Jugulotympanic paragangliomas (JTPs) are rarely encountered benign diseases derived embryonically from the autonomic nervous system. Although JTPs may originate extracranially or intracranially, little has been reported in the literature about large JTPs involving several anatomical structures in the craniofacial regions. Management of large JTPs is controversial. The authors describe a large JTP invading the cranial bones and extending through the neck to the left clavicle. Doppler sonography, computed tomography and magnetic resonance imaging were performed preoperatively to confirm the diagnosis. Combined therapeutic approaches were undertaken with preoperative selective embolization followed by craniofacial resection in cooperation with neurosurgeons.
Paragangliomas are highly vascularized, benign neoplasms derived from neural crest cells. Paragangliomas of the head and neck are rare, accounting for only 0.6% of all neoplasms within this region. They have long been referred to by the site of origin (e.g. carotid body tumours (CBTs), jugular paragangliomas (JPs), vagal paragangliomas (VPs) or tympanic paragangliomas (TPs)) . JP arises in the adventitia of the dome of the jugular bulb and it frequently causes dysfunction of the surrounding cranial nerves VII–XII and progressive bone destruction because of its proximity to the jugular foramen and skull base bones. TP typically arises from the cochlear promontory. Pulsatile tinnitus and conductive hearing loss may be encountered in TP cases when there is interference in the auditory ossicular chain. The distinction between JPs and TPs can no longer be made because of the proximity of the cochlear promontory to the jugular fossa, hence the term jugulotympanic paraganglioma (JTP) . To the best of the authors’ knowledge, there has been no report of a JTP case with both large intracranial invasion and whole neck involvement. The management of JTPs is controversial. The authors present a case of a large paraganglioma with detailed diagnostic and therapeutic aspects for further discussion.
A 44-year-old female patient with a history of hearing loss presented to the authors’ department with a large, painless mass in the left neck, complaining of persistent dizziness and headache. Her medical history included a left-sided progressive hearing loss 7 years prior to the discovery of visible mass, which was discovered 3 months previously. On physical examination, a rubbery, pulsatile lesion with well-defined contours was located in the left neck. The size of the mass was about 14.5 cm × 6 cm × 4.5 cm, whilst the upper border of the mass could not be determined by physical examination, the lower end was palpated at the level of the clavicle. There was mild restriction of head rotation to the right.
The patient underwent vocal cord function assessment by flexible fibreoptic laryngoscopy and no remarkable difference was discerned. Evaluation of her hearing function by pure-tone audiometry showed severe conductive hearing loss. Duplex ultrasound ( Fig. 1 A) revealed an oval, well-demarcated, heterogeneous mass in the lateral neck and variable intratumoural flow signals could be detected. Computed tomography (CT) of the head showed a large tumour expanding through the neck and a ‘moth eaten pattern’ of erosion of the jugular foramen by the tumour offered a clear view of the intracranial protrusion of the tumour. On magnetic resonance imaging (MRI), the tumour was hyperintense with T2-weighted MRI and isointense relative to muscle with T1-weighted MRI. Multiple serpentine and punctuate regions of signal void could be pinpointed throughout the mass ( Fig. 1 B–D). Carotid digital subtraction angiography (DSA) through femoral catheterization allowed visualization of the specific vascular supply to the tumour, which comprised the occipital artery, thyrocervical trunk and muscular branches of the vertebral artery. Preoperative embolization of the former two arteries was performed to reduce the blood loss ( Fig. 1 E and F). A balloon occlusion test was carried out to assess the safety of the internal carotid artery during the surgery. The petro-occipital trans-sigmoid approach combined with a transcervical approach was performed to remove the tumour. A C-shaped postauricular incision extending from above the ear to the level of clavicle was made crossing between the mastoid process and the angle of the mandible. Resection of the tumour in the neck was first carried out with a bottom-up approach and the internal carotid artery was preserved during the process. The main trunk of the facial nerve was then located midway between the cartilaginous tragal pointer of the external auditory canal and the posterior belly of the digastric muscle. The left facial nerve was traced via cautious exploration to the stylomastoid foramen. The fallopian canal in the petrous temporal bone was exposed and the intratemporal segment of the facial nerve was preserved. A mastoidectomy was subsequently performed to uncover the junction of the sigmoid and transverse sinuses. A 4 cm × 6 cm retrosigmoid craniotomy was undertaken immediately after the mastoidectomy. Bone removal continued beneath the labyrinth and posterior semicircular canal to further expose and remove the tumour from surrounding neurovascular structures ( Fig. 2 A and B ). The postoperative pathologic findings confirmed the preoperative diagnosis ( Fig. 2 C and D). After 9 months’ follow up, there was no evidence of cranial nerve damage or tumour recurrence, although her hearing dysfunction persisted ( Fig. 2 E and F).
Head and neck paragangliomas are neuroendocrine tumours originating from paraganglia of the parasympathetic nervous system. In 1941, the name jugular paraganglioma was first proposed by Stacy Guild. In 1953, the discrepancy between JP and JTP was noted by Rossenwasser . Most paragangliomas are sporadic, but they can be familial with autosomal dominant inheritance and incomplete penetrance. It is now claimed that mutations in the SDHB (1p35–36) and SDHD subunits (11q23) lead to head and neck paragangliomas . Malignant transformation of head and neck paragangliomas is recognized with approximately the same frequency (2–13% of cases) as in paragangliomas elsewhere in the body .
