Current perspectives in the management of glomus jugulare tumors.

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NI Feature: CENTS (Concepts, Ergonomics, Nuances, Therbligs, Shortcomings) REVIEW ARTICLE

Current perspectives in the management of glomus jugulare tumors Narayan Jayashankar, Suresh Sankhla1 Department of Otorhinolaryngology and Skull Base Surgery and 1Neurosurgery, Nanavati Superspeciality Hospital, Vile Parle, Mumbai, Maharashtra, India

ABSTRACT Glomus jugulare tumors are benign but locally aggressive tumors. Their location, spread to adjacent areas and biological behavior have been extensively studied and reported. However, controversy exists regarding the role of surgery and stereotactic radiosurgery. The optimal plan of management of the tumor in close proximity to the facial and lower cranial nerves, the internal carotid and vertebral arteries, the venous sinuses, and the neuraxis is still nebulous. This review will discuss the differing viewpoints and attempts to propose a rational strategy in dealing with these tumors Key words: Glomus jugulare; glomus tumors; paraganglioma

Introduction Glomus jugulare are benign tumors that are slow growing, but locally aggressive. The tumor takes its origin from the paraganglionic cells in the adventitia of the jugular bulb. It spreads along pathways of least resistance like the infralabyrinthine and infracochlear cell tracts toward the vertical infratubal segment of the internal carotid artery (ICA), along the petrous segment and then toward the nasopharynx. The medial wall of the jugular bulb acts as a barrier to tumor spread. Once this barrier is breached, the tumor spreads to involve the lower cranial nerves and can also spread intracranially. Inferiorly, it spreads to the neck through the carotid foramen and the carotid sheath. The management of these tumors has been debated with various options being observation, surgery, and gamma knife Access this article online Website: www.neurologyindia.com DOI: 10.4103/0028-3886.152661 PMID: xxxxx

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radiosurgery. The morbidity associated with treatment of these lesions has led to refinements in the surgical technique including ways to preserve the facial and lower cranial nerve function (including subtotal resection, in selected cases). Improvements in interventional neuroradiology have made it possible to deal more effectively with lesions involving the internal carotid or vertebral artery. Rapidly expanding scope of stereotactic radiosurgery has added a further dimension to the treatment options. Hence, a review of the current status of its treatment modalities is necessary.

Literature Review Patient demographics Paragangliomas arise as sporadic or familial entities. All types of paragangliomas are four to six times commoner in female than in male patients. However, males are more commonly affected in the familial type.[1,2] The peak incidence of paragangliomas is in the 4th or 5th decade of life; however, subjects with familial etiology present at a younger age.[3,4] It has now been recognized that approximately 30% of apparently sporadic head and neck paragangliomas are due to germline mutations in one of the genes SDHB, SDHC, and SDHD. Also, the SDHB mutations are associated with a higher percentage of malignant transformation.[5]

Address for correspondence: Dr. Narayan Jayashankar, Narayan Clinic, 14 A Road, Ahinsa Marg, Khar West, Mumbai - 400 052, Maharashtra, India. E-mail: [email protected]

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Clinical features and investigations The most common presenting symptom for glomus jugulare tumors is hearing loss that is present in approximately 60–80% of cases with many subjects also complaining about their pulsatile tinnitus.[6-8] The other symptoms include hoarseness, dizziness, or dysphagia. Facial paresis is occasionally present. A history of palpitations and headaches is suggestive of catecholamine excess but is extremely rare for head and neck paragangliomas. In the case of any suspicion, a 24-hour urine sample is analyzed for epinephrine, dopamine, and vanillymandelic acid. If elevated, 1,231-metaiodobenzylguanidine (mIBG) scintigraphy and MRI of the chest and abdomen may be used to localize the additional extracranial lesion. Catecholamine excess is found in the familial etiology group due to the concomitant presence of a pheochromocytoma in the paraganglioma syndromes.[9] Since catecholamine excess is rarely found in head and neck paraganglia, in case it is discovered, it should be assumed to be from a synchronous thoracic or abdominal lesion unless proved otherwise. High-resolution computed tomography (HRCT) and T1weighted (T1W), T2-weighted (T2W), and T1-weighted gadolinium-enhanced MRI sequences are necessary for identification of the suspected pathology as also the extent of the lesion. HRCT scan will show a moth-eaten appearance of the bone of the jugular fossa and erosion of the caroticojugular spine. Paraganglia give a low to intermediate signal on T1W and a high signal on T2W sequences. The salt and pepper appearance seen on T2W images is due to intratumoral vasculature appearing as flow voids.[10] The scans give adequate information about the likely pathology and Table 1: Modified Fisch classification for glomus jugulare tumors Class C C1 C2 C3 C4 Class D De1 De2 Di1 Di2 Di3 Class V Ve Vi

