Surgical 2 Radiolog,c Anatomy
Surg Radiol Anat (!992) 14 : 203-208
Journal of Clinical Anatomy
© Springer-Verlag 1992
Anatomical basis of the anterior cervical spine approach: topographic study of the nerve structure D Liguoro, JM Vital, J Gu6rin and J Senegas Laboratoire d' Anatomic, UER I, 146, rue L6o Saignat, F-33076 Bordeaux Cedex, France
Summary. The results of the surgical anterior approach to the cervical spine are marked in a number of cases by dysphagia and dysphonia, especially when the approach is extensive or performed at the upper cervical spine. 35 cadaver dissections were performed to define the topography of the nerve structures during operative exposure at various vertebral levels : superior and recurrent laryngeal nerves, hypogtossal nerve and its superior root of the ansa cervicalis. The authors suggest some technical improvements, for each stage of surgical dissection.
Bases anatomiques de l'abord ant~rieur du rachis cervical: ~tude topographic des structures nerveuses Les suites de la chirurgie du rachis cervical par vole ant6rieure pr6sternocl6idomasto'~'dienne sont marqu6es dans un nombre de cas non
Offprint requests : D Liguoro, Service de Neurochirurgie, H6pital Pellegrin, Place Am61ie Raba-L6on, F-33076 Bordeaux C6dex, France
n6gligeable par des troubles de la d6glutition et de la phonation, et ce, d'autant que l'abord est 6tendu. 35 dissections sur cadavres ont 6t6 r6alis6es afin de pr6ciser la topographic par rapport aux niveaux vert6braux, le trajet et les variations des 616ments nerveux rencontr6s lots de cet abord cervical : nerfs laryng6s sup6rieur et r6current, neff hypoglosse et la racine sup6rieure de l'anse cervicale. A partir de cette 6tude morphologique, les auteurs suggbrent quelques points d' am6lioration technique, ~ chacune des &apes de la dissection, en pratique chirurgicale.
Key words : Cervical spine - Anterior approach - - Hypoglossal nerve - - S u p e r i o r and inferior laryngeal nerves
Following the introduction by Smith and Robinson in 1955 of the anterior approach to the cervical spine and its development by Cloward [10], the operation gained widespread acceptance as a relatively safe and effective method of cervical
spine surgery. The original procedure has been modified by many surgeons but the basic aspects remain essentially unchanged [9, 11, 28]. This technique is simple, makes use of natural anatomic planes, but requires dissection in the vicinity of anatomic structures encountered during exposure. Specific problems related to this surgery can be divided into three types : exposure injuries, spinal cord or nerve root injuries and problems related to bone fusion. Injury to nearly all of the structures has been reported in the literature [1, 3, 15, 19, 22, 23, 36, 38, 39, 41]. The most frequent problems related to the anterior approach itself are dysphagia and dysphonia, often transient for a few days but sometimes persisting several months. Different clinical reports have suggested that the damage to these nerves may result from stretching, ligation or division. 35 cadaver dissections were performed to define the topography of the nerve structures during operative exposure at the various vertebral levels. The practical application of the anatomic findings are presented, and r e c o m m e n d a t i o n s are made which have proved beneficial in
204 preventing complications or alleviating those which can not be avoided.
Anatomical study Material and methods In order to work in the most realistic surgical dissection conditions, 35 dissections were performed on fresh cadavers (death < 48 h). Average age was 70 years, 20 had a long thin neck and 15 had necks which were fat and short. The cadavers were placed supine on the operating table without hyperextension of the neck, which was rotated to the opposite side as in the anterior approach, approximately 10 degrees. To preserve the initial aspect of the cadaver, a large transverse collar incision was made along the upper border of the clavicles, from the midline toward the lateral borders of the sternocleidomastoid muscles. The skin and platysmal flaps were retracted to reveal the right and left anterolateral sides of the neck. However, the identification o f the small terminal branches of the superficial cervical plexus and the mandibular branch of the facial nerve was difficult in many cases. The encircling layer of deep cervical fascia was then incised along the anterior border of the sterno-mastoid muscle, allowing access to the space between the carotid sheath laterally, and the midline structures o f the neck medially. The superior belly of the omohyoid muscle was cut, and two strands were left in place to pinpoint the two parts of the muscle head. After its sternoclavicular ties had been cut, the sternomastoid muscle was retracted outwards to reveal the carotid sheath. Along the anterior part of the vascular sheath, the dissection of the ansa cervicalis (or anastomosis between the superior root of the ansa (descending branch of XII) and the inferior root
