SURGICAL ANATOMY OF THE EXTERNAL BRANCH OF THE SUPERIOR LARYNGEAL NERVE Claudio R. Cernea, MD, Albert0 R. Ferraz, MD, Sunao Nishio, MD, August0 Dutra, Jr, MD, Flavio C. Hojaij, MD, and Luiz R. Medina dos Santos, MD

Iatrogenic lesions of the external branch of the superior laryngeal nerve (EBSLN) during thyroidectomies are not infrequent due to the possibility of anatomic variations of the relationships of this nerve with the superior thyroid vessels. Therefore, based on an anatomic analysis of 30 superior thyroid poles from 15 fresh cadavers, a new classification of the EBSLN was proposed, considering the jeopardy during a thyroidectomy. Thirtyseven percent of the nerves were type 2, ie, crossing the superior thyroid pedicle less than 1 cm above the superior thyroid pole. It is notable that 20% were type 2b, ie, crossing the vessels below the upper border of the pole, having been considered “high risk.” This incidence was comparable with other series, which found dangerous anatomic variations of the EBSLN in the range of 15% to 68%, confirming that a significant proportion of these nerves might be at risk during surgery on the superior thyroid pole. @ 1992 John Wiley & Sons, Inc. HEAD & NECK 1992;14:380-383

Many publications have already appeared in the international literature dealing with the surgical anatomy of the inferior laryngeal nerve, due to its obvious importance in surgery of the thy-

From the Department of Head and Neck Surgery of the University of Sao Paula Medical School. Sao Paula, Brazil. Presented as part of a Candidate Thesis (CRC) to the Faculty of the University of Sao Paulo Medical School, in June, 1991 Acknowledgement: We are grateful to Mrs. Beatriz V. Barboza and Mr. Luiz C. Modesto for the :omputer work done on this paper Address reprint requests to Dr. Cernea. Al. Joaquim Eugenio de Lima, 1094-CEP 01403-Sao Paulo, Brazil. Accepted for pubiication February 19, 1992

CCC 0148-6403/92/050380-04 $04.00 0 1992 John Wiley & Sons, Inc.

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roid gland.’-’ Few papers, however, have analyzed the surgical anatomy of the superior laryngeal nerve relative to thyroid surgery. Although some authorsg-13 have pointed out the risk of iatrogenic superior laryngeal nerve injury, few14-23 have quantified that risk. We have performed an anatomic study of the relation of the lowest portion of the external branch of the superior laryngeal nerve (EBSLN) to the superior thyroid vessels. Based on our findings, we have created a classification of the different types of nerves, in an attempt to identify those at risk during surgery. MATERIALS AND METHODS

The fresh cadavers of 9 men and 6 women, ranging in age from 38 to 74 years, were used in this study, with a total of 30 superior thyroid poles being dissected. Access to the central compartment of the neck was gained through a wide cervico-thoracic curved flap, which was elevated in a subplatisma1 plane up to the hyoid bone. Although the incision differed from the one used for a standard thyroidectomy, it enabled us to locate all the external marks on nonvisible areas in a dressed body. The strap muscles were sectioned, and both thyroid lobes were exposed. Both recurrent nerves were also identified. The sternothyroid-laryngeal trianglelg was carefully dissected for identification of the EBSLN and its relation to the superior thyroid vessels. When the nerve

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NOT tWWfF.

1

TYPE

TYPE I b

FIGURE 1. Classification of the EBSLN, according to the potential risk of iatrogenic lesion during a hypothetical thyroidectomy. Type 1: the nerve crosses the superior thyroid vessels 1 or more centimeters above a horizontal plane passing the upper border of the superior thyroid pole. Type 2a: nerve crossing the vessels less than 1 cm above the plane. Type 2b: nerve crossing the vessels below the plane

could not be found, the whole lateral aspect of the neck, from the base of the skull to the supraclavicular fossa, was explored. A potential surgical risk criterion was used to propose the classification of the different types of EBSLN, as follows (Figure 1):

