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As Seen From Within Using Sihler's Stain

Antonius C. Kierner, MD; Irmgard Zelenka, MD; Martin Burian, MD

Arch Otolaryngol Head Neck Surg. 2001;127:1230-1232.

ABSTRACT
Objective  To determine how the spinal accessory nerve and the trapezius branches of the cervical plexus contribute to the innervation of each of the 3 parts of the trapezius muscle. Special emphasis was placed on the nerve supply of the clinically most important descending part of the muscle.

Design  Anatomical analysis of the distribution of the cervical plexus and spinal accessory nerve branches in the human trapezius muscle.

Materials  Twenty-two trapezius muscles from 11 perfusion-fixed human cadavers ranging in age from 66 to 92 years (mean, 81.7 years).

Interventions  The specimens were dissected free and macerated, decalcified, and stained according to Sihler's technique for about 6 weeks. The translucent, stained muscles were then backlit, and the findings were documented photographically and by schematic drawings.

Results  In all 22 muscles, the innervation of each of the 3 parts of the trapezius muscle was seen. In all muscles investigated, the nerve supply to the descending part of the muscle consisted of a single fine branch of the spinal accessory nerve, whereas the transverse and ascending parts were innervated by both the spinal accessory nerve and the trapezius branches of the cervical plexus.

Conclusion  Our results, especially those involving the descending part of the trapezius muscle, may help to minimize the rate of unexpected trapezius muscle paresis after surgery of the neck.

INTRODUCTION

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AS SHOWN IN a recent article,¹ there are more questions than answers concerning the innervation of the trapezius muscle. Against the backdrop of a high rate of unexpected trapezius muscle paresis after surgery of the neck, these questions still demand attention.^2-5 For the physician, the descending part of the trapezius muscle gains outstanding interest because it maintains the stability of the shoulder girdle.^6-9 Various sources of innervation to this muscle have been described.^10-16 Apart from the majority of the statements on this question being purely speculative, the data presented are often confusing or even contradictory. Since almost all surgeons try to save the spinal accessory nerve (SAN) during modified radical neck dissection, the high rate of unexpected trapezius muscle paresis remains unclear. Until now, none of the hypotheses published on trapezius muscle innervation could resolve this problem, perhaps partly because almost all investigations dealing with this topic were based on either gross dissection or electromyography, both of which have considerable limitations.^{12, 17} Thus, a final, reliable statement on the innervation of each of the 3 parts of the trapezius muscle could not be made on the basis of the results obtained by using these techniques.

Our aim was to elucidate how the branches of the cervical plexus and the SAN contribute to the innervation of the 3 parts of the trapezius muscle. The simple, reliable technique of Sihler,¹⁸ recently recalled by Wu and Sanders,¹⁹ was used to stain nerve fibers while simultaneously making muscle tissue translucent.

MATERIALS AND METHODS

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Twenty-two trapezius muscles were taken from 11 cadavers of both sexes that ranged in age from 66 to 92 years (mean, 81.7 years) and had been donated to the Institute of Anatomy 2, University of Vienna, Austria. The nerves passing into the muscles, ie, the SAN and trapezius branches of the cervical plexus, were identified and marked with a colored thread before the muscles were dissected free on both sides. The muscles were fixed for at least 6 weeks in 4% paraformaldehyde buffered with 0.1M phosphate buffer to pH 7.4 and then stained according to the modified method of Sihler¹⁸ as described by Wu and Sanders,¹⁹ as follows:

• The fixed specimens were macerated in a solution containing 4 mL of 3% hydrogen peroxide and 2000 mL of 3% potassium hydroxide for approximately 3 weeks.
  
• The macerated specimens were decalcified by immersion in a combination of 250 mL of glacial acetic acid, 250 mL of 100% glycerin, and 1500 mL of 1% aqueous chloral hydrate (solution 1) for 2 to 4 weeks.
  
• The decalcified specimens were then stained by immersion in a combination of 250 mL of Ehrlich's acid hematoxylin, 250 mL of 100% glycerin, and 1500 mL of 1% aqueous chloral hydrate (solution 2) for 2 to 3 weeks.
  
• After staining, the specimens were again transferred to solution 1 for approximately 6 hours.
  
• For neutralization, the specimens were then immersed in 0.05% lithium carbonate for approximately 1 hour.
  
• Finally, the specimens were immersed in increasing concentrations of glycerin daily and preserved in 100% glycerin with a few thymol crystals (day 1, 30%; day 2, 50%; day 3, 60%; day 4, 70%; day 5, 80%; and day 6, 100% plus thymol).
  

RESULTS

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The SAN and the trapezius branches of the cervical plexus merged on the ventral surface of the transverse part of the trapezius muscle, or a little caudal to that, in all 22 specimens (Figure 1 and Figure 2). Thus, the SAN and cervical plexus branches also passed into the same parts of the muscle in all specimens (Figure 2 and Figure 3).