D Liguoroet al : Anatomicalbasis of the anteriorcervicalspineapproach:nervestructure (descending branch) of the cervical plexus) was then performed; then its collateral branches to the infrahyoid muscles were differentiated (Fig. 1). By moving the index finger carefully, a plane of cleavage could be opened easily in the loose fascia between the carotid sheath and the midline structures of the neck, over a distance sufficient to allow exposure of two or three cervical levels. A right approach was performed on all the cadavers, and a bilateral one on 20 of them. At the lower cervical spine, the recurrent laryngeal nerve and the inferior thyroid artery were located and dissected. Dissection was then pursued upwards towards the submandibular region. The capsule around the submandibular gland was divided three times and the gland retracted cephalad to correctly clear the upper part of the vasculovisceral passage. The hypoglossal trunk, its relationships with the stylohyoid and digastric muscles, and the origin of superior root of the ansa from it, were then located (Fig. 2). Sectioning of the digastric muscle tendon makes it possible to reveal the external and internal carotids, and to shift the hypoglossal trunk outwards and upwards. The branches of the external carotid artery and the superior laryngeal nerve were then dissected (Fig. 3). Exposure was found to be readily obtained from the anterior portion of C2 distally to that of T1. Topography of the various right and left nerves was located with reference to the vertebral levels. The route of the n e r v e s is oblique or vertical, but never exactly horizontal, in the space between the vascular sheath and the midline structures. During the surgical approach, dissection was performed in this plane of cleavage, under the anterior border of the sternothyroid muscle, just medial to the carotid sheath. So the point where the nerve
intersects with the medial wall of the carotid artery, was referred to the vertebral level. The vertebral levels were counted from top to bottom, C2 and its dens were the first reference. In several elderly cadavers, the osteophytes masked the limits between the vertebral bodies and the discs, so these were first resected. Results The shape of the neck varies, particularly according to the plumpness of the individual; however, its length is always roughly the same. So the hyoid bone referred to the intervertebral space C3-C4 or to the vertebral body of C4. The cricoid cartilage corresponds to disc C6-C7. The h y p o g l o s s a l nerve: the superior root of the ansa cervicalis (descending branch of the hypoglossal nerve) leaves the hypoglossal trunk on a level with the upper carotid region, where the vertical XII becomes transverse when it passes between the internal jugular vein and the internal carotid artery. In any case, the superior root is situated a few millimeters upstream the crossing o f the hypoglossal trunk and the digastric muscle tendon. The superior root only once came from XII on a level with this intersection. It was then situated vertically in the anterior dihedral angle between the internal carotid artery and the internal jugular vein, in a doubling into two of the vascular sheath. The superior root of the ansa (descending branch of XII) anastomoses with the inferior root from the cervical plexus at a level with the superior belly of the omohyoid muscle, or sometimes at the level of its intermediate tendon. Twice, this anastomosis, the ansa cervicalis, was one centimeter under the superior belly of the omohyoid, and three times was far superior to the muscle. In most cases therefore the
Figs. la,b-3a,b la,b (1) Internal jugular vein (2) common carotid artery (3) superior root of ansa cervicalis (descending branch of the hypoglossal nerve) (4) nerve branches for the superior belly of the omo-hyoid muscle (5) nerve branches for the infrahyoid muscles (6) infra-hyoid muscles. 2a,b (1) Internal jugular vein (2) common carotid artery (3) superior thyroid artery (4) posterior belly of the digastric muscle (5) stylo-hyoid muscle (6) hypoglossal trunk (7) superior root of ansa cervicalis (descending branch of the hypoglossal nerve) (8) infrahyoid muscles. 3a,b (1) Internal jugular vein (2) common carotid artery (3) external carotid artery (4) superior thyroid artery (5) occipital artery (6) hypoglossal trunk (7) superior root of ansa cervicalis (descending branch of the hypoglossal nerve) (8) great horn of the hyoid bone (9) superior laryngeal nerve la,b (1) Veine jugulaire interne (2) attire carotide commune (3) branche descendante du nerf hypoglosse (4) branche nerveuse pour le ventre supfrieur du muscle omo-hyo'fdien (5) branches nerveuses pour les muscles infra-hyo'ldiens (6) muscles infra-hyo~'diens. 2a,b (1) Veine jugulaire interne (2) art~re carotide commune (3) attire thyro~'dienne suprrieure (4) ventre postrrieur du muscle digastrique (5) muscle styloh y o / d i e n (6) tronc du nerf hypoglosse (7) branche descendante du neff hypoglosse (8) muscles infra-hyoldiens. 3a,b (1) Veine jugulaire interne (2) attire carotide commune (3) attire carotide externe (4) art~re thyro'/dienne sup~rieure (5) attire occipitale (6) tronc du nerf hypogtosse (7) branche descendante du neff hypoglosse (8) grande corne de l'os hyo'ide (9) neff laryng6 suprrieur
CRAN.
