- Email: [email protected]
Minimally invasive surgical exposure of the extreme high cervical internal carotid artery: anatomical study
Journal of Clinical Neuroscience (2000) 7(5), 438–444 © 2000 Harcourt Publishers Ltd DOI: 10.1054/ jocn.1999.0241, available online at http://www.idealibrary.com on
Anatomical study
Minimally invasive surgical exposure of the extreme high cervical internal carotid artery: anatomical study Nobuo Kiya MD, Yutaka Sawamura MD, Catalino Dureza MD, Takanori Fukushima MD DMSc Department of Neurosurgery, Allegheny General Hospital, Allegheny University of the Health Sciences, Pittsburgh, Pennsylvania, USA
Summary The purpose of this study is to investigate a minimally invasive access to a high cervical lesion involving the internal carotid artery. Using 13 fixed cadaveric preparations, we sought to design a surgical approach that would cause minimal involvement of the surrounding structures and maximal exposure to the extreme high cervical area. This technique preserves the function and integrity of the mandible, sternocleidomastoid, posterior belly of digastric and styloid process muscles. The method uses retraction and mobilisation of those muscles, as well as decompression of the facial from the stylomastoid foramen. The internal carotid artery is exposed up to the entry point into the carotid canal. The cranial nerves IX, X, XI and XII are kept in sight up to the jugular foramen. This approach creates a wide corridor into the deep high cervical and inferior cranial base area and can be utilised for high cervical carotid lesions and tumours related to the artery. © 2000 Harcourt Publishers Ltd Keywords: cadaveric study, facial nerve, high cervical region, carotid artery, jugular foramen, surgical anatomy
INTRODUCTION To access the internal carotid artery at the high cervical region and at the inferolateral surface of the cranial base region, various surgical approaches have been described.1–7 These approaches have emphasised displacement of the mandible either by subluxation or mandibulotomy, which involves dividing the posterior belly of the digastric and the styloid group of muscles to facilitate exposure of the internal carotid artery, the entry point of the carotid canal and the dorsolateral aspect of the jugular bulb.1,2,8 The technical difficulty in gaining access has been a major hindrance to effective operation for both the arterial and neoplastic lesions related to the internal carotid artery and penetrating injuries that may occur in these regions. Due to the large surgical involvement of the surrounding structures, this type of surgery has been associated with morbidity. Potential complications of these approaches include problems related to mandibulotomy, such as intraoral contamination, non-union and chronic postoperative pain, as well as decreased neck mobilisation and cosmetically unfavourable results.1,2,8–13 In addition, cranial nerve injury may occur without an appropriate orientation of their courses. Although the lateral neck dissection described here may be a simple modification of prevailing surgical techniques of the anterolateral approach either for access to the first and second vertebral bodies or to the vertebral artery at the junction of its second and third segments; in these approaches, the dissection is carried posterior to the internal jugular vein and the digastric muscle to arrive at the cervical vertebrae.3–7 The technique described here is different from other techniques because it aims at safely exposing the internal carotid artery at its high cervical portion. This report describes a minimally invasive procedure studying cadaveric dissections that would decrease the number of surgically involved structures, obviate the need for surgery on the mandible, and create
an adequate surgical corridor to high cervical lesions above the level of the atlas. The surgical anatomy may help the surgeon to efficiently widen the deep and narrow operative field. MATERIAL AND METHODS Materials Thirteen human cadaver specimens (26 sides) consisting of the whole head and neck prepared above the C7 vertebral body were investigated. The specimens were fixed and injected with red silicone for the carotid and vertebral arteries and with blue silicone
Received 19 October 1998 Accepted 8 December 1999 Correspondence to: Yutaka Sawamura MD, Department of Neurosurgery, Hokkaido University School of Medicine, North-15, West-7, Kita-ku, Sapporo 060, Japan. Tel.: +81–11–716–1161 ext. 5987; Fax: +81–11–706–7878; Email: [email protected]
438
Fig. 1 Schematic drawing indicating a curvilinear skin incision for the extreme high cervical and inferior lateral surface of the skull base region.
Exposure of high cervical carotid 439
Fig. 2 Drawing and photograph showing the mobilised posterior belly of digastric muscle (PBDM). Blunt dissection is used to identify the angle of the mandible (AM), the ventral border of the sternocleidomastoid muscle (SM) and the great auricular nerve (GAN). The accessory nerve (XI) runs dorsolaterally to the anterior edge of the transverse process of the atlas (TPA) while the posterior belly of digastric muscle is retracted supero-ventrally. IJV, internal jugular vein; MP, mastoid process; PG, parotid gland; STA, superficial temporal artery; TFA transverse facial artery.
