- Email: [email protected]
The Hypoglossal Nerve: Anatomical Study of Its Entire Course
Accepted Manuscript The Hypoglossal Nerve: Anatomical Study Of Its Entire Course Giorgio Iaconetta, Domenico Solari, Alessandro Villa, Clotilde Castaldo, Rosa Maria Gerardi, Gianluigi Califano, Stefania Montagnani, Paolo Cappabianca PII:
S1878-8750(17)31733-3
DOI:
10.1016/j.wneu.2017.10.006
Reference:
WNEU 6659
To appear in:
World Neurosurgery
Received Date: 29 April 2017 Revised Date:
30 September 2017
Accepted Date: 3 October 2017
Please cite this article as: Iaconetta G, Solari D, Villa A, Castaldo C, Gerardi RM, Califano G, Montagnani S, Cappabianca P, The Hypoglossal Nerve: Anatomical Study Of Its Entire Course, World Neurosurgery (2017), doi: 10.1016/j.wneu.2017.10.006. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
THE HYPOGLOSSAL NERVE: ANATOMICAL STUDY OF ITS ENTIRE COURSE
RI PT
Giorgio Iaconetta1, Domenico Solari2, Alessandro Villa2, Clotilde Castaldo3, Rosa Maria Gerardi2, Gianluigi Califano2, Stefania Montagnani3, Paolo Cappabianca2.
Department of Medicine and Surgery, Division of Neurosurgery, Università degli Studi di
SC
1
Salerno, Salerno, Italy.
Department of Neurosciences and Reproductive and Odontostomatological Sciences,
M AN U
2
Division of Neurosurgery, Università degli Studi di Napoli Federico II, Napoli, Italy. 3
Department of Public Health, Division of Anatomy, Università degli Studi di Napoli
EP
TE D
Federico II, Napoli, Italy.
Corresponding Author:
AC C
Alessandro Villa, M.D.
Department of Neurosciences and Reproductive and Odontostomatological Sciences Division of Neurosurgery Università degli Studi di Napoli Federico II Via Pansini 5, 80131 Napoli, Italy Tel +39 081 7462490 e-mail: [email protected]
ACCEPTED MANUSCRIPT
ABSTRACT Object: Only a few anatomic studies concerning the entire course of the hypoglossal nerve (cranial nerve XII) have been reported. The purpose of the present study is to
RI PT
analyze all the relationships of the XII nerve with the surrounding structures from the brainstem to the tongue through a microscopic perspective. A comprehensive
anatomically and clinically oriented classification of its different segments is
SC
proposed.
Methods: Ten formalin-fixed adult human cadaveric heads (20 sides) were dissected
M AN U
with the aim to explore the entire course of the XII cranial nerve via the lateral suboccipital, the far lateral partial or total transcondilar routes. Different segments of the nerve were then identified, based on the hypoglossal course and its relationship with surrounding structures. Measurements of every portion of the nerve were taken in all specimens during the dissecting process.
TE D
Results: The hypoglossal nerve was divided into five segments: cisternal, canalar, descending, horizontal, and ascending. Detailed and comprehensive examination of the basic anatomical relationships through the view of different transcranial, and
EP
endoscope-assisted approaches was achieved. A new perspective of the hypoglossal canal is proposed and the venous plexus surrounding the canalar segment of the nerve
AC C
is described in detail.
Conclusion: The classification of five segments for the hypoglossal nerve seems anatomically valid and it is surgically oriented with respect to all surgical approaches. The precise knowledge of the relationships with the surrounding structures may help to prevent some complications during surgery and it is useful to explain, segment by segment, the pathogenic mechanisms for nerve injuries that are evidenced by lesions that exist along the entire intra- and extracranial course.
ACCEPTED MANUSCRIPT
KEY WORDS: hypoglossal nerve, XII, 12th, cranial nerves, hypoglossal canal,
RI PT
venous plexus.
SC
ABBREVIATIONS: REZ: root exit zone; PICA: posterior inferior cerebellar artery;
SHM: stylohyoid muscle.
INTRODUCTION
M AN U
VA: vertebral artery; SPM: stylopharyngeal muscle; SGM: styloglossus muscle;
TE D
During the past two decades, advances in the field of surgical microanatomy have allowed important progress in the development of surgical techniques in order to improve the excision of skull base lesions. Knowledge of the detailed anatomy and
EP
pathway of the hypoglossal nerve is critical for the management of lesions located in the posterior cranial fossa. Several pathological processes such as infections,
AC C
inflammatory diseases, traumas, and skull base tumors as neurinomas, metastasis, glomus jugulare masses may damage the 12th cranial nerve, which is the motor supply of the tongue, leading to its paralysis of both extrinsic and intrinsic muscles. Furthermore, this nerve has also an important role in respiration and swallowing, and a lesion, if unilateral(4, 15), does not cause severe restriction in function, however, if bilateral, may cause severe swallowing disturbances, dysarthria and respiratory difficulties due to airway obstruction(13, 21).
ACCEPTED MANUSCRIPT
In order to understand the pathology of the hypoglossal nerve and its relative treatment, the knowledge of the entire course of the nerve is extremely important. The anatomical relationships with the surrounding neurovascular structures and muscles,
RI PT
as well as having some constant landmarks to follow, are essential in surgical procedures when the preservation of the nerve is required. The nerve can be divided into
two
main
parts:
intracranial
and
extracranial.
Neurosurgeons,
SC
otorhinolaryngologists, maxillofacial surgeons, deal with the pathology of the
different segments of the nerve during surgical treatments to posterior fossa, neck, or
M AN U
mouth.
To our knowledge, very few articles are reported in the pertinent literature regarding the microsurgical anatomy of the hypoglossal nerve in its entire course. In the present anatomical study we describe our observations on the relationships of the nerve with the surrounding structures, from its exit zone on the medulla oblongata,
TE D
to its ending on the muscles of the tongue, describing all landmarks we have
EP
encountered while performing the dissections.
MATERIAL AND METHODS
AC C
Anatomic dissections were performed at the Center of Biotechnology of the “Antonio Cardarelli Hospital” in Napoli on 10 formalin-fixed adult human cadaveric heads (20 sides), whose arterial and venous system had been injected with red and blue latex, respectively. The specimens were from 7 men and from 3 women, aging from 59 to 85 years (mean age 72 years) at the time of death. Cadaveric dissections and nerve measurements took place under surgical microscope (Carl Zeiss®, Oberkochen, Germany) guidance while recording on DVDs.
ACCEPTED MANUSCRIPT
Additionally, a rigid endoscope 4 mm in diameter, 18 cm in length, with a 0-degree and 30-degree lens (Karl Storz, Tuttlingen, Germany) was used during dissections. We used OsiriX Lite®, a freeware software and user friendly, with its 3D volume
RI PT
rendering methods to obtain the 3-dimensional reconstruction of the head position for each approach.
With heads positioned as during surgery in operating room we performed the lateral
SC
suboccipital, the far lateral partial or total transcondilar, without or with removal of the lateral posterior arch of the atlas, surgical approaches according to the well-known
M AN U
techniques. (17)(16)(15)
Additionally, with the aim to expose the nerve in its entirety course we transected the mandibule and drilled all the petrous bone and the posterior wall of the hypoglossal canal. The extracranial course of the nerve with its terminating branches to muscles and tongue were exposed dissecting the neck and mouth floor. Length and thickness
TE D
of each segment of the nerve were measured with millimeter paper (see Table 1).
Transcranial approaches
EP
The lateral suboccipital approach was performed through a hockey-stick retrosigmoid exposure extending superomedial from the mastoid process along the superior nuchal
AC C
line to the inion and downward in the midline. This approach allows exposing our area of interest, located anteriorly to the brainstem toward the jugular foramen or cerebellopontine angle with the aim to expose the nerve running into it. The exposure allows performing a suboccipital craniectomy and laminectomy of the axis with the aim to clearly identify and follow the hypoglossal course. A more complete view of this region came combining the suboccipital approach with the far lateral approach with the aim to obtain a larger lateral view. Indeed, its
ACCEPTED MANUSCRIPT
supracondilar extension allows reaching the hypoglossal canal in its medial aspect, while the further drilling of the condyles enlarges the anatomical view of the
RI PT
surrounding neurovascular structures.
