Clinical Imaging 38 (2014) 655–658

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Hypoglossal canal invasion by glomus jugulare tumors: clinico-radiological correlation☆,☆☆ Merve Gursoy a,⁎, Emanuele Orru a, Ari M. Blitz a, John P. Carey b, Alessandro Olivi c, David M. Yousem a a b c

Division of Neuroradiology, The Russell H. Morgan Department of Radiology and Radiological Science, The Johns Hopkins Medical Institution, 600 N. Wolfe Street, Baltimore, MD 21287 Department of Otolaryngology, Head and Neck Surgery, The Johns Hopkins Medical Institution, 600 N. Wolfe Street, Baltimore, MD 21287 Department of Neurosurgery, The Johns Hopkins Medical Institution, 600 N. Wolfe Street, Baltimore, MD 21287

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Article history: Received 5 January 2014 Received in revised form 28 May 2014 Accepted 10 June 2014 Keywords: Glomus jugulare Hypoglossal canal Magnetic resonance imaging Computed tomography

a b s t r a c t The aim of this retrospective study is to assess the rate at which glomus jugulare tumors invade the hypoglossal canal (HC) and to correlate computed tomography (CT) and magnetic resonance imaging (MRI) findings with the clinical evidence of cranial nerve (CN) XII dysfunction. CT and MRI imaging modalities of 31 patients were blindly reviewed by an attending neuroradiologist. Imaging studies identified involvement in 22 tumors (22/31, 71.0%). Thirteen of 22 patients (59.1%) had clinically evident CN XII symptoms. Accuracy rate was 76.7% (23/30) for MRI and 78.6% (11/14) for CT. MRI showed 100% sensitivity but had only 59% specificity and the specificity for CT was 66.7%. When radiologists elucidate HC involvement, it may alter the surgical approach and may lead to more focused/accurate clinical evaluation of tongue function. © 2014 Elsevier Inc. All rights reserved.

1. Introduction Paragangliomas (PGs) of the head and neck region are rare tumors, representing 3% of all PGs, 0.6% of all neoplasms in the head and neck region, and 0.03% of all neoplasms [1]. These tumors arise from the paraganglia, clusters of glomus cells derived from the embryonic neural crest. These cells act as special chemoreceptors that are located along blood vessels and nerves [2]. These glomus body cells are sensitive to alterations in blood pH and oxygen and carbon dioxide balances [3]. Head and neck PGs can be divided according to their site of origin: Carotid body tumors (CBTs) arise at the carotid bifurcation, glomus jugulare (GJ) tumors arise in the jugular foramen, glomus vagale (GV) tumors are located along the path of the vagus nerve, and glomus tympanicum (GT) arises on the cochlear promontory of the medial wall of the middle ear cavity. PGs may be (1) asymptomatic and discovered incidentally during imaging studies performed for other reasons, (2) detected as a palpable neck mass, or (3) suggested as a diagnosis based on cranial neuropathies. Symptoms related to compression or invasion of structures such as the cranial nerves (CNs) (especially IX, X, XI, and XII) may reveal the presence of a PG or help the clinician to diagnose these tumors. Symptoms associated with GJ tumors that may invade ☆ No grant support. ☆☆ No disclosures. ⁎ Corresponding author. The Johns Hopkins Medical Institution, 600 N. Wolfe Street Phipps B100F, Baltimore, MD 21287, USA. Tel.: +1-410-955-2685; fax: +1-410-614-1213. E-mail address: [email protected] (M. Gursoy). http://dx.doi.org/10.1016/j.clinimag.2014.06.009 0899-7071/© 2014 Elsevier Inc. All rights reserved.