View larger version (33K): [in this window] [in a new window] Figure 1. Schematic illustration of the trapezius muscle innervation. Note the fine branch of the spinal accessory nerve (SAN) (top arrow), which could be found in all 22 specimens investigated. The solid circle (bottom arrow) indicates the approximate point where the SAN and the trapezius branches (dashed lines) of the cervical plexus (rami trapezii) merge, which occurred in all 22 specimens.

View larger version (56K): [in this window] [in a new window] Figure 2. Right trapezius muscle stained according to Sihler's technique. The open arrowhead indicates the spinal accessory nerve (SAN); the solid arrowhead, the branch of the SAN passing into the descending part of the muscle; the long fine arrow, the trapezius branches of the cervical plexus; and the short fine arrows, the cutaneous nerves arising from the posterior divisions of the dorsal nerves (so-called segmental branches) passing through the muscle.

View larger version (30K): [in this window] [in a new window] Figure 3. Enlargement of the descending part of a right trapezius muscle. The arrows indicate the branch of the spinal accessory nerve passing into the descending part of the trapezius muscle.

In all specimens, 1 to 8 (mean, 7.3) dorsal cutaneous branches were found. These segmental branches always passed through the tendinous plane, from which the muscle takes its origin; none of them branched inside the trapezius muscle (Figure 2).

A single fine branch of the SAN passing to the descending part of the trapezius muscle, as recently described in a cross-dissection study,¹ was found in all 22 muscles investigated (Figure 1, Figure 2, and Figure 3). No anastomoses were found between this branch and the nerves passing into the muscle more caudally. No other nerve was detected passing into the descending part of the trapezius muscle (Figure 2).

COMMENT

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As far as we know, this is the first study showing that the SAN and the trapezius branches of the cervical plexus merge and pass together to the transverse as well as to the ascending part of the trapezius muscle (Figure 1 and Figure 2). The descending part of the muscle, however, is innervated solely by a single fine branch of the SAN (Figure 2 and Figure 3). Furthermore, we showed that the so-called segmental branches do not branch within the trapezius muscle and are obviously identical to the cutaneous nerves arising from the posterior divisions of the cervical nerves, which are thought to be purely afferent. Beside the well-known innervation of the trapezius muscle by the SAN and the rami trapezii of the cervical plexus, no other nerve supply could be found. This contrasts with the findings of Soo et al,¹⁵ Krause et al,^{16, 20} and Niemeyer and Ludolph.¹³ Furthermore, we could not detect any branches, other than the one arising from the SAN, passing toward the descending part of the muscle and indicating a dual innervation as stated by Krause et al.²¹ However, a purely cervical innervation of the descending part, as suggested by Haas and Sollberg,⁷ seems even more unusual and has never been proven. On the basis of more recent work by Karuman and Soo²² and our own findings, we strongly disagree with the statement by Weitz et al²³ that the whole trapezius muscle has a dual innervation and the surgical consequences they propose. On the other hand, as early as 1974, Fahrer et al¹¹ pointed out that, based on their clinical experience, a purely cervical supply to the upper part of the trapezius muscle as suggested by Rosenstein²⁴ could not be accepted as a rule, and Fahrer et al could find no evidence that the trapezius muscle can be supplied by cervical fibers only.

It must be stressed that the previous studies mentioned are all based on clinical experience, gross dissection, and/or electromyography, which leaves a shade of doubt on the reliability of their findings.

Since the branch of the SAN passing to the descending part of the trapezius muscle was the only nerve found in this part of the muscle, we believe that it is a mixed nerve. Nonetheless, this important chapter on the innervation of the trapezius muscle still cannot be closed.

In conclusion, although our findings regarding the innervation of the descending part of the trapezius muscle have yet to be proven in clinical practice, we are convinced that they can help minimize the rate of unexpected trapezius muscle paresis after surgery of the neck.

AUTHOR INFORMATION

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Accepted for publication May 16, 2001.

Corresponding author and reprints: Antonius C. Kierner, MD, Schwanheimerstr 3, D-60 528 Frankfurt a.M., Germany (e-mail: kierner{at}em.uni-frankfurt.de).

From the Ear, Nose, and Throat Department, University Hospital Vienna (Drs Kierner and Burian), and the Institute of Anatomy 2, University of Vienna (Dr Zelenka), Vienna, Austria. Dr Kierner is now with the Ear, Nose, and Throat Department, University of Frankfurt, Frankfurt a.M., Germany.