To study the vascular supply of the glomus tumor, angiography is performed prior to superselective embolization of the feeder vessels at our institute. The embolization is preferred around 48 h prior to surgery, especially when polyvinyl alcohol is used as the embolic material. Devascularization of the glomus tumor reduces its size, makes it firmer in consistency and decreases blood loss during surgery.[13] Embolization of feeders from the external carotid artery and its ascending pharyngeal branch is routinely performed. Figure 1a and b show the effect of embolization on tumor devascularization. However, care needs to be exercised in dealing with feeders from the ICA and the vertebral artery. Therapeutic embolization of feeders from these major vessels may be performed in free-flow conditions or with a temporary balloon occlusion of these vessels. However, if these feeders are small, it may be wiser not to embolize these vessels to essentially minimize the risk of stroke associated with dissemination of embolic material to the brain. Temporary balloon occlusion is also used to assess whether or not carotid sacrifice would be possible in desired cases.[14] In instances where the ICA is encased, an alternative to the surgical sacrifice of ICA is its preoperative stenting. This prevents the risk of the carotid rupture during surgery around the encased vessel.[15] Conservative versus an infratemporal fossa approach For small C1 tumors with minimal jugular bulb involvement, the hypotympanic approach has been described.[16] However, this approach does not offer proximal and distal control over the jugular bulb or the ICA. A complete removal of the tympanic bone (that is invariably infiltrated) is impeded. Not

Tumors destroying the jugular foramen and bulb with limited involvement of the vertical portion of the carotid canal Tumors invading the vertical portion of carotid canal (infratubal segment of ICA) Tumors invading the horizontal petrous segment of carotid canal Tumors reaching the anterior foramen lacerum and along the internal carotid artery to the cavernous sinus Tumors with upto 2 cm dural displacement Tumors with more than 2 cm dural displacement Tumors with upto 2 cm intradural extension Tumors with more than 2 cm intradural extension Inoperable intracranial intradural tumors Tumors engulfing the extradural vertebral artery Tumors involving the intradural vertebral artery

ICA - Internal carotid artery

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thus no biopsy is required for confirmation of the diagnosis. Based on the scans, the lesion is staged. Staging for glomus was popularized by Fisch[11] and modified by Sanna.[12] This modified classification is described in Table 1.

a

b

Figure 1: (a) Angiography showing vascular supply to the glomus tumor. (b) Devascularization of the tumor following embolization



being able to excise the styloid process inhibits control over the ICA, parapharyngeal space and also the lower cranial nerves. All these factors could result in incomplete excision of the tumor. A transjugular approach with preservation of the facial nerve may be used for C1 glomus jugulare tumors with a predominantly posterior or an intracranial extension.[17] However, it may be difficult to access the ICA using this approach. The approach also offers a limited anterosuperior exposure. Preservation of the posterior canal wall in class C tumors invites the risk of leaving behind residual tumor. Hence, in class C tumors, the recommendation is to perform a “canal wall down mastoidectomy” with drilling of the tympanic bone, excision of the styloid process, and obtaining a good exposure and control of the internal jugular vein, ICA, and lower cranial nerves in the jugular foramen and neck. All these steps are incorporated in the infratemporal fossa A approach described by Fisch.[18] Surgical technique of the infratemporal fossa A approach for exposure of the jugular foramen A C-shaped incision is taken from the top of helix in the midtemporal area, 2.5–3 cm behind the postaural groove upto the mastoid tip, coursing two finger-breadths below the angle of mandible up to the greater cornu of the hyoid bone. The skin and subcutaneous layers are elevated and reflected anteriorly. The neck flap is elevated in the subplatysmal plane. A rectangular-shaped musculoperiosteal layer is created just posterior to the external auditory canal, which helps in a two layered cul-de-sac closure of the external auditory meatus [Figure 2]. The external auditory canal is transected circumferentially at the level of the spine of Henle. The cartilage is excised from this lateral half of the transected external auditory canal till a circumferential