for the internal jugular vein. Of the 13 specimens, 5 were female and 8 were male with an average age of 66.3 years at the time of death. Dissections were performed on both sides of the head on all 13 cadaver specimens. Each specimen was put in a three-pin holder system to approximate as much as possible the conditions of positioning a real patient in the actual surgical set up. Dissection technique A curvilinear skin incision, beginning approximately 3 cm above the mid-mastoid tip, is taken downward to the inferoanterior edge of the mastoid tip, then curved caudally until it is approximately 1 cm dorsal to the mandibular angle. The full length of the skin incision is about 7 cm (Fig. 1). The platysma muscle is divided along the skin incision. Blunt dissection is used to identify the posterior angle of the mandible, as well as the anterior border of the sternocleidomastoid muscle and the great auricular nerve (Fig. 2). A part of the parotid gland is exposed. The anterior and mid-insertion points of the sternocleidomastoid muscle to the mastoid tip are detached by means of blunt dissection, leaving the posterior insertion of the muscle to the occipital bone surface intact. The great auricular nerve is sacrificed at the most peripheral portion, while maintaining a long stump (Fig. 3) for those cases in which nerve grafting is needed. The dorsal border of the mandible and the superficial posterior border of the mastoid tip define, respectively, the ventrolateral and dorsal limits of the entrance of this approach (Fig. 3). These
© 2000 Harcourt Publishers Ltd
defined borders, with just partial detachment of the muscular insertions, are of primary importance for the postoperative functions of neck movement and mastication. The sternocleidomastoid muscle is retracted dorsally to achieve adequate exposure of the posterior belly of digastric muscle (Figs 2 and 3). The loose connective tissue sheath surrounding the posterior belly of digastric muscle is fully dissected to facilitate mobilisation of this muscle, as described later. The posterior belly of digastric muscle is first carefully retracted ventrally to expose, identify, and avoid injury to the accessory nerve that runs in a dorsocaudal direction between the posterior belly of digastric muscle above and the internal jugular vein below (Fig. 2). An important landmark for identification of the accessory nerve is its lateral point located approximately 3–15 mm caudolaterally to the anterior edge of the transverse process of the atlas. The accessory nerve was located beneath the internal jugular vein in 7 sides (27%) out of 26 sides studied. After identification of the accessory nerve, dorsal retraction of the posterior belly of digastric muscle is applied in order to identify the occipital artery and the hypoglossal nerve, which run caudally and parallel to the occipital artery (Fig. 3). Caudally, using blunt dissection, the superior root of the ansa cervicalis is exposed, proceeding to the point where the ansa cervicalis leaves the hypoglossal nerve, running parallel in the dorsal aspect of the internal carotid artery (Fig. 3). Once the abovementioned structures are identified, the digastric branch of the facial nerve is exposed below the inferior aspect of
Journal of Clinical Neuroscience (2000) 7(5), 438–444
440 Kiya et al.
Fig. 3 Drawing the dorsal retraction of the posterior belly of digastric muscle(PBDM) is applied in order to identify the hypoglossal nerve(XII), the superior root of the ansa cervicalis (Ansa) and the digastric branch (DB) of the facial nerve (VII). GAN, great auricular nerve; IJV, internal jugular vein; OA, occipital artery; ShM, stylohyoid muscle. Photograph shows a magnified view from rectangle on the drawing. The digastric branch (elevated by a nerve dissector) has been exposed to identify the main extracranial trunk of the facial nerve (arrow).
the mastoid tip and ventral to the muscle (Fig. 3). On the other hand, the retroauricular branches of the facial nerve can be identified at the anterior aspect to the mastoid process and followed caudally to find the trunk of the facial nerve. Following these branches of the facial nerve and continuing rostrally with blunt dissection, a partial posterior parotidectomy for approximately 1.5 cm is performed to expose the main extracranial trunk and the anserium of the facial nerve (Fig. 4). The most key element to identify the facial nerve is exposure of either the digastric branch or the retroauricular branches. Exposure of the styloid process with the muscles attached is achieved by performing a dissection following proximally the course of the facial nerve (Fig. 4). The stylohyoid muscle and stylohyoid ligament attached dorsally, the styloglossus muscle inserted to the tip and the stylopharyngeus muscle attached to the medial aspect of the base of the styloid process are preserved, with their insertions intact to the styloid process. The styloid process is resected by drilling with a small burr from the point of insertion to the base of the cranium without any detachment of the muscles inserted thereon (Fig. 5). The stylohyoid, the styloglossus and the stylopharyngeus muscles are supplied by the facial nerve, the hypoglossal nerve and the glossopharyngeal nerve, respectively. Some of these fine nerve branches to the muscles may be severed by this procedure, although the nerve to the styloglossus muscle can be constantly preserved. By retracting the styloid process with the muscle groups caudally, an exposure of the carotid artery near to the entry point of its bony Journal of Clinical Neuroscience (2000) 7(5), 438–444
canal is achieved (Fig. 5). The styloid process can be repositioned by suturing the ligament attaching the process to the firm connective tissue around the cranial base. Approximately 1–2 cm inferior to the entry point of the carotid artery into the carotid canal, on the dorsal aspect, one can observe the glossopharyngeal nerve superiorly and the pharyngeal branch of the vagus inferiorly, crossing on the carotid artery in a mediallateral direction (Fig. 5). The retraction of the internal jugular vein dorsally helps to expose the carotid branch of the glossopharyngeal nerve (the carotid sinus nerve). Also observed and defined at this time are the vagus nerve (which usually adheres to the internal carotid artery), the hypoglossal nerve and its nerve that communicates to the ventral ramus of the C1 nerve, and the origin of the superior laryngeal nerve (Fig. 5). Although at this point of dissection the extremely high cervical portion of the carotid artery is fully exposed, further dissection can be continued only when it is necessary to obtain the higher part of the internal carotid artery and the ventrocaudal aspect of the jugular bulb. After accurately identifying the above-mentioned structures, the ventral and mid-part of the mastoid tip are drilled out and skeletonisation of the stylomastoid foramen is performed to enable mobilisation of the facial nerve (Fig. 6). The remnant of the base of the styloid process can be drilled as well, although this additional procedure makes reattachment of the removed styloid process difficult. The facial nerve is retracted in order to create a maximally exposed space and to facilitate access to the entrance of the carotid canal. © 2000 Harcourt Publishers Ltd
Exposure of high cervical carotid 441
Fig. 4 Drawing and photograph, the partial posterior parotidectomy has been performed to expose the main extracranial trunk of the facial nerve (VII) and the styloid process (SP). The styloid process and attached muscles cover the internal carotid artery at its high position and the jugular vein keep caudal nerves from sight. DB, digastric branch of facial nerve; ECA, external carotid artery; IJV, internal jugular vein; OA, occipital artery; PBDM, posterior belly of digastric muscle; ShM, stylohyoid muscle; XII, hypoglossal nerve.