REFERENCES

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1. Kierner AC, Zelenka I, Heller S, Burian M. Surgical anatomy of the spinal accessory nerve and the trapezius branches of the cervical plexus. Arch Surg. 2000;135:1428-1431. FREE FULL TEXT 2. Gordon SC, Graham WP, Black JT, Miller SH. Accessory nerve function after surgical procedures in the posterior triangle. Arch Surg. 1977;112:264-268. FREE FULL TEXT 3. Carenfelt C, Eliasson K. Occurrence, duration and prognosis of unexpected accessory nerve paresis in radical neck dissection. Acta Otolaryngol. 1980;90:470-473. FULL TEXT | PUBMED 4. Blessing R, Mann W, Beck CHL. Wie sinnvoll ist der Erhalt des Nervus accessorius bei der Halsausräumung? Laryngol Rhinol Otol (Stuttg). 1986;65:403-405. FULL TEXT 5. Yagnik PM, Chong PS. Spinal accessory nerve injury: a complication of carotid endarterectomy. Muscle Nerve. 1996;19:907-909. FULL TEXT | WEB OF SCIENCE | PUBMED 6. Nahum AM, Mullally W, Marmor R. A syndrome resulting from radical neck dissection. Arch Otolaryngol. 1961;74:424-428. 7. Haas E, Sollberg G. Untersuchungen über die Funktion des Schultergürtels nach Durchschneidung des N. accessorius. Laryngologie. 1962;10:669-677. 8. Sikken I, Höltje WJ. Die Rekonstruktion des Nervus accessorius nach radikaler Neck dissection. Dtsch Z Mund Kiefer Gesichtschir. 1980;4:36-39. 9. Kuntz AC, Weymuller EA. Impact of neck dissection on quality of life. Laryngoscope. 1999;109:1334-1338. FULL TEXT | WEB OF SCIENCE | PUBMED 10. Hausamen JE, Samii M, Schmidseder R. Indication and technique for the reconstruction of nerve defects in head and neck. J Maxillofac Surg. 1974;2:159-167. FULL TEXT | PUBMED 11. Fahrer H, Ludin HP, Mumenthaler M, Neiger M. The innervation of the trapezius muscle. J Neurol. 1974;207:183-188. FULL TEXT | WEB OF SCIENCE | PUBMED 12. Weisberger EC. The efferent supply of the trapezius muscle: a neuroanatomic basis for the preservation of shoulder function during neck dissection. Laryngoscope. 1987;97:435-445. WEB OF SCIENCE | PUBMED 13. Niemeyer K, Ludolph A. Zur Bedeutung der subfaszialen Äste des Plexus cervicalis für die motorische Innervation des M. trapezius. Dtsch Z Mund Kiefer Gesichtschir. 1987;11:356-360. PUBMED 14. Brown H, Burn S, Kaiser CW. The spinal accessory nerve plexus, the trapezius muscle, and shoulder stabilization after radical neck cancer surgery. Am Surg. 1988;208:654-661. 15. Soo KC, Guiloff RJ, Oh A, Della Rovere GQ, Westbury G. Innervation of the trapezius muscle: a study in patients undergoing neck dissections. Head Neck. 1990;12:488-495. FULL TEXT | WEB OF SCIENCE | PUBMED 16. Krause HR, Kornhuber A, Dempf R. A technique for diagnosing the individual patterns of innervation of the trapezius muscle prior to neck dissection. J Craniomaxillofac Surg. 1993;21:102-106. PUBMED 17. Jensen C, Westgaard RH. Functional subdivision of the upper trapezius muscle during low-level activation. Eur J Appl Physiol Occup Physiol. 1997;76:335-339. FULL TEXT | WEB OF SCIENCE | PUBMED 18. Sihler C. Über Muskelspindeln und intramuskuläre Nervenendigungenbei Schlangen und Fröschen. Arch Mikros Anat Entwicklungs. 1895;46:709-725. 19. Wu BL, Sanders I. A technique for demonstrating the nerve supply of whole larynges. Arch Otolaryngol Head Neck Surg. 1992;118:822-827. FREE FULL TEXT 20. Krause HR. Reinnervation of the trapezius muscle after radical neck dissection. J Craniomaxillofac Surg. 1994;22:323-329. PUBMED 21. Krause HR, Bremerich A, Herrmann M. The innervation of the trapezius muscle in connection with radical neck-dissection: an anatomical study. J Craniomaxillofac Surg. 1991;19:87-89. PUBMED 22. Karuman PM, Soo KC. Motor innervation of the trapezius muscle: a histochemical study. Head Neck. 1996;18:254-258. FULL TEXT | WEB OF SCIENCE | PUBMED 23. Weitz JW, Weitz SC, McElhinney AJ. A technique for preservation of spinal accessory nerve function in radical neck dissection. Head Neck Surg. 1982;5:75-78. FULL TEXT | WEB OF SCIENCE | PUBMED 24. Rosenstein A. Anatomie der peripheren Nerven. Berlin, Germany: Springer Verlag; 1935. Bumke O, Foerster O, eds. Handbuch der Neurologie; vol 1.

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