Neck dissection
The exposition of the extracranial course of the hypoglossal nerve took place via a
SC
transcervical approach; through a submandibular incision extending from the mastoid tip to the symphysis menti extended downward across the sternocleidomastoid
M AN U
muscle. Its inferior extension was carried from the midpoint of the submandibular incision across the sternocleidomastoid muscle. The transection of the mandibule helped to easily follow the hypoglossal course. The dissection went along the anterior border of the sternocleidomastoid muscle and between the carotid sheath, laterally and the esophagus and trachea, medially and it implied the retraction of prevertebral
TE D
muscles and fascia. At this point, deeper neurovascular structures as the superior thyroid arteries, external and internal laryngeal nerve and lingual artery as well as extrinsic muscles of the tongue were dissected in order to identify the hypoglossal
AC C
EP
course and their relationships.
RESULTS
According to its course and considering the relationships with surrounding structures, we have divided the hypoglossal nerve into five segments: − cisternal, − canalar, − descending,
ACCEPTED MANUSCRIPT
− horizontal, − ascending.
RI PT
Cisternal segment The nucleus of the 12th cranial nerve is located at the posterior aspect of the medulla
oblongata. Previous studies have shown that the nucleus extends for 15-18 mm in
SC
cranio-caudal direction, and it is represented by a focal bulge, named “hypoglossal
trigone”, under the floor of the fourth ventricle. This part of the nerve is
M AN U
intramedullary, traversing the medulla oblongata. From the trigone, the roots run towards the root exit zone (REZ), located at the preolivary sulcus, between the olive and the pyramid(10). The radicular fibers - studied with the help of additional fixation(14) by others Authors(11) - pass medial to the olive and lateral to the medial longitudinal fasciculus, medial lemniscus, accessory olivary nucleus and pyramidal
TE D
tract giving rise to the cisternal segment which ends at the dural pore(10). The rootlets emerging from the preolivary sulcus in our specimens range from 6 to 14 (mean 8.4) and they merge into 2-4 trunks (3 in 12/20, 60% of our specimens) (Fig. 1). They
EP
enter the canal by perforating the dura mater through one, two or three separate pores (Fig. 2). The mean total length of the cisternal segment in our specimens is 12.7 mm
AC C
(range: 8-15 mm) and the mean width of the bundles is 0.4 mm (range: 0.3-0.6 mm). The bundles, within the premedullary cistern, course anterolaterally, between the posterior inferior cerebellar artery (PICA) and the vertebral artery (VA), with the VA anterior to the nerve in nearly 93% of cases and posteriorly located only in 2.9%, according to the literature and as described first by Luschka in 1867(12). The PICA, on the contrary, courses anterior to the nerve in 5.9% of cases. A direct relationship between the hypoglossal nerve, VA and PICA has been previously documented in
ACCEPTED MANUSCRIPT
reports describing how these arteries may compress, distort, displace or stretch the nerve root bundles(25). In our specimens, we found all the bundles coursing posteriorly to the vertebral artery and, in some cases (25%), a cranial rootlet of the
RI PT
12th, longer than others, enveloping the PICA before the entry into the canal (Fig. 2). According with the previous studies, we observed an incredible tortuous course of the
SC
nerve between VA and PICA.
Canalar segment
M AN U
The hypoglossal canal is a bony passage containing the canalar segment of the hypoglossal nerve, a branch of the ascending pharyngeal artery, and a venous plexus which has previously been considered an anterior condylar vein(3). The hypoglossal canal extends from the posterior fossa to the nasopharyngeal carotid space, running anteriorly from an infero-medial direction to reach a supero-lateral
TE D
location. It is surrounded by the occipital condyles inferiorly, the jugular foramen and the jugular process of the occipital bone laterally and the sphenoid part of the clivus supero-medially. Specifically, this canal is closely related with the jugular foramen,
EP
which lies medial, inferior and posterior.
The canalar segment begins where the nerve trunks pass through the dural pore to
AC C
enter the hypoglossal canal (Fig. 2). The nerve is covered by arachnoid and dural sheaths along approximately two thirds of the length of the canal, while a venous plexus surrounds the canalar segment for its entire course. To the best of our knowledge, there are no exhaustive descriptions of this plexus in the literature. The venous plexus is a sort of tube, occupying the canal from the entrance to the exit, and sealed at the inner and outer extremities, corresponding to the entrance and the exit of the nerve from the canal. The plexus fills the space between bone and nerve, with the
ACCEPTED MANUSCRIPT
interior wall that is in contact with the nerve, and the external one that is in contact with the periosteum lining the canal. The plexus drains within the final portion of the sigmoid sinus, and within the jugular bulb through small veins piercing in the bone
RI PT
surface several tiny channels. Such small openings have been documented by endoscope-assisted approach after drilling of the posterior wall of the hypoglossal canal (Fig. 3).
SC
The mean length of the canal in our specimens was 13 mm (range: 9.5-16 mm), while
the mean width was 2 mm (range: 1.3-3). In one specimen, an inner perpendicular
M AN U
bony wall divided the canal in two different canals, and two nerves, fusing 3 mm after the extracranial exit, occupied each resulting canal (Fig. 2).
Descending segment
At its exit from the neurocranium, the hypoglossal nerve descends in the neck. At
TE D
first, it lies underneath the sternocleidomastoid muscle, between the small rectus muscle of the head and the internal carotid artery, and medial to the glossopharyngeal, vagus and accessory nerves. Then, running between the internal carotid and the
EP
jugular vein, it reaches the stylian muscles bundle, the stylopharyngeal (SPM), the styloglossus (SGM), and the stylohyoid (SHM) muscles. The nerve is lateral to the
AC C
SPM and SGM, and lateral to SHM and the posterior belly of the digastric muscle (Fig. 4). It crosses, then, the lateral surface of the external carotid artery and reaches the anterior margin of the sternocleidomastoid muscle, which is the inferior limit of this segment.
The mean length of this segment in our specimens was 65 mm (range: 48-89 mm) and the mean thickness was 3.2 mm (range: 2-4 mm).
ACCEPTED MANUSCRIPT
Horizontal segment The horizontal segment of the nerve runs transversally, passing between the great horn of the hyoid bone, which is located inferiorly, and the middle tendon of the
RI PT
digastric muscle, which is located superiorly. The middle pharynx constrictor and the hyoglossus muscles are medial to this segment of the nerve, while stylohyoid muscle,
submandibular gland, superior cervical aponeurosis, subcutaneous fat, platysma, and
SC
skin are lateral (Fig. 5). During its course, this segment has close relationships with
the lingual artery. The mean length of the horizontal segment in our specimens was
M AN U
34.6 mm (range: 25-54 mm) and the mean thickness was 3.3 mm (range: 1.9-4 mm).
Ascending segment
This segment begins at the edge of the mylohyoid muscle, where the nerve reaches the inferior surface of the tongue (Fig. 6). Following a course that brings it upward to
TE D
the tip and the dorsal surface of the tongue, it runs between the mylohyoid muscle, located laterally, and the hyoglossus and genioglossus muscles, sited medially (Fig. 7). During its course, the nerve is located inferiorly to the Wharton duct and the
EP
lingual artery. This segment ends in 2-5 main terminal branches to the muscle bellies. In our specimens mean length of the ascending segment was 5.7 mm (range: 3.6-19
AC C
mm) and mean thickness 2.4 mm (range: 1-3.5 mm).
Anastomoses with other nerves The hypoglossal nerve gives several collateral branches during its course. Among them some are motor branches for geniohyoid muscle, and anastomotic branches that connect to the vagus, the lingual branch of the trigeminal nerve and the first cervical
ACCEPTED MANUSCRIPT
nerves, forming a neural loop referred to as the ansa cervicalis or ansa hypoglossi, from which leaving fibers reach infrahyoid muscles. The extracranial part of the hypoglossal nerve may receive one or few communicating
RI PT
branches from the vagus nerve. Von Luschka(12) was the first to describe a thin lingual branch of the vagus nerve, arising from its pharyngeal branch and joining the
hypoglossal nerve. Although the functional significance of this anastomosis remains
SC
uncertain, it could provide proprioceptive innervation to the striated muscles supplied by the hypoglossal nerve(7).
M AN U
Furthermore, in agreement with previous studies(2, 6, 18, 24), we found in all specimens intralingual and extralingual neural connections between hypoglossal and lingual nerves. These connections were alongside the region where the hypoglossal nerve branched to the hyoglossus muscle.