DISCUSSION We have been utilising this approach for lesions involving the high cervical portion of the internal carotid artery such as for steno-occlusive disease or large aneurysm to manipulate the distal part of this artery. The other lesions for which this approach was useful were extracranial high cervical neoplasms including carotid paraganglioma with cephalomedial extension, hypoglossal schwannoma, vagal schwannoma, lymphangioma and some parotid tumours which originated medial to the facial nerve. Figure 7 demonstrates an example of a high cervical retropharyngeal tumour. This paraganglioma which was firmly adherent medically to the carotid artery was successfully removed using the present approach without any injury to adjacent cranial nerves. In such case of tumours with a parapharyngeal extension, particular attention was paid to preserve the cranial nerves IX, X and XII which were located on and lateral to the tumour bulk. This approach can also provide room for operation on high cervical cranial nerves, such as hemihypoglossal-facial nerve side-to-end anastomosis.14 Based on our previous clinical experience, there have been no major complications due to applying this approach. Although sacrifice of the great auricular nerve caused analgesia around the ear no patients have complained. Salivary fistulae or vascular injury have not been encountered. In a case of hypoglossal schwannoma, an injury to the Xth and IX cranial nerve trunks occurred because of a fanning deformity of these nerves on the
© 2000 Harcourt Publishers Ltd
surface of a firm tumour; except for this direct injury to the cranial nerve trunks, neither swallowing disturbance nor hoarseness occurred. A gentle manipulation of the nerve trunks is, therefore, particularly commended. The stylohyoid, styloglossus and the stylopharyngeus muscles are supplied by the facial nerve, the hypoglossal nerve and the glossopharyngeal nerves, respectively. The fine nerve branches to the muscles may be severed by retracting the styloid process with the muscle groups caudally. To avoid denervation of these muscles retraction of the styloid process should be as minimal as possible, or anterolateral retraction may be suggested to preserve these muscle functions. No perioperative glossal dysfunction was observed. Various authors have described different approaches to lesions involving the internal carotid artery in the high cervical and inferior surface of the skull base region.1–9,11,15–19 These approaches are aimed at finding the best surgical solution for lesions located in a narrow anatomical place containing vulnerable and intricate nervous system structures. Beginning with Strully et al in 1953, there have been two basic types of surgical approaches.20 The earlier anterolateral approach was characterised by mandibular surgical involvement and provided exposure of the high cervical carotid artery and internal jugular vein.1,2,8,9,15,18,21–24 Postoperative complications included intraoral contamination, infection, nonunion of the mandible, nerve palsy and other morbidity.10–13,25 In the early 1980s, the posterolateral approach, characterised by an intact mandible body, mastoidectomy and division of the sternocleidomastoid and the posterior belly of digastric muscles was
Journal of Clinical Neuroscience (2000) 7(5), 438–444
442 Kiya et al.
Fig. 5 Drawing and photograph showing the styloid process (SP) resected from the base of the skull and retracted caudally without any detachment of the styloid muscles (SMs). Glossopharyngeal nerve (IX) and the pharyngeal branch (PB) of the vagus nerve (X) cross the internal carotid artery. Comm, communication from the first cervical ventral ramus; ICA, internal carotid artery; OA, occipital artery; VII, facial nerve; XI, accessory nerve; XII, hypoglossal nerve.
developed.16,26 Lateral neck dissection either to access the first and second vertebral bodies or the vertebral artery at the junction of its second and third segments has been also well developed, but these approaches principally pass through the area posterior to the jugular vein.3–7 We prefer a posterolateral approach using a curvilinear skin incision, with the advantages of enlarged superficial exposure and better cosmetic results. Identification and exposure of the great auricular nerve on the sternocleidomastoid muscle before division were done as a safety measure in case nerve anastomosis, such as facial nerve repair, would be needed. Partial division by blunt dissection of the sternocleidomastoid muscle from its anteromedial insertion on the mastoid tip, leaving both the posterior insertion of the muscle and the branch of the accessory nerve intact, may contribute to the complete functional and cosmetic outcome of this large neck muscle. Previously described procedures often required transection of the posterior belly of the digastric muscle; however using our procedure, division of the digastric muscle is not needed since adequate dissection and retraction, as described, easily exposes the carotid and ventrolateral jugular vein. It is of the utmost importance to carefully define the posterior belly of digastric muscle and the styloid process in order to facilitate their maximal mobilisa-
Journal of Clinical Neuroscience (2000) 7(5), 438–444
tion. Retraction of the posterior belly of digastric muscle and the styloid muscles are important because complete identification of the nervous and vascular structures behind these muscles is crucial to the postoperative outcome. In addition, the relationship of the accessory nerve to the internal jugular vein was not constant. In a study of 47 human cadavers, Krause et al. found that in 26% of all cases the accessory nerve crossed the medial aspect of the internal jugular vein,27 as our study found in seven out of 26 sides (27%). In conclusion, we believe that the advantages of our approach include minimal damage to surrounding structures and it may reduce the morbidity associated with current methods that require the large exposure usually needed for the high cervical region and inferior surface of the skull base. Systematic structure identification and styloid preservation increase the likelihood of successful reconstruction. This approach creates a wide corridor into the deep high cervical and inferior cranial base area and can be utilised for high cervical carotid lesions and tumours attaching to the artery. ACKNOWLEDGMENT The authors wish to thank Dr Shou-Ren Shih for excellent preparation of the cadaver specimens and Nancy D. Lynch for her editorial assistance.
© 2000 Harcourt Publishers Ltd
Exposure of high cervical carotid 443
Fig. 6 Drawing and photograph, a magnified view beneath the entrance of the carotid canal after partial mastoidectomy. Retraction of the internal jugular vein dorsally helps to expose the glossopharyngeal nerve crossing the carotid artery at the skull base. The ventral and mid part of the mastoid tip have been drilled out to enable mobilisation of the facial nerve (VII) from the styloid foramen. DB, digastric branch of facial nerve; ICA, internal carotid artery; IJV, internal jugular vein; OA, occipital artery; PB, pharyngeal branch of the vagus nerve; PBDM, posterior belly of digastric muscle; IX, glossopharyngeal nerve; XI, accessory nerve; XII, hypoglossal nerve.
