical observer,
more detailed descriptions have helped to elucidate the variations in the
anatomy of the EBSLN to aid the surgeon operating in this area.3-11
This study focused on the anatomy of the EBSLN at its insertion into
the cricothyroid muscle. Terminal branches of the EBSLN penetrate the horizontal
and oblique bellies of the cricothyroid muscle as well as the inferior constrictor.
However, 3 variations have been described for the main trunk of the EBSLN
prior to its terminal branching. In the type 1 variation, it runs its whole
course superficially or laterally to the inferior constrictor, descending
with the superior thyroid vessels until it terminates in the cricothyroid
muscle (Figure 1). In the type 2
variation, the EBSLN penetrates the inferior constrictor in the lower portion
of the muscle (Figure 2). In this
case it is only partially protected by the inferior constrictor. And finally,
the type 3 nerve dives under the superiormost fibers of the inferior constrictor,
remaining covered by this muscle throughout its course to the cricothyroid
muscle (Figure 3).
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Figure 1. Type 1 anatomic variant: the external
branch of the superior laryngeal nerve runs superficially to the inferior
constrictor muscle.
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Figure 2. Type 2 anatomic variant: the external
branch of the superior laryngeal nerve dives deep to the inferior constrictor
muscle, approximately 1 cm proximal to the inferior constrictor–cricothyroid
junction.
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Figure 3. Type 3 anatomic variant: the external
branch of the superior laryngeal nerve runs deep to the inferior constrictor
muscle.
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Often the SLN is not easily visible, and some authors consider these
situations ones of "unidentifiable nerves."1-3
These authors believe that if the course of the distal branch runs under the
inferior constrictor muscle (which occurs in 20% of cases3),
the nerve is unidentifiable. In fact, we have found that in most of these
situations the nerve can be identified by nerve stimulation along the border
of the inferior constrictor and the cricothyroid (type 3, Figure 3).
The muscle response of the stimulated nerve is quite different than
the response of direct muscle stimulation. Absence of identification by stimulation
should direct the surgeon back to the region of the vessels to search for
a missed type 1 nerve.
This classification is based on the terminal aspect of the EBSLN and
is provided as a practical guide for identification. It does not replace previously
described classifications by Kierner et al4
and Cernea et al5 that focus on the EBSLN and
the superior thyroid vessels' relationship. The percentage of patients with
anatomy corresponding to 1 of these 3 types has not been studied in detail
by us or by other investigators. Lennquist et al3
studied the percentage of their patients with type 3 distribution and found
it to be 20%. Although the retrospective review of the data was not detailed
enough in that study to identify which type was present in every case, all
3 types were frequently identified.
SURGICAL TECHNIQUE
A previously described systematic approach14
was used consistently in all of our cases. After raising subplatysmal flaps,
care was taken to maintain meticulous hemostasis as the sternohyoid and sternothyroid
muscles were individually elevated laterally (Figure 4 and Figure 5).
The sternohyoid muscle was elevated laterally up to the hyoid to allow visualization
of the sternothyroid muscle insertion into the oblique line of the thyroid
cartilage. The sternothyroid muscle was then elevated laterally until the
lateral edge of the thyroid gland was reached. The medial edge of the superior
attachment of the sternothyroid muscle was transected with a bipolar cautery
for a distance of 5 mm (Figure 6),
which provided better exposure of the inferior constrictor–cricothyroid
junction. The horizontal and oblique bellies of the cricothyroid muscle were
identified as was the anterior edge of the inferior constrictor.
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Figure 5. The sternohyoid muscle is dissected
laterally up to the hyoid bone to allow visualization of the sternothyroid
muscle and its attachment to the oblique line.
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Figure 6. If the inferior constrictor–cricothyroid
junction is not clearly visible by retraction of the sternothyroid, the medial
5-mm attachment of the sternothyroid is transected.
