Midline mandibulotomy and interposition grafting for lesions involving the internal carotid artery below the skull base
Article Outline
- Abstract
- Materials and methods
- Results
- Discussion
- Conclusion
- Author contributions
- Acknowledgment
- References
- Copyright
Background
The distal part of the internal carotid artery (ICA) close to the skull base can be reached surgically with different approaches. Exposure using the standard lateral incision is eventually limited by bony structures which preclude the wide-angled operative field necessary for en bloc resection of tumors or primary vascular pathology that abuts the parapharyngeal space. In these unusual cases, use of a combined midline mandibulotomy and neck incision provides necessary operative exposure.
Aim
We report our experience using combined midline mandibulotomy and neck incision for exposure of high carotid lesions. We also discuss different surgical and endovascular approaches in light of the literature.
Patients and Methods
Five patients were operated on for high ICA lesions: 2 for malignant head and neck tumors, 1 for an extended paraganglioma, and 2 for large symptomatic ICA aneurysms. All ICAs were reconstructed with an autologous vein interposition graft and the distal anastomoses were performed within the most distal 3 cm of the ICA adjacent to the orifice of bony carotid canal.
Results
All operations were technically successful with no operative mortality or strokes. One aneurysm patient and the paraganglioma patient had minimal long-term sequelae from this procedure. One patient with an extended lingual epidermoid carcinoma was recurrence free at 3.6 years. One aneurysm patient died due to aspiration pneumonia 30 days postoperatively and another patient had early recurrent tumor growth and died due to that after 15 months. Four patients (80%) suffered a major cranial nerve injury in the operation mainly due to the extensive nature of the disease process.
Conclusion
Exposure of the distal carotid artery using midline mandibulotomy is rarely required. However, this technique represents an excellent option for cases of malignancies arising from the oral cavity which abut the carotid artery and instances in which primary carotid pathology extends medially alongside the parapharyngeal space. Performance of these cases should be accomplished by a multidisciplinary surgical team comprised of head and neck and vascular specialists. High rates of cranial nerve deficits should be anticipated.
Surgery of the distal internal carotid artery (ICA) near the skull base is a challenging procedure. Adequate exposure through a standard carotid incision is often not possible. Several approaches to extend the exposure have been suggested.1, 2, 3, 4, 5, 6 Lateral approach is eventually limited by the structures of the skull base unless a radical mastoidectomy and intrapetrosal drilling is performed.1, 2, 6 Midline and paramidline mandibulotomies are frequently used operations to expose and resect tumors of the oral cavity, oropharynx, and parapharyngeal space.7, 8, 9, 10 The internal carotid artery runs in the parapharyngeal space close to the lateral border of nasopharynx11 and can therefore be reached from medial direction using combined midline mandibulotomy and an extended neck incision.
In addition to tumors, traumatic lesions and aneurysms may mandate surgery at this level.6, 12, 13, 14, 15 In order to combine experience from different surgical specialties, we have adopted a multidisciplinary approach to this area in which the face and neck surgeons perform the exposure and resection of any malignancy arising from the neck or oral cavity. Vascular surgeons are present to control the vessels and perform the vascular reconstruction (Fig 1), in cases where these tumors abut the carotid artery and in cases in which the pathology arises directly from the distal carotid artery along the parapharyngeal space (eg, carotid aneurysm).
Fig 1.
A schematic drawing of the autologous interposition graft (blue) and its relation to the bony structures and the resected carotid bifurcation and internal carotid artery (ICA) (dotted red line). A, Intraosseal part of the internal carotid artery; B, distal anastomosis; C, resected carotid artery; D, autologous vein interposition; E, common carotid artery; I, intracranial ICA; S, styloid process; T, tympanic bone. Medial (and oral cavity) is the right side of the picture.
We report our experience with five cases using the combined midline mandibulotomy and lateral cervical incision to approach the ICA at the base of the skull including a technical description of the surgical exposure. Additionally, we report the morbidity and mortality associated with this procedure and discuss advantages and disadvantages in the context of the published literature.