Fig. 7 T1-weighted contrast MR image showing a carotid paraganglioma extending to the retroepipharyngeal space (A). This tumour, which was tightly adherent to the carotid artery, was completely removed with no injury to the cranial nerves (B).
© 2000 Harcourt Publishers Ltd
Journal of Clinical Neuroscience (2000) 7(5), 438–444
444 Kiya et al. REFERENCES 1. Dichtel WJ, Miller RH, Feliciano DV, Woodson GE, Hurt J. Lateral mandibulotomy: A technique of exposure for penetrating injuries of the internal carotid artery at the base of the skull. Laryngoscope 1984; 94: 1140–4. 2. Fisher DF Jr, Clagett GP, Parker JI, Fry RE, Poor MR, Finn RA, Brink BE, Fry WJ. Mandibular subluxation for high carotid exposure. J Vasc Surg 1984; 1: 727–33. 3. George B, Laurian C, Keravel Y, Cophignon J. Extradural and hourglass cervical neurinomas: the vertebral artery problem. Neurosurgery 1985; 16: 591–594. 4. George B, Lot G. Neurinomas of the first two cervical nerve roots: a series of 42 cases. J Neurosurg 1995; 82: 917–923. 5. George B, Lot G, Tran Ba Huy P. The juxtacondylar approach to the jugular foramen without petrous bone drilling. Surg Neurol 1995; 44: 279–284. 6. Lot G, George B. Cervical neuromas with extradural components: Surgical management in a series of 57 patients. Neurosurgery 1997; 41: 813–822. 7. Sen C, Eisenberg M, Casden AM, Sundaresan N, Catalano PJ. Management of the vertebral artery in excision of extradural tumors of the cervical spine. Neurosurgery 1995; 36: 106–116. 8. Batzdorf U, Gregorius FK. Surgical exposure of the high cervical carotid artery: Experimental study and review. Neurosurgery 1983; 13: 657–61. 9. Balagura S, Carter JB, Gossett DL. Surgical approach to the high subcranial internal carotid artery. Neurosurgery 1985; 16: 402–5. 10. Hans SS, Shah A, Hans B. Carotid endarterectomy for high plaques. Am J Surg 1989; 157: 431–5. 11. Shaha A, Philips T, Scala T, Golueke P, McGinn J, Sclafani S, Hoover E, Jaffe BM. Exposure of the internal carotid artery near the skull base: The posterolateral anatomic approach. J Vasc Surg 1988; 8: 618–22. 12. Shievink WI, Piepgras DG, McCaffrey TV, Mokri B. Surgical treatment of extracranial internal carotid artery dissecting aneurysms. Neurosurgery 1994; 35: 809–16. 13. Sundt TM, Pearson BW, Piepgras DG, Houser OW, Mokri B. Surgical management of aneurysms of the distal extracranial internal carotid artery. J Neurosurg 1986; 64: 169–82. 14. Sawamura Y, Abe H. Hypoglossal-facial nerve side-to-end anastomosis for preservation of hypoglossal function: results of delayed treatment with a new technique. J Neurosurg 1997; 86: 27–31.
Journal of Clinical Neuroscience (2000) 7(5), 438–444
15. Fisch UP, Oldring DJ, Senning A. Surgical therapy of internal carotid artery lesions at the skull base and temporal bone. Otolaryngol Head Neck Surg 1980; 88: 548–54. 16. Purdue GF, Pellegrini RV, Arena S. Aneurysms of the high internal carotid artery: a new approach. Surgery 1981; 89: 268–70. 17. Sandmann W, Hennerici M, Aulich A, Kniemeyer H, Kremer KW. Progress in carotid artery surgery at the base of the skull. J Vasc Surg 1984; 1: 734–43. 18. Sekhar LN, Schramm VL, Jones NF, Yonas H, Horton J, Latchaw RE, Curtin H. Operative exposure and management of the petrous and upper cervical internal carotid artery. Neurosurgery 1986; 19: 967–82. 19. Urken ML, Biller HF, Haimov M. Intratemporal carotid artery bypass in resection of a base of skull tumor. LARYNGOSCOPE 1985; 95: 1472–6. 20. Strully KJ, Hurwitt ES, Blankenberg HW. Thrombo-endarterectomy for thrombosis of the internal carotid artery in the neck. J Neurosurg 1953; 10: 474. 21. Fry RE, Fry WJ. Extracranial carotid artery injuries. Surgery 1980; 88: 581–6. 22. Glassock ME, Smith PG, Bond AG, Whitaker SR, Bartels LJ. Management of aneurysms of the petrous portion of the internal carotid artery by resection and primary anastomosis. Laryngoscope 1983; 93: 1445–53. 23. Magnan PE, Branchereau A, Cannoni M. Traumatic aneurysms of the internal carotid artery at the base of the skull: Two cases treated surgically. J Cardiovasc Surg 1992; 33: 372–9. 24. Welsh P, Pradier R, Repetto R. Fibromuscular dysplasia of the distal cervical internal carotid artery. J Cardiovasc Surg 1981; 22: 321–6. 25. Mock CN, Lilly MP, McRae RG, Carney WI. Selection of the approach to the distal internal carotid artery from the second cervical vertebra to the base of the skull. J Vasc Surg 1990; 6: 846–53. 26. Pellegrini RV, Manzetti GW, DiMarco RF, Bekoe S, Arena SA, Marrangoni AG. The direct surgical management of lesions of the high internal carotid artery. J Cardiovasc Surg 1984; 25: 29–35. 27. Krause HR, Bremerich A, Hermann M. The innervation of the trapezius muscle in connection with radical neck-dissection: An anatomical study. J CranioMax-Fac Surg 1991; 19: 87–9.