Concerning the ansa cervicalis, it is composed of two roots: superior and inferior. The
TE D
superior root (descending branch of XII) leaves the hypoglossal trunk on a level with the upper carotid region, where the descending XII becomes horizontal when it passes between the internal jugular vein and the internal carotid artery (Fig. 8). The inferior
AC C
EP
root is instead formed by fibers from spinal nerves C2 and C3.
DISCUSSION
In the last two decades, several Authors have described the microsurgical anatomy of the hypoglossal nerve(1, 5, 22, 25). Nevertheless, so far, no one has systematically followed and described in detail the entire course of the nerve from its exit zone in the medulla oblongata to the tongue.
ACCEPTED MANUSCRIPT
The lower cranial nerves, being very close to each other at the skull base, may be involved in syndromes related to meningiomas, glomus tumors, schwannomas, and other tumors. The Collet syndrome is due to large space-occupying lesions that
RI PT
involve the ninth, tenth, eleventh, and twelfth nerves. Consequently, it causes paralysis of stylopharyngeal muscle, loss of taste in the circumvallate and foliate
papillae, impairment or abolishment of touch, temperature, and deep sensation at the
SC
base of the tongue, the auditory tube, the pharynx, and the tonsil. Disturbances of speech and swallowing, pain to the ear, eye angle of jaw, and into the tonsil region are
M AN U
reported as well. The Villaret syndrome presents sympathetic paresis or paralysis if the sympathetic trunk is involved in addition to the caudal nerves, producing also ptosis, miosis and enophthalmos. Intramedullary tumors and hemorrhages may also result in very complex syndromes, such as Schmidt, Jackson, and Tapia syndromes. Lesions of the nerve along its extracranial course in the neck may produce the same
TE D
signs, with paralysis of the tongue. Therefore, in order to preserve the hypoglossal nerve during surgery, it is of primary importance to follow the nerve through anatomical constant landmarks. Since such anatomical landmarks have never been
EP
described before, the aim of our study is to detail the course of the nerve along with its anatomical relationships.
AC C
In the literature, there are very few reports about unilateral hypoglossal nerve palsy and tongue fasciculation caused by neurovascular conflict(16, 20, 23). The cranial nerve dysfunction syndrome occurs because the nerve is particularly vulnerable to continuous pulsatile pressure at the root entrance zone, where there is also the transition between the peripheral and central myelin in the brainstem. Indeed, because of the strict relationship between the cisternal segment, VA and PICA, a conflict with the vessels that may deviate perpendicularly or indent the nerve, although rare, is
ACCEPTED MANUSCRIPT
possible. Concerning vascular compression syndrome of the 12th cranial nerve, it can cause a hemilingual spasm. It is a very rare event characterized by intermittent paroxysmal involuntary contractions of half of the tongue muscles. In the pertinent
RI PT
literature there is only one report describing a vascular contact/compression along cranial nerve XII at the lower brainstem by a large tortuous vertebral artery causing this syndrome. A 52-year-old man had lower face muscle twitching and tongue
SC
spasms, which worsened with talking, chewing, or emotional stress and magnetic
resonance imaging revealed a compressive vessel along the hypoglossal nerve. It was
M AN U
treated with interposition of Teflon between the artery and the nerve and postoperatively the abnormal spontaneous tongue fasciculation immediately disappeared(16).
The hypoglossal nerve emerges from the medulla oblongata, between the pyramid and the olive. The uppermost radicular filaments arise 1.5 – 5 mm below the bulbopontine
TE D
sulcus and an average of 8.4 filaments are present altogether. They usually unite to form either two or three, seldom even four, large bundles, which run intracisternally for an average length of 12.7 mm. Then, they reach the dural pore of the hypoglossal
EP
canal usually coursing dorsally to the vertebral artery. Rarely the whole nerve runs ventrally to the artery, but more frequently some fiber bundles may run ventrally and
AC C
sometimes they stretch out their shape by looping around the VA or the PICA. The nerve or its fibers can pass through a buttonhole of the VA, too. When the vertebral artery is longer or tortuous, it dislocates the rootlets of the hypoglossal nerve dorsally. The dislocation of rootlets might be so posterior that they intermingle with the fibers of the other caudal cranial nerves. The relationships of the nerve with the PICA can vary markedly, because the PICA has with the cranial nerves the most complex relationships than any other artery. The PICA can arise either rostral or caudal or, in
ACCEPTED MANUSCRIPT
majority of cases, at the same level of the rootlets of the nerve, and very often the rootlets of the hypoglossal nerve embrace the origin and initial segment of the PICA. The PICA usually origins anteriorly to the hypoglossal rootlets if the VA is anterior to
RI PT
the olive, while the PICA origins posteriorly or at level of the rootlets of the nerve if the VA courses lateral to the olive, therefore the rootlets are stretched posteriorly. The initial segment of PICA has usually a very variable course, it can loop upward,
SC
downward, or laterally in front of the rootlets, passing posteriorly, between or around
them and this anatomical aspect is extremely important in managing aneurysms
M AN U
located in this area. Nevertheless, isolated paralysis of the nerve is rarely reported in the main literature(19). According to neurological studies, unilateral paralysis of the hypoglossal nerve is not clinically relevant, and, therefore, it is not reported. The pertinent literature reports that 7-26 rootlets leave the preolivary sulcus; the upper fiber bundle is 7-24 mm in length, while the inferior bundle measure 5.5-18 mm in
TE D
length. According to Lang(8), in 65% of cases the nerve roots are grouped in two trunks running laterally towards the dural pore which is duplicated. The average distance between the pores is 0.5-9 mm, although, in all cases described, the two roots
EP
unite within the hypoglossal canal. Additionally, Lang and Reiter reported more than one dural entrance in 14.8% on the right side and in 27.6% on the left side(9). As
AC C
regards the hypoglossal canal, they described the canal as divided in two in 12.7% of the cases on the right side, and in 25% on the left one(9). According to our observations, in the right side of one specimen (5% of cases) the two separated nerves fused 3 mm after exiting the canal, while in 35% of cases, the fibers of the hypoglossal nerve fuse into a single trunk before the dural pore. Further, in the examined cases, the canal length was between 6.1 mm and 14.1 mm in length, and it runs slantwise forming an angle approximately of 45° with the midsagittal plane.
ACCEPTED MANUSCRIPT
Inside the canal, dura and arachnoid envelope the nerve for two thirds of the length, while a venous plexus surrounds the nerve for the full length. As far as we are concerned, this venous plexus was never described in detail before. Moreover, in one
RI PT
specimen (5%) the hypoglossal nerve was within the canal divided in two trunks running singularly.
As described by Lang, once exited from the skull base, the hypoglossal nerve runs on
SC
the medial surface of the internal jugular vein and on the lateral surface of the vagus
nerve in 92% of cases(8) and, then, it curves around the occipital artery, covered by
M AN U
the sternocleidomastoid muscle. Successively, the hypoglossal nerve runs first on the lateral and then on the anterior surface of the external carotid artery. In 8% of cases, the nerve curves around the external carotid artery where the occipital artery arises, and then it takes a lateral course on the outer surface of the external carotid artery and posterior to the jugular vein.
TE D
After its exit from the canal, the nerve connects with the ventral branches of C1 and C2 and the ventral ansa between the two branches. Hypoglossal nerve and ansa
EP
measured 15-45 mm.
AC C
CONCLUSIONS
We propose a new 5-segment classification of the hypoglossal nerve. This exhaustive anatomical analysis, which considers the entire intra- and extra-cranial course of the nerve along with its relationships with surrounding structures, is valid and clinically and surgically oriented when considering the classical microscopic approaches. The present study could be useful to explain, segment by segment along its intra- and extracranial course, the pathogenic mechanisms of nerve injury caused by lesions that
ACCEPTED MANUSCRIPT
involve the nerve. The neurosurgeon must know this information when approaching the posterior cranial fossa, the cerebellopontine angle and the neck in general to avoid injuring the XIIth nerve.
RI PT
Finally, in the present study we describe a new perspective of the hypoglossal canal
SC
with the venous plexus inside, surrounding the canalar segment of the nerve.