206 ansa cervicalis was on a level with C4, and only once with C3. The collateral nerve branches of the ansa cervicalis, arising from its convexity, innervate the infrahyoid muscles; the branches for the thyrohyoid, sternohyoid and sternothyroid muscles lie as a bridge in the plane of cleavage used surgically between the carotid sheath and the midline structures. The nerve to the superior belly of the o m o h y o i d generally arises very high up, from the superior root of the ansa itself. The nerve to the inferior belly of the omohyoid arises near the convexity of the ansa. The nerves to the last three infrahyoid muscles arise from the ansa independently, or from a c o m m o n trunk for two or all of them. Five times, this inferior anastomosis between the superior root and cervical plexus did not resemble a classical ansa; the inferior root of the ansa seemed to be double. This form corresponds to the medial and lateral varieties o f a n a s t o m o s i s which are usually described. In all cases, the nerves to the infrahyoid muscles were between the level of the vertebral bodies of C5 to C7 (Fig. 2). The recurrent laryngeal nerve : this enters the larynx through the inferior constrictor muscle of the lower pharynx, on a level with C6 or with the intervertebral space C6C7. The t o p o g r a p h y o f the left recurrent laryngeal nerve was not noted because of its vertical direction, ascending in the tracheo-oesophageal groove, and resting somewhat more deeply in this sulcus than on the right side. On the right side, the recurrent laryngeal nerve and the inferior thyroid artery are located. The nerve classically bisects the line of the angle defined by the right tracheal border and the inferior thyroid artery. The nerve was deep to the artery, except once when it was superficial to it. In the sagittal plane, the
D Liguoroet al : Anatomicalbasis of the anteriorcervicalspine approach:nervestructure recurrent laryngeal nerve was in front of the inferior thyroid artery in 10 cases, behind it in 21 cases, and between its collateral branches in 3 cases. The inferior thyroid artery crosses the common carotid artery at the level of the intervertebral space C6-C7, up to the laryngeal nerve, and more or less far away from it. The point of intersection between the recurrent laryngeal nerve and the medial wall of the carotid artery, was on a level with the vertebral body of C7 in 9 cases, of the intervertebral space C7-T1 in 10 cases, and of the vertebral body of T1 in 16 cases. The superior laryngeal nerve: this was always on a level with C3, but f a c i n g the v a s c u l o v i s c e r a l space, it has a concave curve whose vertex is on a level with C3-C4. It was always found behind the great horn of the hyoid bone. The superior thyroid artery is a poor guide for l o c a t i n g the s u p e r i o r l a r y n g e a l nerve, because of its numerous anatomical variations; moreover, for half the cases, the artery did not a c c o m p a n y the nerve, but was always away from it, facing the vasculovisceral space. Except for the recurrent laryngeal nerve, the positional indicators of the nerves are the same, on both right and left sides in the same cadaver.
Surgical applications This morphological study allows prediction with a high degree of probability of the nerve structures met during the anterior approach to the different levels of the cervical spine. The ansa cervicalis cannot be harmed during this surgical procedure owing to its lateral location; its superior root can be stretched if the hypoglossal trunk is too strongly retracted upwards.
One or several nerve branches to the infrahyoid muscles must be cut when the anterior approach is performed between the levels C5 andC7 [2,4,7, 12, 13]. The superior laryngeal nerve on a level with C3 bars the plane of c l e a v a g e a b o v e ; s i m i l a r l y , the recurrent laryngeal nerve shuts off the vasculovisceral passage between C7 and T1. Deglutition and phonation are two complicated functions which involve many organs, and motor activities; they are closely linked with other vital functions such as respiration [14, 20, 25, 26, 29]. Therefore, the least imbalance may s o m e t i m e s disturb one of these functions. Many local injuries often do not cause any disorder themselves, but the association of several injuries lead to post-operative, transient or persistent complications, especially after the approach to the upper cervical spine, or to several levels (more than three). Certain factors seem to influence the occurence of these complications: the type of retractors used, the number of levels approached, the use or not o f the o p e r a t i v e microscope, and recurrent laryngeal nerve injuries due to endotracheal intubation. These factors are debated elsewhere and are not the subj e c t o f our p r e s e n t d i s c u s s i o n . T h e skin incision is u s u a l l y transverse in a crease of the neck, for aesthetic reasons; but when more than two vertebral levels are approached, this incision provides insufficient exposure and anatomic structures have to be stretched; so a vertical incision is more suitable. With the cases of upper cervical spine approach above C3, the incision must be pursued first vertically, then horizontally toward the mastoid, more than 2 cm below the m a n d i b u l a r rim. Indeed, further incision upward or a narrow incision involves more tissue stretching