© 2000 Harcourt Publishers Ltd
Anatomical study
Minimally invasive surgical exposure of the extreme high cervical internal carotid artery: anatomical study Nobuo Kiya MD, Yutaka Sawamura MD, Catalino Dureza MD, Takanori Fukushima MD DMSc Department of Neurosurgery, Allegheny General Hospital, Allegheny University of the Health Sciences, Pittsburgh, Pennsylvania, USA
Summary The purpose of this study is to investigate a minimally invasive access to a high cervical lesion involving the internal carotid artery. Using 13 fixed cadaveric preparations, we sought to design a surgical approach that would cause minimal involvement of the surrounding structures and maximal exposure to the extreme high cervical area. This technique preserves the function and integrity of the mandible, sternocleidomastoid, posterior belly of digastric and styloid process muscles. The method uses retraction and mobilisation of those muscles, as well as decompression of the facial from the stylomastoid foramen. The internal carotid artery is exposed up to the entry point into the carotid canal. The cranial nerves IX, X, XI and XII are kept in sight up to the jugular foramen. This approach creates a wide corridor into the deep high cervical and inferior cranial base area and can be utilised for high cervical carotid lesions and tumours related to the artery. © 2000 Harcourt Publishers Ltd Keywords: cadaveric study, facial nerve, high cervical region, carotid artery, jugular foramen, surgical anatomy
INTRODUCTION To access the internal carotid artery at the high cervical region and at the inferolateral surface of the cranial base region, various surgical approaches have been described.1–7 These approaches have emphasised displacement of the mandible either by subluxation or mandibulotomy, which involves dividing the posterior belly of the digastric and the styloid group of muscles to facilitate exposure of the internal carotid artery, the entry point of the carotid canal and the dorsolateral aspect of the jugular bulb.1,2,8 The technical difficulty in gaining access has been a major hindrance to effective operation for both the arterial and neoplastic lesions related to the internal carotid artery and penetrating injuries that may occur in these regions. Due to the large surgical involvement of the surrounding structures, this type of surgery has been associated with morbidity. Potential complications of these approaches include problems related to mandibulotomy, such as intraoral contamination, non-union and chronic postoperative pain, as well as decreased neck mobilisation and cosmetically unfavourable results.1,2,8–13 In addition, cranial nerve injury may occur without an appropriate orientation of their courses. Although the lateral neck dissection described here may be a simple modification of prevailing surgical techniques of the anterolateral approach either for access to the first and second vertebral bodies or to the vertebral artery at the junction of its second and third segments; in these approaches, the dissection is carried posterior to the internal jugular vein and the digastric muscle to arrive at the cervical vertebrae.3–7 The technique described here is different from other techniques because it aims at safely exposing the internal carotid artery at its high cervical portion. This report describes a minimally invasive procedure studying cadaveric dissections that would decrease the number of surgically involved structures, obviate the need for surgery on the mandible, and create
an adequate surgical corridor to high cervical lesions above the level of the atlas. The surgical anatomy may help the surgeon to efficiently widen the deep and narrow operative field. MATERIAL AND METHODS Materials Thirteen human cadaver specimens (26 sides) consisting of the whole head and neck prepared above the C7 vertebral body were investigated. The specimens were fixed and injected with red silicone for the carotid and vertebral arteries and with blue silicone
Received 19 October 1998 Accepted 8 December 1999 Correspondence to: Yutaka Sawamura MD, Department of Neurosurgery, Hokkaido University School of Medicine, North-15, West-7, Kita-ku, Sapporo 060, Japan. Tel.: +81–11–716–1161 ext. 5987; Fax: +81–11–706–7878; Email: [email protected]
438
Fig. 1 Schematic drawing indicating a curvilinear skin incision for the extreme high cervical and inferior lateral surface of the skull base region.
Exposure of high cervical carotid 439
Fig. 2 Drawing and photograph showing the mobilised posterior belly of digastric muscle (PBDM). Blunt dissection is used to identify the angle of the mandible (AM), the ventral border of the sternocleidomastoid muscle (SM) and the great auricular nerve (GAN). The accessory nerve (XI) runs dorsolaterally to the anterior edge of the transverse process of the atlas (TPA) while the posterior belly of digastric muscle is retracted supero-ventrally. IJV, internal jugular vein; MP, mastoid process; PG, parotid gland; STA, superficial temporal artery; TFA transverse facial artery.