Figure 2: Rectangular musculoperiosteal flap created posterior to the external auditory canal is used as second layer cul-de-sac closure. Facial nerve is identified at its exit from stylomastoid foramen till distal upper and lower divisions. Control of ICA, ECA, and IJV is taken in the neck along with lower cranial nerves. Mpf = Musculoperiosteal flap, MC = Mastoid cortex, FN = Facial nerve main trunk distal to stylomastoid foramen, ICA = internal carotid artery, ECA = External carotid artery, IJV = Internal jugular vein

skin cuff is created which is everted and sutured as the first layer of cul-de-sac closure of the external auditory canal. The rectangular musculoperiosteal layer created earlier is used as a second layer closure. The skin of the medial half of the external auditory canal together with the malleus and the incus (after dislocation of the incudostapedial joint) is excised. The greater auricular nerve that courses along the lateral surface of the upper part of the sternocleidomastoid muscle is preserved or harvested. The anterior border of the sternocleidomastoid muscle is separated from its covering cervical fascia, and its attachment to the mastoid is divided. This helps to retract the sternocleidomastoid muscle and the temporalis muscles posteriorly. The ICA, external carotid artery, and the internal jugular vein are identified, and silicone tubing is loosely placed around them for later control if needed [Figure 2]. The IX, X, XI, and XII cranial nerves are identified. The facial nerve distal to the stylomastoid foramen is delineated including its distal upper and lower divisions in the parotid gland [Figure 2]. A “canal wall down mastoidectomy” is performed. The mastoid tip is excised [Figure 3]. The facial nerve is decompressed in 270 degrees circumference from the geniculate ganglion till the stylomastoid foramen area. At the stylomastoid foramen area, the periosteum is left around the facial nerve. The facial nerve is lifted off its bed and freed from the geniculate ganglion till the distal upper and lower divisions in the parotid [Figure 4]. The facial nerve is then transposed anteriorly by lodging it in the parotid tissue [Figure 5] and suturing the parotid tissue over the nerve so as to create a tunnel for the facial nerve. The tympanic bone is drilled off. The styloid process is exposed by dissecting the muscles off it and excised. This exposes the underlying ICA. The bone over the sigmoid sinus and jugular bulb is taken off to expose the tumor over the jugular bulb. However, a

Figure 3: Mastoid tip (MT) excision. SCM = Sternocleidomastoid muscle, FN = Facial nerve main trunk distal to stylomastoid foramen


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Figure 4: Facial nerve mobilized from geniculate ganglion (GG) to distal upper and lower divisions in parotid. Note the tumor medial to it in jugular foramen. FN = Facial nerve, lsc = lateral semicircular canal, SS = Sigmoid sinus

Figure 5: Complete anterior transposition of facial nerve. FN = Anteriorly transposed facial nerve, T = Tumor in infralabyrinthine and infracochlear compartment

small shelf of bone is kept intact over the upper end of the sigmoid sinus to facilitate its extraluminal packing. The infracochlear cells are drilled off. The drilling can extend anteriorly to expose the infratubal vertical segment of the ICA when desired based on the tumor spread. In type C3 tumors, the infratemporal B approach is used. In this approach, the anterior canal wall is drilled off, and the temporomandibular joint is exposed. Drilling proceeds anteriorly from the base of zygoma. The middle meningeal artery and mandibular nerve are transected. The horizontal petrous segment of the ICA is exposed along with the tumor over it. Drilling can proceed anteriorly until the foramen lacerum where the ICA is seen to course superiorly along its paraclival segment. In case the tumor has destroyed the cochlea and is infiltrating toward the petrous apex, a transcochlear approach is performed. When the tumor extends into the sphenoid sinus or the nasopharynx, these need to be opened up. This forms the basis of infratemporal fossa C approach. In tumors extending posteriorly from the jugular foramen, a far or extreme lateral approach is performed depending on the tumor spread.