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A disposable nerve stimulator (set on 2 mA) was used to identify the
terminal branches of the EBSLN as they enter the cricothyroid bellies. The
stimulator was first used directly on the cricothyroid muscle to assess the
response of direct muscle stimulation. This helps differentiate muscle stimulation
from nerve stimulation. If the EBSLN was identified over the inferior constrictor
(type 1, Figure 1), it was followed
in a retrograde direction. Identification of the nerve in this location allows
for preservation of the nerve. This anatomic variant is usually associated
with an EBSLN that crosses the superior thyroid artery at or below the superior
thyroid pole. This scenario places the nerve at risk not only during ligation
of the superior thyroid vessels but during dissection of the loose areolar
tissue adjacent to the superior pole. Routinely, the superior pole vessels
and the loose areolar tissue surrounding them are not dissected until the
EBSLN is explored. In some cases, the EBSLN can be identified crossing some
of the inferior constrictor and then diving under the muscle for a variable
distance prior to its insertion in the cricothyroid muscle (type 2, Figure 2). Once this nerve is identified,
no further dissection is usually needed.
The EBSLN is considered at risk in each patient until it is identified.
The nerve is stimulatable in almost all cases at the junction of the cricothyroid
and inferior constrictor muscles. Identification by stimulation assures the
surgeon that the nerve is not at risk.
RESULTS
Table 1 summarizes the results
of our study. The identification and preservation rate in 884 patients over
20 years, with a total of 1057 nerves at risk, was 85.1% (900/1057). The identification
rates were calculated annually from 1978 to 1997. In later years, the use
of stimulation to identify the EBSLN covered by the inferior constrictor helped
increase the identification rate from 75% in 1978 to 90% in 1997.
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Table 1. EBSLN* Identification (ID) and Preservation Rates for Benign
and Malignant Disease
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COMMENT
Identification of the EBSLN has become a standard practice in all thyroid
lobectomies performed by one of us (M.F.). The aforementioned technique of
distal identification at the inferior constrictor–cricothyroid junction
has resulted in an average identification rate of 85.1% over the past 20 years,
with recent years demonstrating a higher than 90% success rate. Although the
absence of patient complaints and abnormal laryngeal examination findings
postoperatively allowed the authors to assume a lower injury rate, no specific
studies were routinely performed to confirm this assumption. The purpose of
the study was not to establish an injury rate but to review the anatomy and
establish the identification rate attainable with routine thyroid surgery.
The importance of avoiding injury to the EBSLN should not be understated
when discussing the sequelae of complications during thyroid surgery. Paralysis
of the SLN can be significant to those whose career depends heavily on full
range of voice. One of the earliest reported cases goes back to 1935 when
famous opera singer Amelita Galli-Curci suffered injury to her EBSLN after
thyroid surgery with devastating consequences.15
Damage to the nerve can manifest as ipsilateral paralysis to the cricothryoid
muscle as demonstrated by electromyography (EMG) and fiberoptic stroboscopic
laryngoscopy.16-17 Clinical symptoms
may present as a hoarse, breathy voice, increased throat clearing, vocal fatigue,
or diminished vocal frequency range, especially in regard to raising pitch.
The clinician may find signs of bowing and inferior displacement of the affected
cord on examination.16 Two anatomic studies
on cadavers6-7 using special staining
to map out nerve distributions and patterns around the larynx have demonstrated
communicating nerves between the EBSLN and the recurrent laryngeal nerve.
They suggest that the EBSLN may contribute significant innervation to other
muscles beyond the cricothyroid adding to the evidence of this nerve's importance.
Identification and injury rates have varied greatly across different
studies, with identification rates ranging from 33% to 93%, while injury rates
have been reported between 0% and 58%1-3,8, 16, 18-21
(Table 2). The variation in results
is partially explained by the nonconcordance of surgical techniques used by
different physicians. In many circumstances, inaccuracy of evaluation techniques
has also most likely resulted in underreported EBSLN injury rates. Jansson
et al18 reported that partial SLN lesions could
not be diagnosed reliably based on indirect laryngoscopy or voice symptoms.
They pointed to EMG as a much more definitive method of making a diagnosis.
Unfortunately, many studies to date have not used EMG when reporting injury
rates.1-3,19-20
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Table 2. Reported EBSLN Identification (ID) and Injury Rates*
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Another important factor to consider is that published injury rates
may not be applicable to the average surgeon in every circumstance. As demonstrated
by Cernea et al,8 training level played a significant
role in correlating with injury rates, with residents recording a 28% injury
rate and the senior author (Claudio R. Cernea, MD) reporting only a 12% rate.