for the internal jugular vein. Of the 13 specimens, 5 were female and 8 were male with an average age of 66.3 years at the time of death. Dissections were performed on both sides of the head on all 13 cadaver specimens. Each specimen was put in a three-pin holder system to approximate as much as possible the conditions of positioning a real patient in the actual surgical set up. Dissection technique A curvilinear skin incision, beginning approximately 3 cm above the mid-mastoid tip, is taken downward to the inferoanterior edge of the mastoid tip, then curved caudally until it is approximately 1 cm dorsal to the mandibular angle. The full length of the skin incision is about 7 cm (Fig. 1). The platysma muscle is divided along the skin incision. Blunt dissection is used to identify the posterior angle of the mandible, as well as the anterior border of the sternocleidomastoid muscle and the great auricular nerve (Fig. 2). A part of the parotid gland is exposed. The anterior and mid-insertion points of the sternocleidomastoid muscle to the mastoid tip are detached by means of blunt dissection, leaving the posterior insertion of the muscle to the occipital bone surface intact. The great auricular nerve is sacrificed at the most peripheral portion, while maintaining a long stump (Fig. 3) for those cases in which nerve grafting is needed. The dorsal border of the mandible and the superficial posterior border of the mastoid tip define, respectively, the ventrolateral and dorsal limits of the entrance of this approach (Fig. 3). These
© 2000 Harcourt Publishers Ltd
defined borders, with just partial detachment of the muscular insertions, are of primary importance for the postoperative functions of neck movement and mastication. The sternocleidomastoid muscle is retracted dorsally to achieve adequate exposure of the posterior belly of digastric muscle (Figs 2 and 3). The loose connective tissue sheath surrounding the posterior belly of digastric muscle is fully dissected to facilitate mobilisation of this muscle, as described later. The posterior belly of digastric muscle is first carefully retracted ventrally to expose, identify, and avoid injury to the accessory nerve that runs in a dorsocaudal direction between the posterior belly of digastric muscle above and the internal jugular vein below (Fig. 2). An important landmark for identification of the accessory nerve is its lateral point located approximately 3–15 mm caudolaterally to the anterior edge of the transverse process of the atlas. The accessory nerve was located beneath the internal jugular vein in 7 sides (27%) out of 26 sides studied. After identification of the accessory nerve, dorsal retraction of the posterior belly of digastric muscle is applied in order to identify the occipital artery and the hypoglossal nerve, which run caudally and parallel to the occipital artery (Fig. 3). Caudally, using blunt dissection, the superior root of the ansa cervicalis is exposed, proceeding to the point where the ansa cervicalis leaves the hypoglossal nerve, running parallel in the dorsal aspect of the internal carotid artery (Fig. 3). Once the abovementioned structures are identified, the digastric branch of the facial nerve is exposed below the inferior aspect of
Journal of Clinical Neuroscience (2000) 7(5), 438–444
440 Kiya et al.
Fig. 3 Drawing the dorsal retraction of the posterior belly of digastric muscle(PBDM) is applied in order to identify the hypoglossal nerve(XII), the superior root of the ansa cervicalis (Ansa) and the digastric branch (DB) of the facial nerve (VII). GAN, great auricular nerve; IJV, internal jugular vein; OA, occipital artery; ShM, stylohyoid muscle. Photograph shows a magnified view from rectangle on the drawing. The digastric branch (elevated by a nerve dissector) has been exposed to identify the main extracranial trunk of the facial nerve (arrow).
the mastoid tip and ventral to the muscle (Fig. 3). On the other hand, the retroauricular branches of the facial nerve can be identified at the anterior aspect to the mastoid process and followed caudally to find the trunk of the facial nerve. Following these branches of the facial nerve and continuing rostrally with blunt dissection, a partial posterior parotidectomy for approximately 1.5 cm is performed to expose the main extracranial trunk and the anserium of the facial nerve (Fig. 4). The most key element to identify the facial nerve is exposure of either the digastric branch or the retroauricular branches. Exposure of the styloid process with the muscles attached is achieved by performing a dissection following proximally the course of the facial nerve (Fig. 4). The stylohyoid muscle and stylohyoid ligament attached dorsally, the styloglossus muscle inserted to the tip and the stylopharyngeus muscle attached to the medial aspect of the base of the styloid process are preserved, with their insertions intact to the styloid process. The styloid process is resected by drilling with a small burr from the point of insertion to the base of the cranium without any detachment of the muscles inserted thereon (Fig. 5). The stylohyoid, the styloglossus and the stylopharyngeus muscles are supplied by the facial nerve, the hypoglossal nerve and the glossopharyngeal nerve, respectively. Some of these fine nerve branches to the muscles may be severed by this procedure, although the nerve to the styloglossus muscle can be constantly preserved. By retracting the styloid process with the muscle groups caudally, an exposure of the carotid artery near to the entry point of its bony Journal of Clinical Neuroscience (2000) 7(5), 438–444
canal is achieved (Fig. 5). The styloid process can be repositioned by suturing the ligament attaching the process to the firm connective tissue around the cranial base. Approximately 1–2 cm inferior to the entry point of the carotid artery into the carotid canal, on the dorsal aspect, one can observe the glossopharyngeal nerve superiorly and the pharyngeal branch of the vagus inferiorly, crossing on the carotid artery in a mediallateral direction (Fig. 5). The retraction of the internal jugular vein dorsally helps to expose the carotid branch of the glossopharyngeal nerve (the carotid sinus nerve). Also observed and defined at this time are the vagus nerve (which usually adheres to the internal carotid artery), the hypoglossal nerve and its nerve that communicates to the ventral ramus of the C1 nerve, and the origin of the superior laryngeal nerve (Fig. 5). Although at this point of dissection the extremely high cervical portion of the carotid artery is fully exposed, further dissection can be continued only when it is necessary to obtain the higher part of the internal carotid artery and the ventrocaudal aspect of the jugular bulb. After accurately identifying the above-mentioned structures, the ventral and mid-part of the mastoid tip are drilled out and skeletonisation of the stylomastoid foramen is performed to enable mobilisation of the facial nerve (Fig. 6). The remnant of the base of the styloid process can be drilled as well, although this additional procedure makes reattachment of the removed styloid process difficult. The facial nerve is retracted in order to create a maximally exposed space and to facilitate access to the entrance of the carotid canal. © 2000 Harcourt Publishers Ltd
Exposure of high cervical carotid 441
Fig. 4 Drawing and photograph, the partial posterior parotidectomy has been performed to expose the main extracranial trunk of the facial nerve (VII) and the styloid process (SP). The styloid process and attached muscles cover the internal carotid artery at its high position and the jugular vein keep caudal nerves from sight. DB, digastric branch of facial nerve; ECA, external carotid artery; IJV, internal jugular vein; OA, occipital artery; PBDM, posterior belly of digastric muscle; ShM, stylohyoid muscle; XII, hypoglossal nerve.