periosteum and surrounding tissue around the facial nerve at the stylomastoid foramen so as to preserve the vascular supply from the stylomastoid artery and suggested that it leads to improved results.[19,20] Fallopian bridge technique was also proposed for certain C1 tumors.[21,22] In this, the facial nerve is left intact within the fallopian canal in its vertical (mastoidal) segment with drilling of infralabyrinthine and infracochlear cells, tympanic bone and excision of the styloid process deeper to it to excise the tumor [Figure 6]. Similarly, mobilization of the facial nerve from the second genu till the distal upper and lower divisions in the parotid gland has also been described.

Management of the facial nerve In the infratemporal fossa approach, the facial nerve is freed from the geniculate ganglion till the distal upper and lower divisions in the parotid gland. It must be noted that periosteum is left around the facial nerve at the stylomastoid foramen area to retain some nourishment for the nerve and also to aid in its anterior transposition. The facial nerve is then transposed anteriorly lodging it in a new tunnel created in the parotid gland [Figure 5]. This exposes the entire infralabyrithine area, infracochlear area, the jugular foramen, and anteriorly, the ICA. Various modifications have been proposed that attempt to preserve the facial nerve function. Brackmann and Leonneti et al., suggested maintenance of 86

Review of the literature shows that mobilization of facial nerve from the second genu until the distal upper and lower divisions in the parotid gland results in 93% subjects having House Brackmann grade I or II function at long-term follow-up. Anterior transposition of the facial nerve, however, results in a transient paresis to the subjects in the immediate postoperative period. Sanna et al.,[23] reported recovery of facial nerve functions at 1 year to House Brackmann grade I or II in 66.7% subjects who preoperatively had intact facial functions and were subjected to its anterior transposition. Fisch[24] obtained return of facial function to House Brackmann grade I or II in 87% subjects after anterior transposition in 1 year. Limited mobilization of the facial nerve, however, carries with it the risk of stretch of the nerve and also increases the chances of its accidental injury during drilling of the bone or its manipulation during excision of the tumor below it. Also, it is sometimes essential to displace the nerve forwards and backwards (from the position achieved during its partial anterior mobilization to its original position) to work in the limited space along the vertical infratubal segment of ICA especially in class C2 tumors. Considering the excellent exposure obtained by complete anterior transposition, the



greater risk of injury to a partially mobilized nerve, and the almost comparable postoperative facial nerve recovery, it seems reasonable to perform complete anterior transposition of the facial nerve. This additionally helps in achieving complete tumor clearance. Management of the facial nerve that appears involved [Figure 7] has been clearly defined by Fisch.[11,25] In cases of grade I involvement (tumor is 1mm or more from the perineurium), the tumor bulk is gently dissected away from the facial nerve epineurium. In grade II involvement (epineurium invaded), the epineurium is resected leaving the perineurium intact. When the perineurium (grade III) or endoneurium (grade IV) is invaded, the nerve needs to be resected [Figure 8] and an end-to-end anastomosis or an interposition nerve grafting is performed between the two cut ends of the facial nerve. Grafting is performed using greater auricular or sural nerve grafts. Rarely, in cases where

Figure 6: Fallopian bridge technique. Facial nerve left in fallopian canal and tumor exposed medial to it. FC = Fallopian canal, T = Tumor

Figure 8: Involved segment of facial nerve resected. Fresh cut end of uninvolved segment of facial nerve seen. FN = Facial nerve

grafting is not feasible due to extensive involvement of the proximal segment of the facial nerve, a second stage facialhypoglossal anastomosis is an option. Management of ICA Management of ICA is a subject of intense discussion, and we shall only highlight the important considerations. Involvement of the ICA is assessed preoperatively by magnetic resonance angiography (MRA). In class C2 and C3 tumors where the lumen of ICA appears uninvolved on imaging, the tumor is usually adherent to the periosteum. An area free of tumor is to be identified inferiorly (at the level of proximal ICA). The periosteum around the ICA is then safely dissected off from its walls in this zone.[26] The periosteum is much tougher along the vertical infratubal segment of the ICA than at the horizontal petrous segment [Figure 9]. In certain cases, it is possible to mobilize the vertical segment