Although paragangliomas of the head and neck are generally benign, rare lesions, clinicians and pathologists are still confused about the diagnosis and treatment modalities . The clinical symptoms vary according to size and location of the paraganglioma.
TP and JP sometimes have a similar presentation. They are initially asymptomatic, but with progression they can invade the skull base, affect adjacent cranial nerves and cause the specific ‘jugular foramen syndrome’. Regarding clinical diagnosis it is challenging to distinguish TP from JP on the physical presentation alone . Most often, the confirmation of diagnosis requires imaging . Colour-coded Doppler sonography is useful and non-invasive for primary assessment, but confined to those that occur exclusively in the neck. MRI demonstrates a characteristic ‘salt and pepper’ signal with T1-weighted and hyperintense T2-weighted images for larger tumours. MRI also provides for the evaluation of these tumours in relation to surrounding soft tissue and vascular structures .
Limitations of MRI, which may be overcome by CT, include middle ear ossicular assessment and evaluation of bony erosion at the skull base, such as the temporal bone and jugular fossa. On high-resolution CT scans of the temporal bones, erosion of the jugular foramen with a moth-eaten pattern characterizes the JP tumour. The tumour spreads along the path of least resistance and the hypotympanum, mesotympanum, and the sinus tympani, ossicular chain can be invaded . The most reliable procedure to confirm the diagnosis of a head and neck paraganglioma is DSA. DSA also provides a vessel ‘map’ and identifies the blood supply and flow dynamics of the tumour .
Preoperative embolization is a useful adjunct in the treatment protocol of large JTPs. It is thought that a tumour larger than 3 cm is ideally suited for embolization . The risks of potential complications from embolization are always outweighed by the advantages, which include shrinkage in tumour vascularity and size as well as a consequent reduction of intraoperative blood loss . Resection is facilitated because intraoperative bleeding is decreased and also because the tumour is transformed into a rigid avascular mass that is well delineated against the surrounding normal tissue. These advantages allow en bloc removal of the tumour, particularly in the cervical region .
The management of JTPs poses a particular challenge because of their hypervascular nature, advanced stage at diagnosis and difficult anatomic location. The current main treatment modalities for head and neck paragangliomas are surgery or radiation therapy . Data do not exist to determine which treatment modality (radiotherapy or surgery) is better, especially for large JTPs. Although almost all CBTs and low VPs are treated surgically, management of JTP remains controversial due to serious postoperative complications including cerebrospinal fluid leak, meningitis, stroke, hearing loss, and multiple lower cranial nerve palsies. The effects of radiotherapy have also been questioned by many clinicians owing to reports of radiation-induced neoplasm, conflicting statistics on local control rate and the increased difficulty of surgery after radiation . Irradiation for residual tumours after surgery has also been used occasionally, but there is no consensus on the effects of the combined approaches. Definitive selection of treatment must be based on the comprehensive consideration of biologic activity of the tumour, patient age and condition, tumour site, and potential for treatment related morbidity . Surgery is still regarded as curative, whilst radiation therapy is viewed as a tumour control or palliative therapy. Developments in microsurgery and craniofacial surgery, mean that local surgical control is now claimed to have achieved success rates of 80–90% in most surgical series . Most authors still consider surgery to be the treatment of choice for the majority of patients with cervical paragangliomas. The authors consider that for patients with JTPs, surgery should be the first option for young patients. The size of the tumour is no longer a contraindication for surgery, especially when patients experience significant clinical symptoms such as pain and headache. Both small and large jugulotympanic tumours can be resected, but radical surgery should always be meticulously planed and performed with the aim of minimal morbidity, especially for large tumours. Regarding the access for surgery for JTPs, conservative jugulopetrosectomy can preserve the normal anatomy of the external and middle ear, but it is indicated for small tumours confined to the jugular foramen and infralabyrinthine area . An incision placed behind the postauricular crease and extended inferiorly and superiorly can expose the neck and temporal bone. Facial nerve mobilization is usually required during mastoidectomy, permitting conservation of facial functions. When the tumour extends beyond the jugular foramen into the neck, the authors recommend an extended infratemporal fossa approach with a large C-shaped incision which allows exposure of the petro-occipital skull base, neck, and infratemporal fossa.
Radiation or a wait-and-see approach should only be the choices for cases with residual or recurrent tumours after surgery, for old patients with possible postoperative mortality related to pharyngolaryngeal paralysis or for those with serious general condition problems. Stereotactic radiosurgery can be performed for jugulotympanic tumours in patients who are not surgical candidates.
Although management of JTPs must be tailored to the individual patient and the clinical situation, the authors consider surgery should be the first choice, especially for large JTPs with intracranial extensions, patients suffering from persistent neuropathy or tumours suspected of malignant change. A thorough preoperative diagnosis and plan is the key to the surgical management of JTPs. The authors strongly suggest preoperative embolization for large JTPs.