Lore et al2 argue that it is not necessary
to avoid the nerve to avoid injuring it. They point out that many of the existing
studies show similar rates of injury whether the nerve is located or not.
In their own series they report an extremely low injury rate. In spite of
this, it is an accepted surgical principle that identification is the key
to preservation of structures at risk.
Variability in the anatomy of the EBSLN as it relates to the superior
thyroid artery has been studied in detail.3-5,8-11
Cernea et al5 were among the first to describe
a specific classification system (types 1, 2a, or 2b); they found the percentage
of each pattern to vary among patients with either small or large goiters
owing to the alteration in the anatomic arrangement that takes place with
enlargement of the thyroid gland. Kierner et al4
revisited this subject with cadaver studies and refined the nomenclature,
taking into account the cases that Cernea and colleagues5
labeled as "not identified" (Table 3).
Type 2b (which correlates with our described type 1 pattern) is at the highest
risk during surgery, with the categories in which the nerve crosses relatively
high to the upper thyroid pole being at considerably less risk of iatrogenic
injury. This fact, however, should not preclude one from identifying all circumstances
in which the nerve presents itself. Indeed, the rate of 2b variants is significantly
increased in cases of disease caused by superior displacement of the upper
thyroid pole.5 Cernea et al5
reported a difference of 54% vs 14% in cases of large and small goiters, respectively.
When the surgeon ligates the superior pole vessels and has not identified
the EBSLN, it cannot be assumed that it is a high-crossing variant and therefore
not at risk. Negative findings could always prove to be a case of a 2b nerve
that has yet to be successfully located. At the same time, it is unreasonable
for one to expand the surgical field superiorly to unquestionably identify
these other variants higher in the neck. We propose our system that concentrates
not on the superior thyroid vessels, but on the presentation of the nerve
in the inferior constrictor–cricothyroid junction with subsequent retrograde
dissection and preservation.
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Table 3. EBSLN Classification Systems*
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Only the clinical and anatomic studies of this region by Lennquist et
al3 have described in detail the relationship
of the EBSLN with its entry into the cricothyroid muscle. They point to the
fact that in nearly 20% of cases the nerve is buried in the fibers of the
inferior pharyngeal constrictor and thus not identifiable without dissection
of the fibers. They argue that in these cases where the nerve is covered by
constrictor fibers greater than 10 cm proximal to cricothyroid entry, more
harm than good will result from a search for the nerve.3
Our technique, however, does not subject the constrictor fibers to a destructive
reconnaissance mission because we limit our dissection to the junction between
the 2 muscles. Positive identification of the nerve at the junction of the
inferior constrictor and cricothyroid muscles can be accomplished in most
cases with minimal dissection. This increases the overall identification rate.
In conclusion, preservation of the EBSLN is important for optimal function
of the larynx. The nerve is at risk during thyroidectomy, and although injury
rates are not clearly established, they do exist. The principles of head and
neck surgery dictate that the best way to avoid injury to a structure at risk
is by identification and preservation. The EBSLN has not been routinely identified
because of conflicting data on the ability and rate of intraoperative identification.
This study establishes an identification rate of over 85% based on a simple
technique combined with detailed knowledge of the anatomy of the terminal
branches of the EBSLN. Routine identification and preservation is possible
in most thyroidectomy procedures.
AUTHOR INFORMATION
Accepted for publication November 15, 2001.
This study was presented at the annual meeting of the American Head
and Neck Society, Palm Desert, Calif, May 16, 2001.
Corresponding author: Michael Friedman, MD, 30 N Michigan Ave, Suite
1107, Chicago, IL 60612 (e-mail: khender213{at}aol.com).
Reprints:
Michael Friedman, MD, Department of Otolaryngology and Bronchoesophagology,
Rush-Presbyterian-St Luke's Medical Center, 1653 W Congress Pkwy, Chicago,
IL 60612-3833.
From the Department of Otolaryngology and Bronchoesophagology, Rush-Presbyterian-St
Luke's Medical Center (Drs Friedman and Ibrahim and Mr LoSavio), and the Division
of Otolaryngology, Advocate Illinois Masonic Medical Center (Drs Friedman
and Ibrahim), Chicago, Ill.
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