Figure 7: Facial nerve involved with tumor. FN = Facial nerve, StF = Stylomastoid foramen area

Figure 9: Anatomy of jugular foramen showing the periosteum covering ICA. JB =Jugular bulb, P = Periosteum covering seen over the ICA, XI = Accessory nerve, Co = Cochlea, FN = Anteriorly transposed facial nerve


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of ICA and to work anteromedial to it to clear the tumor. However, care has to be taken to avoid bleeding from the caroticotympanic branch of the ICA which usually arises from close to its horizontal segment and the genu. Also, it has been found that limited mobility of ICA is achieved when anterior petrosal approach is used as compared to the infratemporal fossa approach.[27] In case adventitia of the ICA is involved, a subadventitial dissection can also be performed. However, this is possible only in the vertical, infratubal segment since the adventitia is thicker in this segment.[28] Although possible, it carries with it a risk of a blowout. In cases with proven involvement of the wall of the ICA (seen as irregular narrowing of the ICA on imaging), a preoperative balloon occlusion test is mandatory. The surgical options include sacrifice of the involved ICA (with bypass, when the cerebral cross-circulation is inadequate) or its preoperative stenting. Preoperative stenting is nowadays preferred to the carotid artery sacrifice.[29] Preoperative stenting of the ICA also facilitates removal of the tumor closer to its lumen without the risk of its rupture.[15,23,30,31] Most studies indicate a tendency to avoid carotid sacrifice. A less aggressive option is to subject the residual tumor over ICA to postoperative radiosurgery. Management of the sigmoid sinus and the jugular bulb A thin shelf of bone is left over the upper end of the sigmoid sinus. This is to facilitate its extraluminal compression to control venous bleeding during surgery. An extraluminal compression is the preferred option to control venous bleeding than intraluminal compression as the latter is associated with the possible risk of embolization as well as the risk of retrograde thrombosis of the transverse sinus and the vein of Labbe. The internal jugular vein is ligated in the neck. It is dissected off the surrounding tissues and passed under the accessory nerve toward the jugular foramen. The lateral wall of the sigmoid sinus is excised along with the tumor and the internal jugular vein. At this point, brisk bleeding ensues from the openings of the inferior petrosal sinus located in the medial wall of the jugular bulb. These openings are meticulously packed with surgicel without any undue pressure since the lower cranial nerves traverse beneath the medial wall of the jugular bulb. Bleeding also arises from the posterior condylar vein, which is also controlled with surgicel. Complete ligation and excision of the sigmoid sinus is avoided as requires an additional dural patch to prevent a cerebrospinal fluid leak. When the tumor is extradural and has not invaded the medial wall of the jugular bulb, the cervical course of the lower 88

cranial nerves is traced superiorly toward their exit at the skull base (medial to the medial wall of the jugular bulb) and preserved. Intrabulbar dissection is also performed to preserve the medial wall of the jugular bulb.[32] However, if the tumor has invaded the medial wall of the jugular bulb, it becomes almost impossible to preserve the function of the lower cranial nerves if total resection is attempted. The alternative is to leave a sliver of tumor over the lower cranial nerves to avoid compromising their function. However, in the younger age group, complete excision is preferred even at the expense of transient loss of lower cranial nerve function since a good postoperative recovery of swallowing and speech function is usually expected. However, in the elderly patients, preservation of the lower cranial nerve function gains precedence over complete removal of the tumor. Intradural extensions A single stage surgery is often recommended for intradural extensions of the tumor.[32-34] Small intradural extensions may be excised along with the involved dura in a single stage. However, in larger defects, it is not always possible to plug the defect securely. The opening of the fascial planes in the neck and extensive bony drilling further prevents a watertight dural closure. Hence, the risk of cerebrospinal fluid (CSF) leak has been quoted as ranging from 3.8 to 33.3% in different series.[32,35,36,37] In comparison, the incidence of CSF leak in a second stage surgery is extremely low (4.4%).[12] The reasons for propagating a two-staged surgery in patients with a large intracranial extension are: (i) blockage of the sigmoid sinus and the ensuing venous congestion may precipitate raised intracranial pressure that may cause CSF leak through the large dural defect; ii) removal of extensive intracranial lesions in close proximity to the lower cranial nerves may lead to their paresis. This may precipitate severe coughing and aspiration pneumonitis in the early postoperative period. Severe coughing raises the intracranial pressure and may again precipitate a CSF leak; (iii) devascularization of the tumor during the first stage surgery decreases the intraoperative hemorrhage during the second stage surgery. This preserves the arachnoidal planes in the tumor-brainstem interface and also causes the tumor to shrink. Thus, tumor excision is facilitated; and, (iv) it is easier to seal dural defects in the second stage due to a smaller area of exposure and prior closure of communication with the fascial spaces in the neck. A small dural defect is plugged securely with a fat plug and covered by fascia. Fibrin glue is applied at its edges to obtain a good sealing of the defect. The whole cavity is then obliterated with fat. A large defect has to be obliterated first with a layer of fascia or dural substitute, which is held in place with fibrin glue and then the whole cavity is obliterated with