DISCUSSION We have been utilising this approach for lesions involving the high cervical portion of the internal carotid artery such as for steno-occlusive disease or large aneurysm to manipulate the distal part of this artery. The other lesions for which this approach was useful were extracranial high cervical neoplasms including carotid paraganglioma with cephalomedial extension, hypoglossal schwannoma, vagal schwannoma, lymphangioma and some parotid tumours which originated medial to the facial nerve. Figure 7 demonstrates an example of a high cervical retropharyngeal tumour. This paraganglioma which was firmly adherent medically to the carotid artery was successfully removed using the present approach without any injury to adjacent cranial nerves. In such case of tumours with a parapharyngeal extension, particular attention was paid to preserve the cranial nerves IX, X and XII which were located on and lateral to the tumour bulk. This approach can also provide room for operation on high cervical cranial nerves, such as hemihypoglossal-facial nerve side-to-end anastomosis.14 Based on our previous clinical experience, there have been no major complications due to applying this approach. Although sacrifice of the great auricular nerve caused analgesia around the ear no patients have complained. Salivary fistulae or vascular injury have not been encountered. In a case of hypoglossal schwannoma, an injury to the Xth and IX cranial nerve trunks occurred because of a fanning deformity of these nerves on the
© 2000 Harcourt Publishers Ltd
surface of a firm tumour; except for this direct injury to the cranial nerve trunks, neither swallowing disturbance nor hoarseness occurred. A gentle manipulation of the nerve trunks is, therefore, particularly commended. The stylohyoid, styloglossus and the stylopharyngeus muscles are supplied by the facial nerve, the hypoglossal nerve and the glossopharyngeal nerves, respectively. The fine nerve branches to the muscles may be severed by retracting the styloid process with the muscle groups caudally. To avoid denervation of these muscles retraction of the styloid process should be as minimal as possible, or anterolateral retraction may be suggested to preserve these muscle functions. No perioperative glossal dysfunction was observed. Various authors have described different approaches to lesions involving the internal carotid artery in the high cervical and inferior surface of the skull base region.1–9,11,15–19 These approaches are aimed at finding the best surgical solution for lesions located in a narrow anatomical place containing vulnerable and intricate nervous system structures. Beginning with Strully et al in 1953, there have been two basic types of surgical approaches.20 The earlier anterolateral approach was characterised by mandibular surgical involvement and provided exposure of the high cervical carotid artery and internal jugular vein.1,2,8,9,15,18,21–24 Postoperative complications included intraoral contamination, infection, nonunion of the mandible, nerve palsy and other morbidity.10–13,25 In the early 1980s, the posterolateral approach, characterised by an intact mandible body, mastoidectomy and division of the sternocleidomastoid and the posterior belly of digastric muscles was
Journal of Clinical Neuroscience (2000) 7(5), 438–444
442 Kiya et al.
Fig. 5 Drawing and photograph showing the styloid process (SP) resected from the base of the skull and retracted caudally without any detachment of the styloid muscles (SMs). Glossopharyngeal nerve (IX) and the pharyngeal branch (PB) of the vagus nerve (X) cross the internal carotid artery. Comm, communication from the first cervical ventral ramus; ICA, internal carotid artery; OA, occipital artery; VII, facial nerve; XI, accessory nerve; XII, hypoglossal nerve.
developed.16,26 Lateral neck dissection either to access the first and second vertebral bodies or the vertebral artery at the junction of its second and third segments has been also well developed, but these approaches principally pass through the area posterior to the jugular vein.3–7 We prefer a posterolateral approach using a curvilinear skin incision, with the advantages of enlarged superficial exposure and better cosmetic results. Identification and exposure of the great auricular nerve on the sternocleidomastoid muscle before division were done as a safety measure in case nerve anastomosis, such as facial nerve repair, would be needed. Partial division by blunt dissection of the sternocleidomastoid muscle from its anteromedial insertion on the mastoid tip, leaving both the posterior insertion of the muscle and the branch of the accessory nerve intact, may contribute to the complete functional and cosmetic outcome of this large neck muscle. Previously described procedures often required transection of the posterior belly of the digastric muscle; however using our procedure, division of the digastric muscle is not needed since adequate dissection and retraction, as described, easily exposes the carotid and ventrolateral jugular vein. It is of the utmost importance to carefully define the posterior belly of digastric muscle and the styloid process in order to facilitate their maximal mobilisa-
Journal of Clinical Neuroscience (2000) 7(5), 438–444
tion. Retraction of the posterior belly of digastric muscle and the styloid muscles are important because complete identification of the nervous and vascular structures behind these muscles is crucial to the postoperative outcome. In addition, the relationship of the accessory nerve to the internal jugular vein was not constant. In a study of 47 human cadavers, Krause et al. found that in 26% of all cases the accessory nerve crossed the medial aspect of the internal jugular vein,27 as our study found in seven out of 26 sides (27%). In conclusion, we believe that the advantages of our approach include minimal damage to surrounding structures and it may reduce the morbidity associated with current methods that require the large exposure usually needed for the high cervical region and inferior surface of the skull base. Systematic structure identification and styloid preservation increase the likelihood of successful reconstruction. This approach creates a wide corridor into the deep high cervical and inferior cranial base area and can be utilised for high cervical carotid lesions and tumours attaching to the artery. ACKNOWLEDGMENT The authors wish to thank Dr Shou-Ren Shih for excellent preparation of the cadaver specimens and Nancy D. Lynch for her editorial assistance.
© 2000 Harcourt Publishers Ltd
Exposure of high cervical carotid 443
Fig. 6 Drawing and photograph, a magnified view beneath the entrance of the carotid canal after partial mastoidectomy. Retraction of the internal jugular vein dorsally helps to expose the glossopharyngeal nerve crossing the carotid artery at the skull base. The ventral and mid part of the mastoid tip have been drilled out to enable mobilisation of the facial nerve (VII) from the styloid foramen. DB, digastric branch of facial nerve; ICA, internal carotid artery; IJV, internal jugular vein; OA, occipital artery; PB, pharyngeal branch of the vagus nerve; PBDM, posterior belly of digastric muscle; IX, glossopharyngeal nerve; XI, accessory nerve; XII, hypoglossal nerve.