D Liguoroet al : Anatomicalbasis of the anteriorcervicalspineapproach:nervestructure and can cause an injury to the mandibular branch of the facial nerve [16, 30]. There is much discussion as to which side should be chosen in the anterior approach because of the recurrent laryngeal nerve. On the left, the recurrent nerve is strictly vertical, ascending to the tracheo-oesophageal groove [33, 37]; it may be compressed but is less vulnerable to stretching. Nevertheless, some authors insist on the risk associated with the oesophagus being situated slightly to the left and on the risk from the presence of the thoracic duct. On the right, the recurrent laryngeal nerve is oblique, superior and inside, and is more superficial. It shuts off the vasculovisceral pass between C7 et TI. Its position is guided by the inferior thyroid artery. Many surgeons do not locate the recurrent nerve and usually ligate the inferior thyroid artery near the common carotid artery. This compromises vascularization of the right parathyroid glands, but this is not of great importance, not of cervical oesophageal vascularization. Moreover, the oesophagus is compressed by surgical retractors. So it seems more logical to prevent dysphagia and dysphonia, by ligating the inferior thyroid artery medial to the recurrent nerve. It is then necessary to locate the nerve. In rare cases, the right recurrent laryngeal nerve is not recurrent, is located higher than normal; this anatomical variety is, for some surgeons, an argument for the left anterior approach to the cervical spine [6, 31, 32, 34, 40]. The importance of the superior laryngeal nerve in swallowing and phonation is diversely estimated. Several surgeons consider that this nerve can be d e l i b e r a t e l y cut without sequellae. However, injury to the superior laryngeal nerve gives rise to a palsy of the cricothyroid
muscle and to a sensory deficit of the laryngeal mucous membrane. In practice, the diagnosis is not easy because the alterations of the vocal properties are often discreet. Yet this problem may be of some importance according to the patients and their profession [5, 18, 24]. In our 35 dissections, the superior laryngeal nerve had an invariable route. It barred above, and on a level with C3, the plane of cleavage to the anterior approach. At this level, dissection has to be performed close to the arterial wails of the carotid bifurcation and the superior thyroid artery, in order to mobilize the laryngeal nerve more easily. Sectioning of the trunk of the hypoglossal nerve entails a palsy of the homolateral hemi-tongue, and perturbs the oral stage of deglutition, so the nerve must be located. When the XII is located during approaches above C3, the tendon of the digastric muscle has to be cut in order to avoid stretching lesions of the trunk of XII and to retract it upwards. The occipital artery also has to be ligated because it often surrounds the trunk of XII. Innervation of the infrahyoid muscles can be interrupted, either by sectioning the nerve branches of these muscles on this side during cervical spine exposures from C5 to C7, or by stretching the superior root of the ansa (descending branch of XII), when the latter is too strongly retracted upwards. Elaborate electrophysiological research has investigated the role in p h o n a t i o n of these i n f r a h y o i d muscles which, with the cricothyroid muscle (innervated by the superior laryngeal nerve), adjust the pitch of the voice [17, 21, 27, 35]. In effect, during cervical ganglionic treatment in cervicofacial surgery, the superior root of the ansa (descending branch of the XII) is cut without involving post-operative dysphonia. However these nerve
207 lesions associated with others, such as those caused by compression on the visceral axis, may explain the transient post-operative dysphagia and/or dysphonia, which is more frequent in this spinal surgery. At the end of the surgical procedure, closure must avoid unbalancing the structures of this region. The two parts of the superior belly of the omohyoid muscle are carefully sutured, as well as the platysma, mainly for aesthetic reasons and owing to the accessory action of the latter in mimicking. Conclusion Dysphagia and dysphonia are the most frequent complications of the anterior cervical approach to the cervical spine, and mainly to the upper cervical spine or with extensive approaches. Swallowing and phonation are very complex functions, and the least imbalance may sometimes disturb one of them. Many of these local surgical lesions do not cause any trouble individually, but their association favours transitory or persistent post-operative complications. This anatomic study throws new light on the muscular and neurovascutar relations during the operative approach to the various vertebral levels. Technical improvements are suggested for each stage of dissection, with particular emphasis on the value of locating the superior and recurrent laryngeal nerves and the hypoglossal nerve in order to protect them. References 1. Barber FA (1977) Anterior cervical fusion; the post-operative complications. RockyMount Med J 75 : 93-100 2. Barnard JW (1940) The hypoglossal complex of vertebrates. J Comp Neurol 72 : 489-524 3. BertalanffyH, Eggert HR (1989) Complications of anteriorcervical discecto-
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17. F a a b o u r g - A n d e r s e n K, Sonninen A (1960) The function of the extrinsic laryngeal muscles at different pitch, Acta Oto-Laryngol 51 : 89-93 18. F a a b o u r g - A n d e r s e n K, Jensen AM (1964) Unilateral paralysis of the superior laryngeal nerve. Acta Oto-Laryngol 57 : 155-159 19. Flynn TB (1982) Neurologic complications of anterior cervical interbody fusion. Spine 7 : 536-539 20. Haguenauer JP (1984) Physiologie de la drglufition. Oto-Rhino-Laryngologie 20801 A10, 4-1-1t : 55-66 21. Hast MH (1968) Etudes sur les muscles laryngds extrinsbques. Arch Oto-Laryngol 88 : 273-278 22. Heeneman H (1973) Vocal cord paralysis following approaches to the anterior cervical spine. Laryngoscope 83 : 17-21 23. Jacobson L (1979) Bilateral vocal cord paralysis following anterior cervical fusion. Anaesthesia 34 : 1020-1023 24. Kaeser HE, Richter HR (1965) La paralysie isolde du muscle cricothyro~dien. Rev Neurol 112 : 339-341 25. Le Huche F, Allali A (1984) La voix. In: Anatomie et physiologic des organes de la voix et de la parole. Collection phoniatrie Masson, Paris 26. Leperchey F (1979) Embryogdnie des muscles faciaux, masticateurs, de la langue, du voile et du cou. Rev Stomatol Chir Maxillo-Fac 80 : 45-67 27. Lesoine W (1971) Etudes expdrimentales des muscles sus et sons-hyo'/diens. Archiv Ohren-Nasen-Kehlkopfheilkd 199 : 707-714 28. Louis R (1982) Chirurgie du rachis. In : Anatomie chirurgicale et voies d' abord. Springer-Verlag, Berlin Heidelberg New York, pp 148-173 29. Meyer B (1984) Voles nerveuses et physiologie de la phonation, Oto-RhinoLaryngologie 20632 AI0, 12-1984, 1-14 30. Nelson DW, Gingrass RP (1979) Anatomy of the mandibular branches of the facial nerve, Plastic Reconstr Surg 64 : 479-482