Materials and methods
Between Sep 2004 and Jun 2006, 5 patients were operated on for high carotid artery lesions close to the skull base using midline mandibulotomy approach at the Helsinki University Central Hospital. The patient charts and operative records where re-analyzed. Three patients, who were still alive, were contacted to obtain their follow-up data and status.
The operations were performed by a team including an ENT-surgeon or a maxillofacial surgeon and a vascular surgeon. A standard midline mandibulotomy9 was used in all cases. Tracheostomy was performed in the three tumor cases. The lipsplit and midneck skin incision were used in order to gain proximal control of the common carotid artery and to perform neck dissection in tumor cases (Fig 2). An intraoral mucosal incision was performed along the floor of the mouth. The tongue was mobilized medially and the lateral aspect of the oropharynx was exposed. The mandible was then elevated and subluxated in lateral direction. By performing lateral rotation of the mandible, the region of interest could be exposed both medially and laterally. The tympanic bone and the carotid canal could be reached in a wide angle and the distal ICA control could be obtained. The wide angle made it possible to perform the distal anastomosis in a standard end-to-end manner in all cases. The bony structures of the skull base where not resected. After distal and proximal carotid artery control, the final tumor resection was performed en bloc. In aneurysm operations, the ICA and common carotid artery (CCA) were clamped after heparinization and the aneurysm sac was opened and partially resected. Shunting with a standard Pruitt-Inahara carotid shunt was performed in three of the operations (tumor cases). Distal supportive hold sutures were used in two cases in order to prevent the distal ICA from sliding into the carotid canal as the anastomosis was performed at the orifice of the carotid canal. The internal carotid artery was reconstructed with either crural or thigh great saphenous vein (Fig 1, Fig 3).
Fig 2.
Skin incision for combined midline mandibulotomy and radical neck tumour surgery exposure.
Fig 3.
Operative field after a radical neck dissection with the interposition in place. In this operation for an extensive lingual epidermoid carcinoma, the left hemimandible was resected (Patient 1). In the other cases, the hemimandible was lifted up as a hinge and did not restrict the exposition to the distal internal carotid artery (ICA). Note that the neck is hyperextended and thus the graft seems to be under tension, which will be relieved when the neck is neutralized. Arrows, proximal and distal anastomosis; A, anteriorly transsected mandible.
Cranial nerves were evaluated clinically by the head and neck surgeons pre- and postoperatively. All operations were performed using standard 3.5 × magnifying optical loops and small vascular instrumentation. Microscopes were not used in these cases, although the surgeons were familiar with microsurgical techniques.
Results
Five patients were operated on using combined midline mandibulotomy and standard neck incision for medial carotid exposure. Two patients had high internal carotid aneurysms extending close to the skull base. Three patients had a neoplastic lesion: 2 malignant oral tumors with neck metastasis and 1 primary paraganglioma.
All operations were initially successful and no immediate strokes or deaths were encountered. One aneurysm patient and a paraganglioma patient had almost no operation-related morbidity at follow-up (Patients 4 and 5). One patient with an extended lingual epidermoid carcinoma with local extension into the mandibular bone is recurrence free at 3.6 years (Patient 1). One aneurysm patient with glossopharyngeal nerve injury died 30 days postoperatively due to aspiration pneumonia (Patient 3). Another patient died due to malignant tumor recurrence after 15 months (Patient 2). Hypoglossal and glossopharyngeal nerve injury was also seen in Patient 4 with a paraganglioma invading glossopharyngeal nerve close to the cranial base. The vagal nerve was resected in all three tumor cases. External carotid artery was reconstructed end-to-side to the interposition graft in two cases and ligated in three cases.
Median operation time and blood loss were 550 minutes (148-705 minutes) and 1730 mL (1000-3500 mL), respectively. A Pruitt-Inahara shunt was used in 3 patients and carotid closure time was 8-11 minutes with a shunt and 15 and 31 minutes in the aneurysm operations in which no shunt was used due to strong backflow from the ICA. Intravenous cefuroxime and metronidazole were used perioperatively and these were planned to be continued perorally when possible. However, in 4 patients some kind of postoperative problem (aspiration pneumonia, local fistula, or free flap ischemia) led to various use of broad-spectrum antibiotics.