AKNOWLEDGEMENTS
M AN U
The authors would like to thank Dr. Santolo Cozzolino, Director of Center of Biotechnologies, “A. Cardarelli” Hospital, Napoli, Italy, for his highly qualified cooperation to produce the anatomical dissection.
TE D
FIGURE LEGENDS
Figure 1: Microsurgical microscopic view of the origin of the hypoglossal nerve until its entry into the canal. Different rootlets merged into three trunks. On the right the 3-
EP
dimensional reconstruction of the head position for the approach. sXII: superior rootlets of XIIth cn; iXII: inferior rootlets of XIIth cn; VA: vertebral
AC C
artery; PICA: posterior inferior cerebellar artery; dp: dural pore Figure 2: Microsurgical microscopic view of the hypoglossal nerve entering in the
canal after passed through the dural pore. In this specimen is evident a perforation of the dura mater through two separate pores and a division in two different canals with the two nerves fusing after the extracranial exit. Relationships with vetebral and posterior inferior cerebellar arteries are shown. On the right the 3-dimensional reconstruction of the head position for the approach.
ACCEPTED MANUSCRIPT
sXII: superior rootlets of XIIth cn; iXII: inferior rootlets of XIIth cn; VA: vertebral artery; PICA: posterior inferior cerebellar artery; dp: dural pore Figure 3: Endoscopic transcranial closed view of the canalar segment; particular of
RI PT
the small veins piercing in the bone surface several tiny channels for the drainage into the jugular bulb
Figure 4: Photograph showing the descending segment of the hypoglossal nerve in
SC
the portion where it runs laterally to stylohyoid muscle and the posterior belly of the digastric muscle.
M AN U
Figure 5: Photograph showing the horizontal segment of the hypoglossal nerve, at its origin from the previous one, passing inferiorly to the middle tendon of the digastric muscle; stylohyoid muscle, submandibular gland and superior cervical aponeurosis are located laterally.
Figure 6: Photograph showing the ascending segment of the hypoglossal nerve where
tongue.
TE D
it begins at the edge of the mylohyod muscle reaching the inferior surface of the
Figure 7: Photograph showing the ascending segment of the hypoglossal nerve where
EP
it ends up on the underside of the tongue.
Figure 8: Photograph showing the transition between horizontal and ascending
AC C
segment; the superior root of the ansa hypoglossi leaves the hypoglossal trunk on a level with the upper carotid region.
ACCEPTED MANUSCRIPT
REFERENCES 1.
Bademci G, Yasargil MG: Microsurgical anatomy of the hypoglossal nerve. Journal of clinical neuroscience : official journal of the Neurosurgical Society of Australasia 13:841-847, 2006. Candir N, Develi S, Kilir C, Satar B, Yazar F: Distribution of the hypoglossal
RI PT
2.
nerve at the base of the tongue and its clinical importance in radiofrequency ablation therapy. Turk J Med Sci 44:427-431, 2014. 3.
Caruso RD, Rosenbaum AE, Chang JK, Joy SE: Craniocervical junction venous anatomy on enhanced MR images: the suboccipital cavernous sinus.
4.
SC
AJNR American journal of neuroradiology 20:1127-1131, 1999.
Cheng VS, Schultz MD: Unilateral hypoglossal nerve atrophy as a late
M AN U
complication of radiation therapy ofhead and neck carcinoma: a report of four cases and a review of the literature on peripheral and cranial nerve damages after radiation therapy. Cancer 35:1537-1544, 1975. 5.
Curto FS, Jr., Suarez F, Kornblut AD: The extracranial hypoglossal nerve: 112 cadaver dissection. Ear Nose Throat J 59:94-99, 1980.
6.
Fitzgerald MJ, Law ME: The peripheral connexions between the lingual and hypoglossal nerves. J Anat 92:178-188, 1958.
Landois L, Brubaker AP, Eshner AA: Text-book of human physiology,
TE D
7.
including histology and microscopical anatomy, with especial reference to the practice of medicine. Philadelphia,, P. Blakiston's son & co., 1904. 8.
Lang J: Skull base and related structures: Atlas of clinical anatomy. Stuttgart,
9.
EP
Schattauer Verlag, 1995. Lang J, Reiter U: [Intracisternal length of cranial nerves 7-12].
AC C
Neurochirurgia 28:153-157, 1985. 10.
Leblanc A: The Cranial Nerves Anatomy Imaging Vascularisation. Berlin,
Heidelberg, Springer Berlin Heidelberg,, 1995, p 1 online resource.
11.
Loh C, Maya MM, Go JL: Cranial nerve XII: the hypoglossal nerve. Semin Ultrasound CT MR 23:256-265, 2002.
12.
Luschka Hv: Die Anatomie des menschlichen Kopfes. Tubingen,, H. Laupp'schen Buchhandlung, 1867.
13.
Macedo TF, Gow PJ, Heap SW, Wallis WE: Bilateral hypoglossal nerve palsy due to vertical subluxation of the odontoid process in rheumatoid arthritis. Br J Rheumatol 27:317-320, 1988.
ACCEPTED MANUSCRIPT
14.
Mattos JP, Santos MJ, Zullo JF, Joaquim AF, Chaddad-Neto F, Oliveira E: Dissection technique for the study of the cerebral sulci, gyri and ventricles. Arquivos de neuro-psiquiatria 66:282-287, 2008.
15.
Nagai K, Sakuramoto C, Goto F: Unilateral hypoglossal nerve paralysis
RI PT
following the use of the laryngeal mask airway. Anaesthesia 49:603-604, 1994. 16.
Osburn LL, Moller AR, Bhatt JR, Cohen-Gadol AA: Hemilingual spasm: defining a new entity, its electrophysiological correlates and surgical treatment through microvascular decompression. Neurosurgery 67:192-195; discussion
17.
SC
196, 2010.
Perneczky A, R R: Keyhole Approaches in Neurosurgery. Springer-Verlag,
18.
M AN U
2008.
Saigusa H, Tanuma K, Yamashita K, Saigusa M, Niimi S: Nerve fiber analysis for the lingual nerve of the human adult subjects. Surg Radiol Anat 28:59-65, 2006.
19.
Scotti G, Melancon D, Olivier A: Hypoglossal paralysis due to compression by a tortuous internal carotid artery in the neck. Neuroradiology 14:263-265, 1978.
Shiozawa Z, Koike G, Seguchi K, Shindo K, Sugita K: Unilateral tongue
TE D
20.
atrophy due to an enlarged emissary vein in the hypoglossal canal. Surgical neurology 45:477-479, 1996. 21.
Stewart A, Lindsay WA: Bilateral hypoglossal nerve injury following the use
22.
EP
of the laryngeal mask airway. Anaesthesia 57:264-265, 2002. Thompson EO, Smoker WR: Hypoglossal nerve palsy: a segmental approach.
AC C
Radiographics 14:939-958, 1994. 23.
Toldo I, Manara R, Sartori S, Suppiej A, Drigo P: Unilateral hypoglossal nerve palsy due to neurovascular conflict in a child. Brain Dev 31:461-464, 2009.
24.
Toure G, Bicchieray L, Selva J, Vacher C: The intra-lingual course of the nerves of the tongue. Surg Radiol Anat 27:297-302, 2005.
25.
Yousry I, Moriggl B, Schmid UD, Wiesman M, Fesl G, Bruckmann H, Naidich TP, Yousry TA: Detailed anatomy of the intracranial segment of the hypoglossal nerve: neurovascular relationships and landmarks on magnetic resonance imaging sequences. Journal of neurosurgery 96:1113-1122, 2002.
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
ACCEPTED MANUSCRIPT
TABLE
Length (mm)
Thickness (mm)
SEGMENT
Range
Mean
Range
Cisternal
8 - 15
12.7
0.3 - 0.6
0.4
Canalar
9.5 - 16
13
1.3 - 3
2
Descending
48 - 89
65
2-4
3.2
Horizontal
25 - 54
34.6
1.9 - 4
3.3
Ascending
3.6 - 19
5.7
1 - 3.5
2.4
RI PT
SC
M AN U
EP
TE D
Table 1. Summary of length and thickness of each hypoglossal segment.
AC C
Mean
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
ACCEPTED MANUSCRIPT
EP
TE D
M AN U
SC
RI PT
Few anatomic studies concerning the hypoglossal nerve have been reported. We dissected 10 formalin-fixed adult human cadaveric heads (20 specimens). Classification in 5 segments: cisternal, canalar, descending, horizontal, ascending. A new perspective of the hypoglossal canal is proposed. The venous plexus surrounding the canalar segment of the nerve is well described.