31. Nemiroff PM, Katz AD (1982) Extralaryngeal divisions of the recurrent laryngeal nerve. Surgical and clinical significance. Am J Surg 144 : 466-469 32. Nobles ER (1970) Non-recurrent laryngeal nerve. Arch Surg 100 : 741-742 33. Rouviere H (1972) Anatomic humaine, descriptive, topographique et fonctionnelle. Massou, Paris 34. Sanders G, U y e d a RY, Karlan MS (1983) Non-recurrent inferior laryngeal nerves and their association with a recurrent branch. Am J Surg 146 : 501-503 35. Sapir S, Campbell C, Larson C (1981) Effect of geniohyoM, cricothyro~'d and sternothyro[d muscle stimulation on voice fundamental frequency of electrically elicited phonation in rhesus macaque. Laryngoscope 91 : 457-468 36. Selecki BR (1971) Complications and limitations of anterior decompression and fusion of the cervical spine (Cloward's technique). Meal J Australia 58 : 1235-1237 37. Testut L, Latarjet A (1949) Trait6 d'anatomie humaine. Doin Ed. & Cie, Paris pp 193-204 38. Tew JM, Mayfield FH (1976) Complications of surgery of the anterior cervical spine. Clin Neurosurg 23 : 424-434 39. Tew JM, Mayfield FH (t981) Surgery of the anterior cervical spine : prevention of complications. In : Dunsker SB, ed. Cervical spondylosis. Raven Press, New York, pp 191-208 40. Vuillard P, Bouchet A, Gouillat C, Armand D (1978) Le neff laryng6 infrrienr non rrcurrent. Apropos de 15 cas oprratoires. Bull Assoc Anat 62 : 497505 41. Whitecloud TS (1978) Complications of anterior cervical fusion. In : AAOS, Instructional courses lectures, 27, Chapl6
Received September 16, 1991~Accepted in final form April 21, 1992
Surg Radiol Anat (!992) 14 : 203-208
Journal of Clinical Anatomy
© Springer-Verlag 1992
Anatomical basis of the anterior cervical spine approach: topographic study of the nerve structure D Liguoro, JM Vital, J Gu6rin and J Senegas Laboratoire d' Anatomic, UER I, 146, rue L6o Saignat, F-33076 Bordeaux Cedex, France
Summary. The results of the surgical anterior approach to the cervical spine are marked in a number of cases by dysphagia and dysphonia, especially when the approach is extensive or performed at the upper cervical spine. 35 cadaver dissections were performed to define the topography of the nerve structures during operative exposure at various vertebral levels : superior and recurrent laryngeal nerves, hypogtossal nerve and its superior root of the ansa cervicalis. The authors suggest some technical improvements, for each stage of surgical dissection.
Bases anatomiques de l'abord ant~rieur du rachis cervical: ~tude topographic des structures nerveuses Les suites de la chirurgie du rachis cervical par vole ant6rieure pr6sternocl6idomasto'~'dienne sont marqu6es dans un nombre de cas non
Offprint requests : D Liguoro, Service de Neurochirurgie, H6pital Pellegrin, Place Am61ie Raba-L6on, F-33076 Bordeaux C6dex, France
n6gligeable par des troubles de la d6glutition et de la phonation, et ce, d'autant que l'abord est 6tendu. 35 dissections sur cadavres ont 6t6 r6alis6es afin de pr6ciser la topographic par rapport aux niveaux vert6braux, le trajet et les variations des 616ments nerveux rencontr6s lots de cet abord cervical : nerfs laryng6s sup6rieur et r6current, neff hypoglosse et la racine sup6rieure de l'anse cervicale. A partir de cette 6tude morphologique, les auteurs suggbrent quelques points d' am6lioration technique, ~ chacune des &apes de la dissection, en pratique chirurgicale.
Key words : Cervical spine - Anterior approach - - Hypoglossal nerve - - S u p e r i o r and inferior laryngeal nerves
Following the introduction by Smith and Robinson in 1955 of the anterior approach to the cervical spine and its development by Cloward [10], the operation gained widespread acceptance as a relatively safe and effective method of cervical
spine surgery. The original procedure has been modified by many surgeons but the basic aspects remain essentially unchanged [9, 11, 28]. This technique is simple, makes use of natural anatomic planes, but requires dissection in the vicinity of anatomic structures encountered during exposure. Specific problems related to this surgery can be divided into three types : exposure injuries, spinal cord or nerve root injuries and problems related to bone fusion. Injury to nearly all of the structures has been reported in the literature [1, 3, 15, 19, 22, 23, 36, 38, 39, 41]. The most frequent problems related to the anterior approach itself are dysphagia and dysphonia, often transient for a few days but sometimes persisting several months. Different clinical reports have suggested that the damage to these nerves may result from stretching, ligation or division. 35 cadaver dissections were performed to define the topography of the nerve structures during operative exposure at the various vertebral levels. The practical application of the anatomic findings are presented, and r e c o m m e n d a t i o n s are made which have proved beneficial in
204 preventing complications or alleviating those which can not be avoided.