Patient 1
A 36-year-old male with an extensive recurrent lingual epidermoid carcinoma with local growth to the mandibular bone was operated on in September 2004. Due to tumor invasion into the left ICA, the carotid bifurcation and most of the extracranial ICA were resected en bloc with the tumor. The distal ICA anastomosis was performed at the orifice of the bony carotid canal, with hold sutures preventing the ICA from retracting into the canal (Fig 3). The mandible was resected and reconstructed with an iliac crest microvascular free flap, anastomosed to the left subclavian artery and vein. The microvascular reconstruction was lost due to necrosis and the area was covered with a pectoralis major rotational flap. The patient survived and has no signs of recurrence after 3.6 years of follow-up. His mandible was re-reconstructed in 2007 with a parascapular and a latissimus dorsi muscle microvascular free flap anastomosed to the left internal mammary artery and subclavian vein. He lives at home, but still needs a jejunal feeding tube for his enteral nutrition. He has also been scheduled for a secondary trimming operation of the reconstruction transfer for aesthetic reasons.
Patient 2A 48-year-old female with extended epidermoid carcinoma of the hypopharynx had metastasis to both sides of the neck. Her left internal jugular vein was resected due to tumor growth and the right was left in situ after careful dissection of all macroscopic tumor growth. The left carotid artery was reconstructed from midline mandibulotomy exposition and the distal anastomosis was performed approximately 1.0 cm from the base of the skull. A radical neck dissection was performed on both sides and a pectoralis major flap was used to cover the reconstructed side. Her neck wound healed by second intention after prolonged antibiotics and a split thickness skin grafting. Two months after the operation, a recurrent tumor was identified and she had a fistula from the tumor close to her ear. The situation was stated as incurable and no further adjuvant therapy was given. She died 15 months later due to this recurrence.
Patient 3A 68-year-old female with cyphoscoliosis and chronic respiratory insufficiency with ambulatory oxygen treatment developed a 4-cm ICA aneurysm causing pain and bleeding from a peritonsillar ulceration and she needed treatment on an emergency basis. Endovascular treatment was considered, but due to turtuosity, supposed difficulty in distal control, and local compression symptoms of the ICA open surgery using midline mandibulotomy was performed in Oct 2005. Due to the cyphosis, the intubation was difficult and performed nasally, but the mandibulotomy gave an excellent exposition to ICA distal to the aneurysm. The aneurysm was opened, the ICA transected and replaced with autologous vein (greater saphenous vein) interposition graft. She had hypoglossal and glossopharyngeal nerve injuries and postoperative pharyngeal edema. Due to the edema, her intubation was prolonged and she was on parenteral nutrition. Postoperative tracheostomy was considered, but due to patient refusal to have one during an earlier hospitalization due to her pulmonary situation, and the fact that her pharyngeal swelling diminished, it was never performed. She was extubated on postoperative day 7 and transferred 4 days later to a local hospital. She died 30 days postoperatively due to aspiration pneumonia.
Patient 4A 21-year-old male patient with extended paraganglioma had local tumor growth extending to the carotid canal and surrounding the internal carotid artery (Fig 4). During the operation it became obvious that the cranial extension of the tumor invaded glossopharyngeal and hypoglossal nerves close to the skull base. The distal ICA was controlled with shunting and the anastomosis was performed at the orifice of the carotid canal. Hypoglossal, vagal, and a part of the glossopharyngeal nerves were sacrificed and he suffered from swallowing and speech disturbances postoperatively. He had an aspiration pneumonia which was successfully treated with antibiotics. Histological examination showed a noncapsular, but benign paraganglioma. Low proliferation rate (3%) was estimated with Ki-67 (= MIB-1) immunohistochemistry. Four months later, a contralateral 10 × 30 mm paraganglioma was identified and treated with radiation therapy. After a 27-month follow-up, his magnetic resonance imaging (MRI) showed an 11 × 25 mm tumor on the radiated side and no recurrence on the operated side. The tumor had diminished in size and caused no local or general symptoms. He had recovered from the cranial nerve injuries and his swallowing and speech functions were remarkably good. He had taken up with his previous studies in technical engineering.