AC C
• • • • •
S1878-8750(17)31733-3
DOI:
10.1016/j.wneu.2017.10.006
Reference:
WNEU 6659
To appear in:
World Neurosurgery
Received Date: 29 April 2017 Revised Date:
30 September 2017
Accepted Date: 3 October 2017
Please cite this article as: Iaconetta G, Solari D, Villa A, Castaldo C, Gerardi RM, Califano G, Montagnani S, Cappabianca P, The Hypoglossal Nerve: Anatomical Study Of Its Entire Course, World Neurosurgery (2017), doi: 10.1016/j.wneu.2017.10.006. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
THE HYPOGLOSSAL NERVE: ANATOMICAL STUDY OF ITS ENTIRE COURSE
RI PT
Giorgio Iaconetta1, Domenico Solari2, Alessandro Villa2, Clotilde Castaldo3, Rosa Maria Gerardi2, Gianluigi Califano2, Stefania Montagnani3, Paolo Cappabianca2.
Department of Medicine and Surgery, Division of Neurosurgery, Università degli Studi di
SC
1
Salerno, Salerno, Italy.
Department of Neurosciences and Reproductive and Odontostomatological Sciences,
M AN U
2
Division of Neurosurgery, Università degli Studi di Napoli Federico II, Napoli, Italy. 3
Department of Public Health, Division of Anatomy, Università degli Studi di Napoli
EP
TE D
Federico II, Napoli, Italy.
Corresponding Author:
AC C
Alessandro Villa, M.D.
Department of Neurosciences and Reproductive and Odontostomatological Sciences Division of Neurosurgery Università degli Studi di Napoli Federico II Via Pansini 5, 80131 Napoli, Italy Tel +39 081 7462490 e-mail: [email protected]
ACCEPTED MANUSCRIPT
ABSTRACT Object: Only a few anatomic studies concerning the entire course of the hypoglossal nerve (cranial nerve XII) have been reported. The purpose of the present study is to
RI PT
analyze all the relationships of the XII nerve with the surrounding structures from the brainstem to the tongue through a microscopic perspective. A comprehensive
anatomically and clinically oriented classification of its different segments is
SC
proposed.
Methods: Ten formalin-fixed adult human cadaveric heads (20 sides) were dissected
M AN U
with the aim to explore the entire course of the XII cranial nerve via the lateral suboccipital, the far lateral partial or total transcondilar routes. Different segments of the nerve were then identified, based on the hypoglossal course and its relationship with surrounding structures. Measurements of every portion of the nerve were taken in all specimens during the dissecting process.
TE D
Results: The hypoglossal nerve was divided into five segments: cisternal, canalar, descending, horizontal, and ascending. Detailed and comprehensive examination of the basic anatomical relationships through the view of different transcranial, and
EP
endoscope-assisted approaches was achieved. A new perspective of the hypoglossal canal is proposed and the venous plexus surrounding the canalar segment of the nerve
AC C
is described in detail.
Conclusion: The classification of five segments for the hypoglossal nerve seems anatomically valid and it is surgically oriented with respect to all surgical approaches. The precise knowledge of the relationships with the surrounding structures may help to prevent some complications during surgery and it is useful to explain, segment by segment, the pathogenic mechanisms for nerve injuries that are evidenced by lesions that exist along the entire intra- and extracranial course.
ACCEPTED MANUSCRIPT
KEY WORDS: hypoglossal nerve, XII, 12th, cranial nerves, hypoglossal canal,
RI PT
venous plexus.
SC
ABBREVIATIONS: REZ: root exit zone; PICA: posterior inferior cerebellar artery;
SHM: stylohyoid muscle.
INTRODUCTION
M AN U
VA: vertebral artery; SPM: stylopharyngeal muscle; SGM: styloglossus muscle;
TE D
During the past two decades, advances in the field of surgical microanatomy have allowed important progress in the development of surgical techniques in order to improve the excision of skull base lesions. Knowledge of the detailed anatomy and
EP
pathway of the hypoglossal nerve is critical for the management of lesions located in the posterior cranial fossa. Several pathological processes such as infections,
AC C
inflammatory diseases, traumas, and skull base tumors as neurinomas, metastasis, glomus jugulare masses may damage the 12th cranial nerve, which is the motor supply of the tongue, leading to its paralysis of both extrinsic and intrinsic muscles. Furthermore, this nerve has also an important role in respiration and swallowing, and a lesion, if unilateral(4, 15), does not cause severe restriction in function, however, if bilateral, may cause severe swallowing disturbances, dysarthria and respiratory difficulties due to airway obstruction(13, 21).
ACCEPTED MANUSCRIPT
In order to understand the pathology of the hypoglossal nerve and its relative treatment, the knowledge of the entire course of the nerve is extremely important. The anatomical relationships with the surrounding neurovascular structures and muscles,
RI PT
as well as having some constant landmarks to follow, are essential in surgical procedures when the preservation of the nerve is required. The nerve can be divided into
two
main
parts:
intracranial
and
extracranial.
Neurosurgeons,
SC
otorhinolaryngologists, maxillofacial surgeons, deal with the pathology of the
different segments of the nerve during surgical treatments to posterior fossa, neck, or
M AN U
mouth.
To our knowledge, very few articles are reported in the pertinent literature regarding the microsurgical anatomy of the hypoglossal nerve in its entire course. In the present anatomical study we describe our observations on the relationships of the nerve with the surrounding structures, from its exit zone on the medulla oblongata,
TE D
to its ending on the muscles of the tongue, describing all landmarks we have
EP
encountered while performing the dissections.
MATERIAL AND METHODS
AC C
Anatomic dissections were performed at the Center of Biotechnology of the “Antonio Cardarelli Hospital” in Napoli on 10 formalin-fixed adult human cadaveric heads (20 sides), whose arterial and venous system had been injected with red and blue latex, respectively. The specimens were from 7 men and from 3 women, aging from 59 to 85 years (mean age 72 years) at the time of death. Cadaveric dissections and nerve measurements took place under surgical microscope (Carl Zeiss®, Oberkochen, Germany) guidance while recording on DVDs.
ACCEPTED MANUSCRIPT
Additionally, a rigid endoscope 4 mm in diameter, 18 cm in length, with a 0-degree and 30-degree lens (Karl Storz, Tuttlingen, Germany) was used during dissections. We used OsiriX Lite®, a freeware software and user friendly, with its 3D volume
RI PT
rendering methods to obtain the 3-dimensional reconstruction of the head position for each approach.
With heads positioned as during surgery in operating room we performed the lateral
SC
suboccipital, the far lateral partial or total transcondilar, without or with removal of the lateral posterior arch of the atlas, surgical approaches according to the well-known
M AN U
techniques. (17)(16)(15)
Additionally, with the aim to expose the nerve in its entirety course we transected the mandibule and drilled all the petrous bone and the posterior wall of the hypoglossal canal. The extracranial course of the nerve with its terminating branches to muscles and tongue were exposed dissecting the neck and mouth floor. Length and thickness
TE D
of each segment of the nerve were measured with millimeter paper (see Table 1).
Transcranial approaches
EP
The lateral suboccipital approach was performed through a hockey-stick retrosigmoid exposure extending superomedial from the mastoid process along the superior nuchal
AC C
line to the inion and downward in the midline. This approach allows exposing our area of interest, located anteriorly to the brainstem toward the jugular foramen or cerebellopontine angle with the aim to expose the nerve running into it. The exposure allows performing a suboccipital craniectomy and laminectomy of the axis with the aim to clearly identify and follow the hypoglossal course. A more complete view of this region came combining the suboccipital approach with the far lateral approach with the aim to obtain a larger lateral view. Indeed, its
ACCEPTED MANUSCRIPT
supracondilar extension allows reaching the hypoglossal canal in its medial aspect, while the further drilling of the condyles enlarges the anatomical view of the
RI PT
surrounding neurovascular structures.