Anatomical study Material and methods In order to work in the most realistic surgical dissection conditions, 35 dissections were performed on fresh cadavers (death < 48 h). Average age was 70 years, 20 had a long thin neck and 15 had necks which were fat and short. The cadavers were placed supine on the operating table without hyperextension of the neck, which was rotated to the opposite side as in the anterior approach, approximately 10 degrees. To preserve the initial aspect of the cadaver, a large transverse collar incision was made along the upper border of the clavicles, from the midline toward the lateral borders of the sternocleidomastoid muscles. The skin and platysmal flaps were retracted to reveal the right and left anterolateral sides of the neck. However, the identification o f the small terminal branches of the superficial cervical plexus and the mandibular branch of the facial nerve was difficult in many cases. The encircling layer of deep cervical fascia was then incised along the anterior border of the sterno-mastoid muscle, allowing access to the space between the carotid sheath laterally, and the midline structures o f the neck medially. The superior belly of the omohyoid muscle was cut, and two strands were left in place to pinpoint the two parts of the muscle head. After its sternoclavicular ties had been cut, the sternomastoid muscle was retracted outwards to reveal the carotid sheath. Along the anterior part of the vascular sheath, the dissection of the ansa cervicalis (or anastomosis between the superior root of the ansa (descending branch of XII) and the inferior root
D Liguoroet al : Anatomicalbasis of the anteriorcervicalspineapproach:nervestructure (descending branch) of the cervical plexus) was then performed; then its collateral branches to the infrahyoid muscles were differentiated (Fig. 1). By moving the index finger carefully, a plane of cleavage could be opened easily in the loose fascia between the carotid sheath and the midline structures of the neck, over a distance sufficient to allow exposure of two or three cervical levels. A right approach was performed on all the cadavers, and a bilateral one on 20 of them. At the lower cervical spine, the recurrent laryngeal nerve and the inferior thyroid artery were located and dissected. Dissection was then pursued upwards towards the submandibular region. The capsule around the submandibular gland was divided three times and the gland retracted cephalad to correctly clear the upper part of the vasculovisceral passage. The hypoglossal trunk, its relationships with the stylohyoid and digastric muscles, and the origin of superior root of the ansa from it, were then located (Fig. 2). Sectioning of the digastric muscle tendon makes it possible to reveal the external and internal carotids, and to shift the hypoglossal trunk outwards and upwards. The branches of the external carotid artery and the superior laryngeal nerve were then dissected (Fig. 3). Exposure was found to be readily obtained from the anterior portion of C2 distally to that of T1. Topography of the various right and left nerves was located with reference to the vertebral levels. The route of the n e r v e s is oblique or vertical, but never exactly horizontal, in the space between the vascular sheath and the midline structures. During the surgical approach, dissection was performed in this plane of cleavage, under the anterior border of the sternothyroid muscle, just medial to the carotid sheath. So the point where the nerve
intersects with the medial wall of the carotid artery, was referred to the vertebral level. The vertebral levels were counted from top to bottom, C2 and its dens were the first reference. In several elderly cadavers, the osteophytes masked the limits between the vertebral bodies and the discs, so these were first resected. Results The shape of the neck varies, particularly according to the plumpness of the individual; however, its length is always roughly the same. So the hyoid bone referred to the intervertebral space C3-C4 or to the vertebral body of C4. The cricoid cartilage corresponds to disc C6-C7. The h y p o g l o s s a l nerve: the superior root of the ansa cervicalis (descending branch of the hypoglossal nerve) leaves the hypoglossal trunk on a level with the upper carotid region, where the vertical XII becomes transverse when it passes between the internal jugular vein and the internal carotid artery. In any case, the superior root is situated a few millimeters upstream the crossing o f the hypoglossal trunk and the digastric muscle tendon. The superior root only once came from XII on a level with this intersection. It was then situated vertically in the anterior dihedral angle between the internal carotid artery and the internal jugular vein, in a doubling into two of the vascular sheath. The superior root of the ansa (descending branch of XII) anastomoses with the inferior root from the cervical plexus at a level with the superior belly of the omohyoid muscle, or sometimes at the level of its intermediate tendon. Twice, this anastomosis, the ansa cervicalis, was one centimeter under the superior belly of the omohyoid, and three times was far superior to the muscle. In most cases therefore the
Figs. la,b-3a,b la,b (1) Internal jugular vein (2) common carotid artery (3) superior root of ansa cervicalis (descending branch of the hypoglossal nerve) (4) nerve branches for the superior belly of the omo-hyoid muscle (5) nerve branches for the infrahyoid muscles (6) infra-hyoid muscles. 2a,b (1) Internal jugular vein (2) common carotid artery (3) superior thyroid artery (4) posterior belly of the digastric muscle (5) stylo-hyoid muscle (6) hypoglossal trunk (7) superior root of ansa cervicalis (descending branch of the hypoglossal nerve) (8) infrahyoid muscles. 3a,b (1) Internal jugular vein (2) common carotid artery (3) external carotid artery (4) superior thyroid artery (5) occipital artery (6) hypoglossal trunk (7) superior root of ansa cervicalis (descending branch of the hypoglossal nerve) (8) great horn of the hyoid bone (9) superior laryngeal nerve la,b (1) Veine jugulaire interne (2) attire carotide commune (3) branche descendante du nerf hypoglosse (4) branche nerveuse pour le ventre supfrieur du muscle omo-hyo'fdien (5) branches nerveuses pour les muscles infra-hyo'ldiens (6) muscles infra-hyo~'diens. 2a,b (1) Veine jugulaire interne (2) art~re carotide commune (3) attire thyro~'dienne suprrieure (4) ventre postrrieur du muscle digastrique (5) muscle styloh y o / d i e n (6) tronc du nerf hypoglosse (7) branche descendante du neff hypoglosse (8) muscles infra-hyoldiens. 3a,b (1) Veine jugulaire interne (2) attire carotide commune (3) attire carotide externe (4) art~re thyro'/dienne sup~rieure (5) attire occipitale (6) tronc du nerf hypogtosse (7) branche descendante du neff hypoglosse (8) grande corne de l'os hyo'ide (9) neff laryng6 suprrieur
CRAN.