fat. Various local vascularized flaps like the temporalis muscle and sternocleidomastoid muscle have been tried.[38] However, these flaps have a limited rotational arc and may undergo atrophy producing a significant cosmetic deformity.[39] The postaural muscle, sternocleidomastoid, and the posterior belly of digastric are mobilized and sutured to the temporalis muscle. Thus, a tight musculoperiosteal layer closure is attempted over the fat placed within the tumor cavity. The subcutaneous and skin layers are sutured separately. No drain is kept. Tumor involving the vertebral artery Posteriorly based paragangliomas may involve the vertebral artery, lower clivus, and foramen magnum and require a far lateral or extreme lateral transcondylar approach for adequate exposure.[40] Usually, it is possible to separate the tumor from the vertebral artery by microdissection techniques. If the tumor has infiltrated the wall of the vertebral artery, a preoperative stenting facilitates its preservation during dissection. Alternatively, a nondominant vertebral artery may be sacrificed.[41] If the vertebral artery is encased and/or the lower cranial nerves are infiltrated by the tumor, then a subtotal resection is performed.[42]

Role of Gamma Knife Radiosurgery Stereotactic radiosurgery, by inducing vascular endothelial damage, may be particularly effective for vascular tumors, such as a glomus.[43] Pollock et al[44] have found tumor shrinkage by approximately 31% following stereotactic radiosurgery at a mean follow up of 44 months following radiotherapy. Other series also offer encouraging results.[45,46] Gottfried et al.,[47] compared the efficacy of surgery and radiotherapy in glomus jugulare tumors. They concluded that surgery is associated with higher morbidity rates but has the advantage of immediately and totally eliminating the tumor. The results of radiosurgery are promising; however, the incidence of long-term recurrence is at present not well defined. There is a consensus that surgery is the preferred option in young patients, in those with a catecholamine secreting paraganglioma, and in those with rapidly progressive neurological deficits.[48] As the target volume of the tumor increases, there is a proportional increase in the radiation dose on the surrounding normal tissues. For this reason, stereotactic radiosurgery is not suited for large lesions. However, for residual or small recurrent lesions, stereotactic radiosurgery is very effective.[49,50,51]

Surgery is the preferred option in the young and in medically fit middle aged to elderly patients in whom total extirpation of the tumor is the aim. Extensive infiltration of lower cranial nerves or the dominant vessels is an indication for a more conservative excision of the lesion. Improved surgical techniques have considerably decreased surgical morbidity. Speech and swallowing therapy as well as extensive physiotherapy have helped to overcome the morbidity arising due to lower cranial nerve paresis or palsy. In the elderly and medically unfit subjects with minimal symptoms, a close observation is an option. These subjects, if significantly symptomatic or showing disease progression, may be subjected to stereotactic radiosurgery. Stereotactic radiosurgery is the preferred option in residual or small recurrent tumors.

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Conclusions Management of glomus jugulare tumors requires a good knowledge of the temporal bone and cervical as well as intracranial anatomy to evaluate the extent and progression of the tumor and the type of surgical approach required.

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