Neck dissection
The exposition of the extracranial course of the hypoglossal nerve took place via a
SC
transcervical approach; through a submandibular incision extending from the mastoid tip to the symphysis menti extended downward across the sternocleidomastoid
M AN U
muscle. Its inferior extension was carried from the midpoint of the submandibular incision across the sternocleidomastoid muscle. The transection of the mandibule helped to easily follow the hypoglossal course. The dissection went along the anterior border of the sternocleidomastoid muscle and between the carotid sheath, laterally and the esophagus and trachea, medially and it implied the retraction of prevertebral
TE D
muscles and fascia. At this point, deeper neurovascular structures as the superior thyroid arteries, external and internal laryngeal nerve and lingual artery as well as extrinsic muscles of the tongue were dissected in order to identify the hypoglossal
AC C
EP
course and their relationships.
RESULTS
According to its course and considering the relationships with surrounding structures, we have divided the hypoglossal nerve into five segments: − cisternal, − canalar, − descending,
ACCEPTED MANUSCRIPT
− horizontal, − ascending.
RI PT
Cisternal segment The nucleus of the 12th cranial nerve is located at the posterior aspect of the medulla
oblongata. Previous studies have shown that the nucleus extends for 15-18 mm in
SC
cranio-caudal direction, and it is represented by a focal bulge, named “hypoglossal
trigone”, under the floor of the fourth ventricle. This part of the nerve is
M AN U
intramedullary, traversing the medulla oblongata. From the trigone, the roots run towards the root exit zone (REZ), located at the preolivary sulcus, between the olive and the pyramid(10). The radicular fibers - studied with the help of additional fixation(14) by others Authors(11) - pass medial to the olive and lateral to the medial longitudinal fasciculus, medial lemniscus, accessory olivary nucleus and pyramidal
TE D
tract giving rise to the cisternal segment which ends at the dural pore(10). The rootlets emerging from the preolivary sulcus in our specimens range from 6 to 14 (mean 8.4) and they merge into 2-4 trunks (3 in 12/20, 60% of our specimens) (Fig. 1). They
EP
enter the canal by perforating the dura mater through one, two or three separate pores (Fig. 2). The mean total length of the cisternal segment in our specimens is 12.7 mm
AC C
(range: 8-15 mm) and the mean width of the bundles is 0.4 mm (range: 0.3-0.6 mm). The bundles, within the premedullary cistern, course anterolaterally, between the posterior inferior cerebellar artery (PICA) and the vertebral artery (VA), with the VA anterior to the nerve in nearly 93% of cases and posteriorly located only in 2.9%, according to the literature and as described first by Luschka in 1867(12). The PICA, on the contrary, courses anterior to the nerve in 5.9% of cases. A direct relationship between the hypoglossal nerve, VA and PICA has been previously documented in
ACCEPTED MANUSCRIPT
reports describing how these arteries may compress, distort, displace or stretch the nerve root bundles(25). In our specimens, we found all the bundles coursing posteriorly to the vertebral artery and, in some cases (25%), a cranial rootlet of the
RI PT
12th, longer than others, enveloping the PICA before the entry into the canal (Fig. 2). According with the previous studies, we observed an incredible tortuous course of the
SC
nerve between VA and PICA.
Canalar segment
M AN U
The hypoglossal canal is a bony passage containing the canalar segment of the hypoglossal nerve, a branch of the ascending pharyngeal artery, and a venous plexus which has previously been considered an anterior condylar vein(3). The hypoglossal canal extends from the posterior fossa to the nasopharyngeal carotid space, running anteriorly from an infero-medial direction to reach a supero-lateral
TE D
location. It is surrounded by the occipital condyles inferiorly, the jugular foramen and the jugular process of the occipital bone laterally and the sphenoid part of the clivus supero-medially. Specifically, this canal is closely related with the jugular foramen,
EP
which lies medial, inferior and posterior.
The canalar segment begins where the nerve trunks pass through the dural pore to
AC C
enter the hypoglossal canal (Fig. 2). The nerve is covered by arachnoid and dural sheaths along approximately two thirds of the length of the canal, while a venous plexus surrounds the canalar segment for its entire course. To the best of our knowledge, there are no exhaustive descriptions of this plexus in the literature. The venous plexus is a sort of tube, occupying the canal from the entrance to the exit, and sealed at the inner and outer extremities, corresponding to the entrance and the exit of the nerve from the canal. The plexus fills the space between bone and nerve, with the
ACCEPTED MANUSCRIPT
interior wall that is in contact with the nerve, and the external one that is in contact with the periosteum lining the canal. The plexus drains within the final portion of the sigmoid sinus, and within the jugular bulb through small veins piercing in the bone
RI PT
surface several tiny channels. Such small openings have been documented by endoscope-assisted approach after drilling of the posterior wall of the hypoglossal canal (Fig. 3).
SC
The mean length of the canal in our specimens was 13 mm (range: 9.5-16 mm), while
the mean width was 2 mm (range: 1.3-3). In one specimen, an inner perpendicular
M AN U
bony wall divided the canal in two different canals, and two nerves, fusing 3 mm after the extracranial exit, occupied each resulting canal (Fig. 2).
Descending segment
At its exit from the neurocranium, the hypoglossal nerve descends in the neck. At
TE D
first, it lies underneath the sternocleidomastoid muscle, between the small rectus muscle of the head and the internal carotid artery, and medial to the glossopharyngeal, vagus and accessory nerves. Then, running between the internal carotid and the
EP
jugular vein, it reaches the stylian muscles bundle, the stylopharyngeal (SPM), the styloglossus (SGM), and the stylohyoid (SHM) muscles. The nerve is lateral to the
AC C
SPM and SGM, and lateral to SHM and the posterior belly of the digastric muscle (Fig. 4). It crosses, then, the lateral surface of the external carotid artery and reaches the anterior margin of the sternocleidomastoid muscle, which is the inferior limit of this segment.
The mean length of this segment in our specimens was 65 mm (range: 48-89 mm) and the mean thickness was 3.2 mm (range: 2-4 mm).
ACCEPTED MANUSCRIPT
Horizontal segment The horizontal segment of the nerve runs transversally, passing between the great horn of the hyoid bone, which is located inferiorly, and the middle tendon of the
RI PT
digastric muscle, which is located superiorly. The middle pharynx constrictor and the hyoglossus muscles are medial to this segment of the nerve, while stylohyoid muscle,
submandibular gland, superior cervical aponeurosis, subcutaneous fat, platysma, and
SC
skin are lateral (Fig. 5). During its course, this segment has close relationships with
the lingual artery. The mean length of the horizontal segment in our specimens was
M AN U
34.6 mm (range: 25-54 mm) and the mean thickness was 3.3 mm (range: 1.9-4 mm).
Ascending segment
This segment begins at the edge of the mylohyoid muscle, where the nerve reaches the inferior surface of the tongue (Fig. 6). Following a course that brings it upward to
TE D
the tip and the dorsal surface of the tongue, it runs between the mylohyoid muscle, located laterally, and the hyoglossus and genioglossus muscles, sited medially (Fig. 7). During its course, the nerve is located inferiorly to the Wharton duct and the
EP
lingual artery. This segment ends in 2-5 main terminal branches to the muscle bellies. In our specimens mean length of the ascending segment was 5.7 mm (range: 3.6-19
AC C
mm) and mean thickness 2.4 mm (range: 1-3.5 mm).
Anastomoses with other nerves The hypoglossal nerve gives several collateral branches during its course. Among them some are motor branches for geniohyoid muscle, and anastomotic branches that connect to the vagus, the lingual branch of the trigeminal nerve and the first cervical
ACCEPTED MANUSCRIPT
nerves, forming a neural loop referred to as the ansa cervicalis or ansa hypoglossi, from which leaving fibers reach infrahyoid muscles. The extracranial part of the hypoglossal nerve may receive one or few communicating
RI PT
branches from the vagus nerve. Von Luschka(12) was the first to describe a thin lingual branch of the vagus nerve, arising from its pharyngeal branch and joining the
hypoglossal nerve. Although the functional significance of this anastomosis remains
SC
uncertain, it could provide proprioceptive innervation to the striated muscles supplied by the hypoglossal nerve(7).
M AN U
Furthermore, in agreement with previous studies(2, 6, 18, 24), we found in all specimens intralingual and extralingual neural connections between hypoglossal and lingual nerves. These connections were alongside the region where the hypoglossal nerve branched to the hyoglossus muscle.