Nerve not identified. Type 1- Nerve crossing the superior thyroid vessels 1 or more cm above a horizontal plane passing the upper border of the superior thyroid pole (Figure 2). Type %Nerve crossing the vessels less than 1 cm above or below that horizontal plane. Type 2a-Nerve less than 1 cm above the plane (Figure 3). Type 2b-Nerve below the plane (Figure 4). RESULTS

The results are summarized in Table 1. It is noteworthy that, among the 18 type 1 nerves, 5 (28%) had a course within the fibers of the inferior pharyngeal constrictor muscle. Only 7 (47%) of the cadavers were found to have both EBSLN of the same type. A comparison with other series of the literature is shown in Table 2. Regarding the recurrent nerve, there were 5 (17%) instances of extra-laryngeal bifurcations and 1 (3%)of trifurcation. No relations could be

established between these and the EBSLN variations. An extra-laryngeal anastomosis between the recurrent nerve and the EBSLN was observed in only one (3%)dissection. Of the 15 cadavers used, 4 (28%) were found to have small goiters: 2 (14%) were multinodular, 1 (7%) diffuse, and 1 (7%) uninodular. DISCUSSION

Most of the literature about nerve lesions following thyroidectomy focuses on paralysis of the recurrent laryngeal nerve. Nervertheless, a few authors have pointed out that another nerve, the EBSLN, might be in serious jeopardy during the dissection and ligation of the superior thyroid l3 pedi~1e.~In 1968, Moosman and De Weeselg defined the anatomical limits of the sternothyroid-laryngeal triangle, where the EBSLN usually runs. Nevertheless, they observed an aberrant course in 21% of the 400 dissections they performed. The anatomic classification of the EBSLN proposed here, which has a clear surgical importance, has demonstrated that the type 2 nerves, totaling 37%) might, at least in theory, present

Table 2. Percentage of high-risk EBSLN ~~

No of dissections

%

Clader’ Durham” Moosrnan’g EspinozaZ3 LennquistZ2

96 100 400 30 50

68 25 21 15 18

Present study

30

20

Ref

Table 1. Results. Type of Nerve

Number (%)

Not identified Type 1 Type 2a Type 2b

1(3%) 18 (60%) 5 (17%) 6 (20%)

~-

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FIGURE 2. Dissection showing a Type 1 EBSLN (arrow) crossing the superior thyroid pedicle more than 1 cm above the upper border of the superior thyroid pole.

an increased risk of iatrogenic lesion during a thyroidectomy. It is notable that 20% of these nerves were type 2b, ie, were situated below the upper border of the superior thyroid pole. In this situation, there is extreme danger of a nerve lesion during the ligation of the superior thyroid pedicle, especially if performed by a inexperienced surgeon. If we compare this “high-risk nerve” frequency with other publications (Table 21, it becomes clear that, despite the different criterion adopted, the potential risk of lesion oscillates between 15% and 65%, being, therefore, far from negligible. This wide variation is probably due to the lack of a universally accepted classification, such as the one proposed in this paper. Among such studies, that published by Espinoza et al,23 showing a 15% incidence, is probably the one that better reflects reality, because the authors tried to reproduce the steps of a thyroidectomy with great accuracy. An interesting findingOf this study was the asymmetry among the characteristics Of the two EBSLN, which was seen in 53% of the cadavers. This fact demonstrates that, during bilateral

FIGURE 3. Type 2a EBSLN (arrow), located very close to the upper border of the superior thyroid Pole.

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Superior Laryngeal Nerve in Thyroid Surgery

FIGURE 4. Type 2b EBSLN (large arrow), closely attached to the anterior branch of the superior thyroid artery. In this particular dissection. the internal branch of the suoerior larvnaeal nerve (small arrow) was also located lower than ‘usual.

.”