206 ansa cervicalis was on a level with C4, and only once with C3. The collateral nerve branches of the ansa cervicalis, arising from its convexity, innervate the infrahyoid muscles; the branches for the thyrohyoid, sternohyoid and sternothyroid muscles lie as a bridge in the plane of cleavage used surgically between the carotid sheath and the midline structures. The nerve to the superior belly of the o m o h y o i d generally arises very high up, from the superior root of the ansa itself. The nerve to the inferior belly of the omohyoid arises near the convexity of the ansa. The nerves to the last three infrahyoid muscles arise from the ansa independently, or from a c o m m o n trunk for two or all of them. Five times, this inferior anastomosis between the superior root and cervical plexus did not resemble a classical ansa; the inferior root of the ansa seemed to be double. This form corresponds to the medial and lateral varieties o f a n a s t o m o s i s which are usually described. In all cases, the nerves to the infrahyoid muscles were between the level of the vertebral bodies of C5 to C7 (Fig. 2). The recurrent laryngeal nerve : this enters the larynx through the inferior constrictor muscle of the lower pharynx, on a level with C6 or with the intervertebral space C6C7. The t o p o g r a p h y o f the left recurrent laryngeal nerve was not noted because of its vertical direction, ascending in the tracheo-oesophageal groove, and resting somewhat more deeply in this sulcus than on the right side. On the right side, the recurrent laryngeal nerve and the inferior thyroid artery are located. The nerve classically bisects the line of the angle defined by the right tracheal border and the inferior thyroid artery. The nerve was deep to the artery, except once when it was superficial to it. In the sagittal plane, the
D Liguoroet al : Anatomicalbasis of the anteriorcervicalspine approach:nervestructure recurrent laryngeal nerve was in front of the inferior thyroid artery in 10 cases, behind it in 21 cases, and between its collateral branches in 3 cases. The inferior thyroid artery crosses the common carotid artery at the level of the intervertebral space C6-C7, up to the laryngeal nerve, and more or less far away from it. The point of intersection between the recurrent laryngeal nerve and the medial wall of the carotid artery, was on a level with the vertebral body of C7 in 9 cases, of the intervertebral space C7-T1 in 10 cases, and of the vertebral body of T1 in 16 cases. The superior laryngeal nerve: this was always on a level with C3, but f a c i n g the v a s c u l o v i s c e r a l space, it has a concave curve whose vertex is on a level with C3-C4. It was always found behind the great horn of the hyoid bone. The superior thyroid artery is a poor guide for l o c a t i n g the s u p e r i o r l a r y n g e a l nerve, because of its numerous anatomical variations; moreover, for half the cases, the artery did not a c c o m p a n y the nerve, but was always away from it, facing the vasculovisceral space. Except for the recurrent laryngeal nerve, the positional indicators of the nerves are the same, on both right and left sides in the same cadaver.
Surgical applications This morphological study allows prediction with a high degree of probability of the nerve structures met during the anterior approach to the different levels of the cervical spine. The ansa cervicalis cannot be harmed during this surgical procedure owing to its lateral location; its superior root can be stretched if the hypoglossal trunk is too strongly retracted upwards.