Concerning the ansa cervicalis, it is composed of two roots: superior and inferior. The
TE D
superior root (descending branch of XII) leaves the hypoglossal trunk on a level with the upper carotid region, where the descending XII becomes horizontal when it passes between the internal jugular vein and the internal carotid artery (Fig. 8). The inferior
AC C
EP
root is instead formed by fibers from spinal nerves C2 and C3.
DISCUSSION
In the last two decades, several Authors have described the microsurgical anatomy of the hypoglossal nerve(1, 5, 22, 25). Nevertheless, so far, no one has systematically followed and described in detail the entire course of the nerve from its exit zone in the medulla oblongata to the tongue.
ACCEPTED MANUSCRIPT
The lower cranial nerves, being very close to each other at the skull base, may be involved in syndromes related to meningiomas, glomus tumors, schwannomas, and other tumors. The Collet syndrome is due to large space-occupying lesions that
RI PT
involve the ninth, tenth, eleventh, and twelfth nerves. Consequently, it causes paralysis of stylopharyngeal muscle, loss of taste in the circumvallate and foliate
papillae, impairment or abolishment of touch, temperature, and deep sensation at the
SC
base of the tongue, the auditory tube, the pharynx, and the tonsil. Disturbances of speech and swallowing, pain to the ear, eye angle of jaw, and into the tonsil region are
M AN U
reported as well. The Villaret syndrome presents sympathetic paresis or paralysis if the sympathetic trunk is involved in addition to the caudal nerves, producing also ptosis, miosis and enophthalmos. Intramedullary tumors and hemorrhages may also result in very complex syndromes, such as Schmidt, Jackson, and Tapia syndromes. Lesions of the nerve along its extracranial course in the neck may produce the same
TE D
signs, with paralysis of the tongue. Therefore, in order to preserve the hypoglossal nerve during surgery, it is of primary importance to follow the nerve through anatomical constant landmarks. Since such anatomical landmarks have never been
EP
described before, the aim of our study is to detail the course of the nerve along with its anatomical relationships.
AC C
In the literature, there are very few reports about unilateral hypoglossal nerve palsy and tongue fasciculation caused by neurovascular conflict(16, 20, 23). The cranial nerve dysfunction syndrome occurs because the nerve is particularly vulnerable to continuous pulsatile pressure at the root entrance zone, where there is also the transition between the peripheral and central myelin in the brainstem. Indeed, because of the strict relationship between the cisternal segment, VA and PICA, a conflict with the vessels that may deviate perpendicularly or indent the nerve, although rare, is
ACCEPTED MANUSCRIPT
possible. Concerning vascular compression syndrome of the 12th cranial nerve, it can cause a hemilingual spasm. It is a very rare event characterized by intermittent paroxysmal involuntary contractions of half of the tongue muscles. In the pertinent
RI PT
literature there is only one report describing a vascular contact/compression along cranial nerve XII at the lower brainstem by a large tortuous vertebral artery causing this syndrome. A 52-year-old man had lower face muscle twitching and tongue
SC
spasms, which worsened with talking, chewing, or emotional stress and magnetic
resonance imaging revealed a compressive vessel along the hypoglossal nerve. It was
M AN U
treated with interposition of Teflon between the artery and the nerve and postoperatively the abnormal spontaneous tongue fasciculation immediately disappeared(16).
The hypoglossal nerve emerges from the medulla oblongata, between the pyramid and the olive. The uppermost radicular filaments arise 1.5 – 5 mm below the bulbopontine
TE D
sulcus and an average of 8.4 filaments are present altogether. They usually unite to form either two or three, seldom even four, large bundles, which run intracisternally for an average length of 12.7 mm. Then, they reach the dural pore of the hypoglossal
EP
canal usually coursing dorsally to the vertebral artery. Rarely the whole nerve runs ventrally to the artery, but more frequently some fiber bundles may run ventrally and
AC C
sometimes they stretch out their shape by looping around the VA or the PICA. The nerve or its fibers can pass through a buttonhole of the VA, too. When the vertebral artery is longer or tortuous, it dislocates the rootlets of the hypoglossal nerve dorsally. The dislocation of rootlets might be so posterior that they intermingle with the fibers of the other caudal cranial nerves. The relationships of the nerve with the PICA can vary markedly, because the PICA has with the cranial nerves the most complex relationships than any other artery. The PICA can arise either rostral or caudal or, in
ACCEPTED MANUSCRIPT
majority of cases, at the same level of the rootlets of the nerve, and very often the rootlets of the hypoglossal nerve embrace the origin and initial segment of the PICA. The PICA usually origins anteriorly to the hypoglossal rootlets if the VA is anterior to
RI PT
the olive, while the PICA origins posteriorly or at level of the rootlets of the nerve if the VA courses lateral to the olive, therefore the rootlets are stretched posteriorly. The initial segment of PICA has usually a very variable course, it can loop upward,
SC
downward, or laterally in front of the rootlets, passing posteriorly, between or around
them and this anatomical aspect is extremely important in managing aneurysms
M AN U
located in this area. Nevertheless, isolated paralysis of the nerve is rarely reported in the main literature(19). According to neurological studies, unilateral paralysis of the hypoglossal nerve is not clinically relevant, and, therefore, it is not reported. The pertinent literature reports that 7-26 rootlets leave the preolivary sulcus; the upper fiber bundle is 7-24 mm in length, while the inferior bundle measure 5.5-18 mm in
TE D
length. According to Lang(8), in 65% of cases the nerve roots are grouped in two trunks running laterally towards the dural pore which is duplicated. The average distance between the pores is 0.5-9 mm, although, in all cases described, the two roots
EP
unite within the hypoglossal canal. Additionally, Lang and Reiter reported more than one dural entrance in 14.8% on the right side and in 27.6% on the left side(9). As
AC C
regards the hypoglossal canal, they described the canal as divided in two in 12.7% of the cases on the right side, and in 25% on the left one(9). According to our observations, in the right side of one specimen (5% of cases) the two separated nerves fused 3 mm after exiting the canal, while in 35% of cases, the fibers of the hypoglossal nerve fuse into a single trunk before the dural pore. Further, in the examined cases, the canal length was between 6.1 mm and 14.1 mm in length, and it runs slantwise forming an angle approximately of 45° with the midsagittal plane.
ACCEPTED MANUSCRIPT
Inside the canal, dura and arachnoid envelope the nerve for two thirds of the length, while a venous plexus surrounds the nerve for the full length. As far as we are concerned, this venous plexus was never described in detail before. Moreover, in one
RI PT
specimen (5%) the hypoglossal nerve was within the canal divided in two trunks running singularly.
As described by Lang, once exited from the skull base, the hypoglossal nerve runs on
SC
the medial surface of the internal jugular vein and on the lateral surface of the vagus
nerve in 92% of cases(8) and, then, it curves around the occipital artery, covered by
M AN U
the sternocleidomastoid muscle. Successively, the hypoglossal nerve runs first on the lateral and then on the anterior surface of the external carotid artery. In 8% of cases, the nerve curves around the external carotid artery where the occipital artery arises, and then it takes a lateral course on the outer surface of the external carotid artery and posterior to the jugular vein.
TE D
After its exit from the canal, the nerve connects with the ventral branches of C1 and C2 and the ventral ansa between the two branches. Hypoglossal nerve and ansa
EP
measured 15-45 mm.
AC C
CONCLUSIONS
We propose a new 5-segment classification of the hypoglossal nerve. This exhaustive anatomical analysis, which considers the entire intra- and extra-cranial course of the nerve along with its relationships with surrounding structures, is valid and clinically and surgically oriented when considering the classical microscopic approaches. The present study could be useful to explain, segment by segment along its intra- and extracranial course, the pathogenic mechanisms of nerve injury caused by lesions that
ACCEPTED MANUSCRIPT
involve the nerve. The neurosurgeon must know this information when approaching the posterior cranial fossa, the cerebellopontine angle and the neck in general to avoid injuring the XIIth nerve.
RI PT
Finally, in the present study we describe a new perspective of the hypoglossal canal
SC
with the venous plexus inside, surrounding the canalar segment of the nerve.
AKNOWLEDGEMENTS
M AN U
The authors would like to thank Dr. Santolo Cozzolino, Director of Center of Biotechnologies, “A. Cardarelli” Hospital, Napoli, Italy, for his highly qualified cooperation to produce the anatomical dissection.