Fig 4.
Computed tomography (CT) reconstruction of a bipartial benign noncapsular paraganglioma in a 21-year-old male (Patient 4). The white arrows mark the two parts of the tumor. The smaller, more cranial part is extending into the carotid canal. The upper internal carotid artery (ICA) interposition anastomosis was performed at the level marked with a small black arrow. This picture shows the limiting bony structure of the tympanic bone. ECA, External carotid artery; DEX, dexter.
A 52-year-old male had been under surveillance in his local hospital for 12 years due to an ICA aneurysm which gradually reached the diameter of 60 mm. He presented with compression symptoms and a large pulsating neck mass. The ICA aneurysm originated 3 cm above the carotid bifurcation (Fig 5). The distal anastomosis was performed approximately 2 cm beneath the base of the skull. His recovery was uneventful and after 2 years he has almost no morbidity and the scars have healed well (Fig 6).
Fig 5.
A computed tomography (CT) reconstruction of a 60 mm internal carotid artery (ICA) aneurysm showing the distal proportions of skull base and the artery cranial to the aneurysm (white arrow). B marks the level of the carotid bifurcation (Patient 5).
Fig 6.
A 54-year-old male internal carotid artery (ICA) aneurysm patient 2 years after the operation (Patient 5). He had no major surgery-related difficulties and stated that after 12 years of follow-up and uncertainty, he was very happy with the physical and psychological impact of the operation.
Discussion
We describe our experience with five consecutive cases undergoing surgery for extended lesions affecting the ICA covered by the mandible. Five patients were operated on for high ICA lesions: 2 for malignant head and neck tumors, 1 for an extended paraganglioma, and 2 for large symptomatic ICA aneurysms. All ICAs were reconstructed with autologous vein interposition grafts and the distal anastomosis was within 3 cm from the bony carotid canal.
When surgically approaching the distal ICA close to the skull base from a standard lateral incision, the operative field is progressively narrowed and the approach complicated by the location of cranial nerves. After dividing the digastric muscle, a retroparotid dissection is continued, the mandible is subluxated, and the styloid process may be resected, however, the glossopharyngeal and vagus nerves lie just medial to the styloid process and may be damaged already during this procedure. The mastoid process, the mandibular ramus and condyle, and the styloid process eventually make it impossible to expose the ICA without osteotomy or resection.2 The mandible has to be luxated and/or divided and the styloid process has to be resected.1, 2, 3 In a cadaveric anatomic study by Beretta et al, even with these risky procedures, the last 10 mm of ICA before the skull base were left unexposed and the operative field remained narrow (range, 5-49 degrees) making a distal anastomosis hazardous or impossible to perform.2 Exposure of the part 1 cm immediately below the base of the skull has been reached through a posterior approach by performing radical mastoidectomy.1 Alimi et al presented a method to reach parts of the ICA within the carotid canal after radical mastoidectomy, complete rerouting of the third portion of the facial nerve, and reaming the canal open in 7 patients with significant neurologic deficit after blunt injury to the internal carotid artery.6 Surgical ligation of the ICA carries a high risk of stroke and the risk cannot be fully estimated with preoperative occlusive tests.16 Ligation of the ECA carries no known major risks, but in spite of that we decided to reconstruct it in two cases. We wanted to keep the vasculature of the area as good as possible and, in these cases, the reconstruction seemed to add very little to the operative risk.
The midline and paramidline mandibulotomies, with a lateral luxation of the ipsilateral mandible, give an excellent exposure to the oral cavity and the oropharynx. This method is in routine use in tumor surgery, when adequate exposure is required. The skull base may be widely exposed and the distal ICA runs lateral to the nasopharyngeal cavity superficially under the mucous membrane. The sterility of this operative field is obviously compromised, but when minimizing the use of prosthetic material and using broad-spectrum antibiotics we have not encountered major infection problems that could not have been controlled in this highly vascular region. The operation times varied a lot due to the differences in the disease processes. The aneurysm operations needed no extra dissections and took a fairly short time (148 and 261 minutes) whereas the extensive tumor surgery took clearly longer (550-705 minutes, including the tracheostomies).