One or several nerve branches to the infrahyoid muscles must be cut when the anterior approach is performed between the levels C5 andC7 [2,4,7, 12, 13]. The superior laryngeal nerve on a level with C3 bars the plane of c l e a v a g e a b o v e ; s i m i l a r l y , the recurrent laryngeal nerve shuts off the vasculovisceral passage between C7 and T1. Deglutition and phonation are two complicated functions which involve many organs, and motor activities; they are closely linked with other vital functions such as respiration [14, 20, 25, 26, 29]. Therefore, the least imbalance may s o m e t i m e s disturb one of these functions. Many local injuries often do not cause any disorder themselves, but the association of several injuries lead to post-operative, transient or persistent complications, especially after the approach to the upper cervical spine, or to several levels (more than three). Certain factors seem to influence the occurence of these complications: the type of retractors used, the number of levels approached, the use or not o f the o p e r a t i v e microscope, and recurrent laryngeal nerve injuries due to endotracheal intubation. These factors are debated elsewhere and are not the subj e c t o f our p r e s e n t d i s c u s s i o n . T h e skin incision is u s u a l l y transverse in a crease of the neck, for aesthetic reasons; but when more than two vertebral levels are approached, this incision provides insufficient exposure and anatomic structures have to be stretched; so a vertical incision is more suitable. With the cases of upper cervical spine approach above C3, the incision must be pursued first vertically, then horizontally toward the mastoid, more than 2 cm below the m a n d i b u l a r rim. Indeed, further incision upward or a narrow incision involves more tissue stretching
D Liguoroet al : Anatomicalbasis of the anteriorcervicalspineapproach:nervestructure and can cause an injury to the mandibular branch of the facial nerve [16, 30]. There is much discussion as to which side should be chosen in the anterior approach because of the recurrent laryngeal nerve. On the left, the recurrent nerve is strictly vertical, ascending to the tracheo-oesophageal groove [33, 37]; it may be compressed but is less vulnerable to stretching. Nevertheless, some authors insist on the risk associated with the oesophagus being situated slightly to the left and on the risk from the presence of the thoracic duct. On the right, the recurrent laryngeal nerve is oblique, superior and inside, and is more superficial. It shuts off the vasculovisceral pass between C7 et TI. Its position is guided by the inferior thyroid artery. Many surgeons do not locate the recurrent nerve and usually ligate the inferior thyroid artery near the common carotid artery. This compromises vascularization of the right parathyroid glands, but this is not of great importance, not of cervical oesophageal vascularization. Moreover, the oesophagus is compressed by surgical retractors. So it seems more logical to prevent dysphagia and dysphonia, by ligating the inferior thyroid artery medial to the recurrent nerve. It is then necessary to locate the nerve. In rare cases, the right recurrent laryngeal nerve is not recurrent, is located higher than normal; this anatomical variety is, for some surgeons, an argument for the left anterior approach to the cervical spine [6, 31, 32, 34, 40]. The importance of the superior laryngeal nerve in swallowing and phonation is diversely estimated. Several surgeons consider that this nerve can be d e l i b e r a t e l y cut without sequellae. However, injury to the superior laryngeal nerve gives rise to a palsy of the cricothyroid
muscle and to a sensory deficit of the laryngeal mucous membrane. In practice, the diagnosis is not easy because the alterations of the vocal properties are often discreet. Yet this problem may be of some importance according to the patients and their profession [5, 18, 24]. In our 35 dissections, the superior laryngeal nerve had an invariable route. It barred above, and on a level with C3, the plane of cleavage to the anterior approach. At this level, dissection has to be performed close to the arterial wails of the carotid bifurcation and the superior thyroid artery, in order to mobilize the laryngeal nerve more easily. Sectioning of the trunk of the hypoglossal nerve entails a palsy of the homolateral hemi-tongue, and perturbs the oral stage of deglutition, so the nerve must be located. When the XII is located during approaches above C3, the tendon of the digastric muscle has to be cut in order to avoid stretching lesions of the trunk of XII and to retract it upwards. The occipital artery also has to be ligated because it often surrounds the trunk of XII. Innervation of the infrahyoid muscles can be interrupted, either by sectioning the nerve branches of these muscles on this side during cervical spine exposures from C5 to C7, or by stretching the superior root of the ansa (descending branch of XII), when the latter is too strongly retracted upwards. Elaborate electrophysiological research has investigated the role in p h o n a t i o n of these i n f r a h y o i d muscles which, with the cricothyroid muscle (innervated by the superior laryngeal nerve), adjust the pitch of the voice [17, 21, 27, 35]. In effect, during cervical ganglionic treatment in cervicofacial surgery, the superior root of the ansa (descending branch of the XII) is cut without involving post-operative dysphonia. However these nerve
207 lesions associated with others, such as those caused by compression on the visceral axis, may explain the transient post-operative dysphagia and/or dysphonia, which is more frequent in this spinal surgery. At the end of the surgical procedure, closure must avoid unbalancing the structures of this region. The two parts of the superior belly of the omohyoid muscle are carefully sutured, as well as the platysma, mainly for aesthetic reasons and owing to the accessory action of the latter in mimicking. Conclusion Dysphagia and dysphonia are the most frequent complications of the anterior cervical approach to the cervical spine, and mainly to the upper cervical spine or with extensive approaches. Swallowing and phonation are very complex functions, and the least imbalance may sometimes disturb one of them. Many of these local surgical lesions do not cause any trouble individually, but their association favours transitory or persistent post-operative complications. This anatomic study throws new light on the muscular and neurovascutar relations during the operative approach to the various vertebral levels. Technical improvements are suggested for each stage of dissection, with particular emphasis on the value of locating the superior and recurrent laryngeal nerves and the hypoglossal nerve in order to protect them. References 1. Barber FA (1977) Anterior cervical fusion; the post-operative complications. RockyMount Med J 75 : 93-100 2. Barnard JW (1940) The hypoglossal complex of vertebrates. J Comp Neurol 72 : 489-524 3. BertalanffyH, Eggert HR (1989) Complications of anteriorcervical discecto-
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Received September 16, 1991~Accepted in final form April 21, 1992