TE D
FIGURE LEGENDS
Figure 1: Microsurgical microscopic view of the origin of the hypoglossal nerve until its entry into the canal. Different rootlets merged into three trunks. On the right the 3-
EP
dimensional reconstruction of the head position for the approach. sXII: superior rootlets of XIIth cn; iXII: inferior rootlets of XIIth cn; VA: vertebral
AC C
artery; PICA: posterior inferior cerebellar artery; dp: dural pore Figure 2: Microsurgical microscopic view of the hypoglossal nerve entering in the
canal after passed through the dural pore. In this specimen is evident a perforation of the dura mater through two separate pores and a division in two different canals with the two nerves fusing after the extracranial exit. Relationships with vetebral and posterior inferior cerebellar arteries are shown. On the right the 3-dimensional reconstruction of the head position for the approach.
ACCEPTED MANUSCRIPT
sXII: superior rootlets of XIIth cn; iXII: inferior rootlets of XIIth cn; VA: vertebral artery; PICA: posterior inferior cerebellar artery; dp: dural pore Figure 3: Endoscopic transcranial closed view of the canalar segment; particular of
RI PT
the small veins piercing in the bone surface several tiny channels for the drainage into the jugular bulb
Figure 4: Photograph showing the descending segment of the hypoglossal nerve in
SC
the portion where it runs laterally to stylohyoid muscle and the posterior belly of the digastric muscle.
M AN U
Figure 5: Photograph showing the horizontal segment of the hypoglossal nerve, at its origin from the previous one, passing inferiorly to the middle tendon of the digastric muscle; stylohyoid muscle, submandibular gland and superior cervical aponeurosis are located laterally.
Figure 6: Photograph showing the ascending segment of the hypoglossal nerve where
tongue.
TE D
it begins at the edge of the mylohyod muscle reaching the inferior surface of the
Figure 7: Photograph showing the ascending segment of the hypoglossal nerve where
EP
it ends up on the underside of the tongue.
Figure 8: Photograph showing the transition between horizontal and ascending
AC C
segment; the superior root of the ansa hypoglossi leaves the hypoglossal trunk on a level with the upper carotid region.
ACCEPTED MANUSCRIPT
REFERENCES 1.
Bademci G, Yasargil MG: Microsurgical anatomy of the hypoglossal nerve. Journal of clinical neuroscience : official journal of the Neurosurgical Society of Australasia 13:841-847, 2006. Candir N, Develi S, Kilir C, Satar B, Yazar F: Distribution of the hypoglossal
RI PT
2.
nerve at the base of the tongue and its clinical importance in radiofrequency ablation therapy. Turk J Med Sci 44:427-431, 2014. 3.
Caruso RD, Rosenbaum AE, Chang JK, Joy SE: Craniocervical junction venous anatomy on enhanced MR images: the suboccipital cavernous sinus.
4.
SC
AJNR American journal of neuroradiology 20:1127-1131, 1999.
Cheng VS, Schultz MD: Unilateral hypoglossal nerve atrophy as a late
M AN U
complication of radiation therapy ofhead and neck carcinoma: a report of four cases and a review of the literature on peripheral and cranial nerve damages after radiation therapy. Cancer 35:1537-1544, 1975. 5.
Curto FS, Jr., Suarez F, Kornblut AD: The extracranial hypoglossal nerve: 112 cadaver dissection. Ear Nose Throat J 59:94-99, 1980.
6.
Fitzgerald MJ, Law ME: The peripheral connexions between the lingual and hypoglossal nerves. J Anat 92:178-188, 1958.
Landois L, Brubaker AP, Eshner AA: Text-book of human physiology,
TE D
7.
including histology and microscopical anatomy, with especial reference to the practice of medicine. Philadelphia,, P. Blakiston's son & co., 1904. 8.
Lang J: Skull base and related structures: Atlas of clinical anatomy. Stuttgart,
9.
EP
Schattauer Verlag, 1995. Lang J, Reiter U: [Intracisternal length of cranial nerves 7-12].
AC C
Neurochirurgia 28:153-157, 1985. 10.
Leblanc A: The Cranial Nerves Anatomy Imaging Vascularisation. Berlin,
Heidelberg, Springer Berlin Heidelberg,, 1995, p 1 online resource.
11.
Loh C, Maya MM, Go JL: Cranial nerve XII: the hypoglossal nerve. Semin Ultrasound CT MR 23:256-265, 2002.
12.
Luschka Hv: Die Anatomie des menschlichen Kopfes. Tubingen,, H. Laupp'schen Buchhandlung, 1867.
13.
Macedo TF, Gow PJ, Heap SW, Wallis WE: Bilateral hypoglossal nerve palsy due to vertical subluxation of the odontoid process in rheumatoid arthritis. Br J Rheumatol 27:317-320, 1988.
ACCEPTED MANUSCRIPT
14.
Mattos JP, Santos MJ, Zullo JF, Joaquim AF, Chaddad-Neto F, Oliveira E: Dissection technique for the study of the cerebral sulci, gyri and ventricles. Arquivos de neuro-psiquiatria 66:282-287, 2008.
15.
Nagai K, Sakuramoto C, Goto F: Unilateral hypoglossal nerve paralysis
RI PT
following the use of the laryngeal mask airway. Anaesthesia 49:603-604, 1994. 16.
Osburn LL, Moller AR, Bhatt JR, Cohen-Gadol AA: Hemilingual spasm: defining a new entity, its electrophysiological correlates and surgical treatment through microvascular decompression. Neurosurgery 67:192-195; discussion
17.
SC
196, 2010.
Perneczky A, R R: Keyhole Approaches in Neurosurgery. Springer-Verlag,
18.
M AN U
2008.
Saigusa H, Tanuma K, Yamashita K, Saigusa M, Niimi S: Nerve fiber analysis for the lingual nerve of the human adult subjects. Surg Radiol Anat 28:59-65, 2006.
19.
Scotti G, Melancon D, Olivier A: Hypoglossal paralysis due to compression by a tortuous internal carotid artery in the neck. Neuroradiology 14:263-265, 1978.
Shiozawa Z, Koike G, Seguchi K, Shindo K, Sugita K: Unilateral tongue
TE D
20.
atrophy due to an enlarged emissary vein in the hypoglossal canal. Surgical neurology 45:477-479, 1996. 21.
Stewart A, Lindsay WA: Bilateral hypoglossal nerve injury following the use
22.
EP
of the laryngeal mask airway. Anaesthesia 57:264-265, 2002. Thompson EO, Smoker WR: Hypoglossal nerve palsy: a segmental approach.
AC C
Radiographics 14:939-958, 1994. 23.
Toldo I, Manara R, Sartori S, Suppiej A, Drigo P: Unilateral hypoglossal nerve palsy due to neurovascular conflict in a child. Brain Dev 31:461-464, 2009.
24.
Toure G, Bicchieray L, Selva J, Vacher C: The intra-lingual course of the nerves of the tongue. Surg Radiol Anat 27:297-302, 2005.
25.
Yousry I, Moriggl B, Schmid UD, Wiesman M, Fesl G, Bruckmann H, Naidich TP, Yousry TA: Detailed anatomy of the intracranial segment of the hypoglossal nerve: neurovascular relationships and landmarks on magnetic resonance imaging sequences. Journal of neurosurgery 96:1113-1122, 2002.
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
ACCEPTED MANUSCRIPT
TABLE
Length (mm)
Thickness (mm)
SEGMENT
Range
Mean
Range
Cisternal
8 - 15
12.7
0.3 - 0.6
0.4
Canalar
9.5 - 16
13
1.3 - 3
2
Descending
48 - 89
65
2-4
3.2
Horizontal
25 - 54
34.6
1.9 - 4
3.3
Ascending
3.6 - 19
5.7
1 - 3.5
2.4
RI PT
SC
M AN U
EP
TE D
Table 1. Summary of length and thickness of each hypoglossal segment.
AC C
Mean
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
ACCEPTED MANUSCRIPT
EP
TE D
M AN U
SC
RI PT
Few anatomic studies concerning the hypoglossal nerve have been reported. We dissected 10 formalin-fixed adult human cadaveric heads (20 specimens). Classification in 5 segments: cisternal, canalar, descending, horizontal, ascending. A new perspective of the hypoglossal canal is proposed. The venous plexus surrounding the canalar segment of the nerve is well described.
AC C
• • • • •