Aneurysms of the extracranial portion of the ICA are rare, accounting for only 0.1-2% of all surgical procedures affecting the ICA and most are effectively treated using the standard lateral cervical incision approach. Due to the lack of a large patient series, the natural history of the disease is unclear and the indications for reconstruction are controversial. However, it is clear that conservative treatment is not plausible in extensive cases, even though the operative risk is high. Endovascular methods have been used and suggested as a first-line treatment.17 However, anatomical circumstances often make endovascular methods difficult and risky to perform. Trinidad-Hernández et al presented a saccular aneurysm case with an abundant redundant loop of the ICA, treated successfully with a combined surgical straightening of the loop and stenting and coiling of the aneurysm.18 There is insufficient data to draw any definite conclusions on which method to choose in the management of high ICA aneurysms.
Tumor invasion in the ICA is also surgically challenging and neck tumors involving the distal ICA are often considered inoperable. Radical tumor excision is, on the other hand, the only curative treatment for malignant neck tumors and might be considered in selected cases also in spite of arterial invasion. The conventional method in neck tumor surgery is to dissect the tumor sharply away from the carotid sheath. However, as carotid interposition is a method in routine use in vascular surgery and can be performed with minor added morbidity it seems obvious that in some cases interposition should be performed instead of taking a risk of incomplete tumor resection.15, 19, 20
Cranial nerve injuries seem to be a frequent problem in these patients. Only one aneurysm patient had no major cranial nerve deficit. The 3 tumor patients had tumor growth that made the sacrifice of the nerves obligatory. In the second aneurysm patient the injuries might have been avoided with surgical perfection, but this is impossible to know afterwards. During the study period 1 patient with acute traumatic pseudoaneurysm of the distal ICA was treated in our institution endovascularly with stent coverage. Due to compression of a large hematoma, he had to remain intubated for 7 days in the intensive care unit. After extubation he had hypoglossal and glossopharyngeal nerve injuries which were still persistent 1 year postoperatively. The cranial nerve injuries were either due to the original stabbing trauma or due to the prolonged hematoma distension. Also aneurysms can cause compression and distension to the adjacent cranial nerves and, thus, cranial nerve injury may be possible even with endovascular methods.
One further patient (not included in this series) was operated on by the same team, for high ICA aneurysm with superior extension behind the styloid process, leaving ICA disease-free for 3.5 cm below the opening of the carotid canal. In this patient we used an extended lateral approach with resection of the styloid process and mandibular subluxation, but no osteotomy. He also suffered from glossopharyngeal nerve injury emphasizing that the risk for cranial nerve problems is not unique to the midline mandibulotomy approach.
One patient in this series died due to aspiration pneumonia (Patient 3). However, she had several aspiration pneumonias already prior to surgery and it was difficult to decide whether this pneumonia was due to the cranial nerve injuries or her previous morbidity. Another previously healthy patient who had a tracheostomy (Patient 4) had a mild aspiration pneumonia that was managed with antibiotics. The surgeon should maintain a low threshold for the use of prophylactic surgical adjuncts such as tracheostomy and gastrostomy to lessen the risk of aspiration events in the postoperative period.
We believe that medial mandibulotomy gives a clearly wider exposition than lateral approaches and, therefore, a more distal ICA reconstruction is possible. To further avoid injuries to the cranial nerves, careful dissection should be performed and microscopic techniques could be considered.
Conclusion
In carefully selected cases, it may be optimal to use the described multidisciplinary approach and medial mandibulotomy exposure in otherwise inoperable patients with tumors or aneurysms of the distal ICA close to the skull base. Patients should be informed about the risk of cranial nerve deficits.
Author contributions
The authors want to thank Pekka Paavola, MSc (Tech), for the graphic work for Fig 1 and photographers Jarmo Nummenpää and Mikko Hinkkanen for taking the photos and helping in the preparation of the images.
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Competition of interest: none.
PII: S0741-5214(08)01398-0
doi:10.1016/j.jvs.2008.08.047
© 2009 The Society for Vascular Surgery. Published by Elsevier Inc. All rights reserved.