Fig. 7 T1-weighted contrast MR image showing a carotid paraganglioma extending to the retroepipharyngeal space (A). This tumour, which was tightly adherent to the carotid artery, was completely removed with no injury to the cranial nerves (B).
© 2000 Harcourt Publishers Ltd
Journal of Clinical Neuroscience (2000) 7(5), 438–444
444 Kiya et al. REFERENCES 1. Dichtel WJ, Miller RH, Feliciano DV, Woodson GE, Hurt J. Lateral mandibulotomy: A technique of exposure for penetrating injuries of the internal carotid artery at the base of the skull. Laryngoscope 1984; 94: 1140–4. 2. Fisher DF Jr, Clagett GP, Parker JI, Fry RE, Poor MR, Finn RA, Brink BE, Fry WJ. Mandibular subluxation for high carotid exposure. J Vasc Surg 1984; 1: 727–33. 3. George B, Laurian C, Keravel Y, Cophignon J. Extradural and hourglass cervical neurinomas: the vertebral artery problem. Neurosurgery 1985; 16: 591–594. 4. George B, Lot G. Neurinomas of the first two cervical nerve roots: a series of 42 cases. J Neurosurg 1995; 82: 917–923. 5. George B, Lot G, Tran Ba Huy P. The juxtacondylar approach to the jugular foramen without petrous bone drilling. Surg Neurol 1995; 44: 279–284. 6. Lot G, George B. Cervical neuromas with extradural components: Surgical management in a series of 57 patients. Neurosurgery 1997; 41: 813–822. 7. Sen C, Eisenberg M, Casden AM, Sundaresan N, Catalano PJ. Management of the vertebral artery in excision of extradural tumors of the cervical spine. Neurosurgery 1995; 36: 106–116. 8. Batzdorf U, Gregorius FK. Surgical exposure of the high cervical carotid artery: Experimental study and review. Neurosurgery 1983; 13: 657–61. 9. Balagura S, Carter JB, Gossett DL. Surgical approach to the high subcranial internal carotid artery. Neurosurgery 1985; 16: 402–5. 10. Hans SS, Shah A, Hans B. Carotid endarterectomy for high plaques. Am J Surg 1989; 157: 431–5. 11. Shaha A, Philips T, Scala T, Golueke P, McGinn J, Sclafani S, Hoover E, Jaffe BM. Exposure of the internal carotid artery near the skull base: The posterolateral anatomic approach. J Vasc Surg 1988; 8: 618–22. 12. Shievink WI, Piepgras DG, McCaffrey TV, Mokri B. Surgical treatment of extracranial internal carotid artery dissecting aneurysms. Neurosurgery 1994; 35: 809–16. 13. Sundt TM, Pearson BW, Piepgras DG, Houser OW, Mokri B. Surgical management of aneurysms of the distal extracranial internal carotid artery. J Neurosurg 1986; 64: 169–82. 14. Sawamura Y, Abe H. Hypoglossal-facial nerve side-to-end anastomosis for preservation of hypoglossal function: results of delayed treatment with a new technique. J Neurosurg 1997; 86: 27–31.
Journal of Clinical Neuroscience (2000) 7(5), 438–444
15. Fisch UP, Oldring DJ, Senning A. Surgical therapy of internal carotid artery lesions at the skull base and temporal bone. Otolaryngol Head Neck Surg 1980; 88: 548–54. 16. Purdue GF, Pellegrini RV, Arena S. Aneurysms of the high internal carotid artery: a new approach. Surgery 1981; 89: 268–70. 17. Sandmann W, Hennerici M, Aulich A, Kniemeyer H, Kremer KW. Progress in carotid artery surgery at the base of the skull. J Vasc Surg 1984; 1: 734–43. 18. Sekhar LN, Schramm VL, Jones NF, Yonas H, Horton J, Latchaw RE, Curtin H. Operative exposure and management of the petrous and upper cervical internal carotid artery. Neurosurgery 1986; 19: 967–82. 19. Urken ML, Biller HF, Haimov M. Intratemporal carotid artery bypass in resection of a base of skull tumor. LARYNGOSCOPE 1985; 95: 1472–6. 20. Strully KJ, Hurwitt ES, Blankenberg HW. Thrombo-endarterectomy for thrombosis of the internal carotid artery in the neck. J Neurosurg 1953; 10: 474. 21. Fry RE, Fry WJ. Extracranial carotid artery injuries. Surgery 1980; 88: 581–6. 22. Glassock ME, Smith PG, Bond AG, Whitaker SR, Bartels LJ. Management of aneurysms of the petrous portion of the internal carotid artery by resection and primary anastomosis. Laryngoscope 1983; 93: 1445–53. 23. Magnan PE, Branchereau A, Cannoni M. Traumatic aneurysms of the internal carotid artery at the base of the skull: Two cases treated surgically. J Cardiovasc Surg 1992; 33: 372–9. 24. Welsh P, Pradier R, Repetto R. Fibromuscular dysplasia of the distal cervical internal carotid artery. J Cardiovasc Surg 1981; 22: 321–6. 25. Mock CN, Lilly MP, McRae RG, Carney WI. Selection of the approach to the distal internal carotid artery from the second cervical vertebra to the base of the skull. J Vasc Surg 1990; 6: 846–53. 26. Pellegrini RV, Manzetti GW, DiMarco RF, Bekoe S, Arena SA, Marrangoni AG. The direct surgical management of lesions of the high internal carotid artery. J Cardiovasc Surg 1984; 25: 29–35. 27. Krause HR, Bremerich A, Hermann M. The innervation of the trapezius muscle in connection with radical neck-dissection: An anatomical study. J CranioMax-Fac Surg 1991; 19: 87–9.
© 2000 Harcourt Publishers Ltd