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thyroidectomies, the risk of nerve injury is usually different for each side. The presence of an abnormal thyroid gland, observed in 28% of the individuals, did not interfere significantly with the position of the nerve in relation to the superior thyroid pedicle, although no huge goiter has been found. Vernetti" advocated that the elevation of the superior thyroid pole due to nodular diseases might alter the position of the superior thyroid vessels, joining them t o the nerve. Menasche et alZ1 found the EBSLN closely related to the gland in six dissections, three of which were in individuals with goiters. Interestingly enough, 28% of type 1 nerves were located within the fibers of the inferior pharyngeal constrictor muscle, being thus well protected against an iatrogenic lesion during the dissection of the superior thyroid pole. In conclusion, there is a significant incidence of EBSLN with aberrant courses, carrying an increased risk of iatrogenic lesion during operations on the superior pole of the thyroid gland. Therefore, we emphasize the need for careful dissection and, when an anatomical variation is present, the surgeon should be aware of the possibility of injury, mainly in the type 2b nerves. In addition, we suggest a new classification of the EBSLN, aiming to establish a uniform comparison among the different series.

REFERENCES

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Superior Laryngeal Nerve in Thyroid Surgery

laryngeal nerves and their association with a recurrent branch. A m J Surg 1983;146:501-503. 6. Friedman M, Toriumi DM, Grybauskas V, Katz A. Nonrecurrent laryngeal nerves and their significance. Laryngoscope 1986;96:87-90. 7. Katz A. Extralaryngeal division of the recurrent laryngeal nerve. Am J Surg 1986;152:407-409. 8. Henry JF, Audifret J, Denizot A, Paln M. The non recurrent inferior laryngeal nerve: review of 33 cases, including two on the left side. Surgery 1988;104:977-984. 9. Roeder CA. Operations on the superior pole of the thyroid. Arch Surg 1931;41:448-459. 10. Ferraz AR, Toledo AC. Aspectos tbcnicos no tratamento do b6cio nodular Re Hosp Clin Fac Med S Paul0 1979;34:88-92. 11. Carosi V, Stancanelli V, Balanzoni S. L'isolamento (di routine) dei nervi laringei nella chirurgia della tireoide. Minerua Med 1980;71:1661- 1664.. 12. Kark AE, Kissin MW, Auerbach R, Meikle M. Voice changes after thyroidectomy: role of the external laryngeal nerve. Br Med J 1984;289:1412-1415. 13. Jansson S, Tisell LE, Hagne I, Sanner E, Stenborg R, Svensson P. Partial laryngeal nerve lesions before and after thyroid surgery. World J Surg 1988;12:522-527, 14. Berlin DD, Lahey FH. Dissections of the recurrent and superior laryngeal nerves: the relation of the recurrent to the inferior thyroid artery and the relation of the superior to abductor paralysis. Surg Gynecol Obstet 1929;49:102- 104. 15. Nordland M. The larynx as related to surgery of the thyroid based on an anatomical study. Surg Gynecol Obstet 1930;51:449-459. 16. Vernetti L. Studio anatomo-chirurgico sui rapporti della branca esterna del nervo laringeo superiore con il pedunculo vascolare superiore della tireoide. Minerua Chir 1947;2:427-432. 17. Clader DN, Luter PW, Daniels BT. A photographic study of the superior and inferior laryngeal nerves and superior and inferior thyroid arteries. A m Surg 1957;23:609-618. 18. Durham CF, Harrison TS. The surgical anatomy of the superior laryngeal nerve. Surg Gynecol Obstet 1964; 118:38-44. 19. Moosman DA, DeWeese MS. The external laryngeal nerve as related to thyroidectomy. Surg Gynecol -0gstet 1968:127:1011- 1016. 20. Visset J, LeBorgne J, Barbin JY. Le nerf larynge externe. Bull Assoc Anat (Nancy) 1975;59:1001- 1012. 21. Menasche P, Mamoudy P, Blondeau, P. Le nerf larynge externe, danger possible de la chirurgie thyreoidienne. Ann Chir 1976;30:121-129. 22. Lennquist S, Cahlin C, Smeds S. The superior laryngeal nerve in thyroid surgery. Surgery 1987;102:999- 1008. 23. Espinoza J, Hamoir M, Dhem A. Preservation of the external branch of the superior laryngeal nerve in thyroid surgery: An anatomic study of 30 dissections. Ann Otolaryngol Chir Ceruicofac 1989;106:127- 134.

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Surgical anatomy of the external branch of the superior laryngeal nerve.

Iatrogenic lesions of the external branch of the superior laryngeal nerve (EBSLN) during thyroidectomies are not infrequent due to the possibility of ...
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