the jugular foramen or hypoglossal canal (HC) include loss of sensation of taste on the posterior third of the tongue and swallowing dysfunction (CN IX), aphonia or weak/hoarse voice (CN X), shoulder drop, atrophy of the trapezius and sternocleidomastoid muscle (CN XI), and deviation and atrophy of tongue toward the affected side (CN XII). These clinical manifestations of lower CN invasion may become evident in the late phases of PGs’ growth [4–8]. The aim of this study was to assess the rate at which GJ tumors invade the HC determined by imaging findings and to correlate these computed tomography (CT) and magnetic resonance imaging (MRI) findings of HC invasion with clinical evidence of CN XII dysfunction. 2. Materials and methods This retrospective study was HIPAA compliant and approved by the institutional review board. Thirty-one patients with a diagnosis of GJ evaluated in the past 5 years were identified via a radiology information system keyword search. The neuroradiological studies (CT and MRI) and medical data including history, symptoms, and clinical features of all patients with GJs were analyzed. CT and MRI imaging modalities were reviewed by an attending neuroradiologist blinded to the clinical findings for characteristics of the GJ, looking specifically for HC invasion. The HC was said to be invaded when neoplastic tissue spread beyond a wall of the HC, directly invaded it (Fig. 1), or expanded (Fig. 2) or destroyed the canal walls. If a patient was studied with both MRI and CT, they were blindly reviewed at different times spaced out 3–4 weeks apart to assure no bias. The clinical notes (history and neurologic exam) of the patients in the database were reviewed by another author who did not evaluate the

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imaging studies and was blinded to the imaging findings to determine the presence of clinical evidence of CN XII dysfunction. The entire medical record was assessed for clinical findings of hypoglossal dysfunction over the extended preoperative period and postoperative period and this was not a single point in time evaluation. Atrophy and/or deviation of the tongue toward the side of the lesion on physical examination were considered positive clinical signs of CN XII dysfunction, which were taken as the gold standard for reference with the CT and MRI findings, in the absence of surgical pathology. The obtained data were then processed and analyzed to determine the rate of HC invasion by imaging findings and to assess the specificity (Sp), sensitivity (Sn), and accuracy (Acc) of CT and magnetic resonance (MR) in predicting a clinical manifestation of such invasion.

3. Results The study group consisted of 31 patients, 19 females (61.3%) and 12 males (38.7%) with an average age of 52.3 years (range: 26–85 years, standard deviation=15.3). There were 31 GJ tumors and one patient had multiple tumors, with CBT and GJ on contralateral sides. Imaging studies identified HC involvement that met the abovementioned criteria in 22/31 GJ tumors (71%). Thirteen of 31 patients (41.9%) had clinically evident CN XII dysfunction symptoms. All 13 patients showed HC invasion by imaging but there were an additional 9 GJ tumors, which demonstrated HC invasion by imaging without CN XII symptoms (i.e., imaging false positive). The false positives were defined as imaging positive, clinical negative. We aim to determine whether an imaging test predicts clinical symptoms, then this is a true false positive. The statistics were applied to HC invasion at imaging predicting clinical symptoms of hypoglossal nerve dysfunction. MRI was performed in 30 patients and gave positive results in 20 tumors of which 7 were false positive (i.e., patients had no symptoms). There were no false negatives. Therefore, the Sn was 100% (13/13), Sp was 58.8% (10/17), positive predictive value (PPV) was 65% (13/20), and negative predictive value (NPV) was 100% (10/10), with an overall Acc of 76.7% (23/30). CT was performed in 14 patients with 9 positive results of which 2 were false positive. There was one false negative. Sn was 87.5% (7/8), Sp was 66.7% (4/6), PPV was 81.8% (9/11), and NPV was 80% (4/5) with an overall Acc of 78.6% (11/14). In the tumors that were analyzed with both modalities, there was no disagreement on the findings between MR and CT.

4. Discussion PGs are generally benign slow-growing tumors and usually remain clinically silent over years. They can be found in many different locations. They arise in the head and neck as four primary entities: the CBT, the GJ, the GT, and the GV [2,9]. These tumors, depending on the location of origin, spread following the anatomical pathways of least resistance: they can invade the fat of the carotid space and grow along the parapharyngeal space, and they can erode the temporal bone and grow inside vascular structures such as internal jugular vein or invade the skull base passing through the HC. The assessment of the tumoral growth and of the degree of skull base involvement, including the invasion of the HC, may be conducted using both CT and MRI. On CECT, GJs are seen as an avidly, homogenously enhancing masses, while on MRI, they appear as enhancing soft tissue masses that may have “salt and pepper” appearance with characteristic internal flow voids if the lesion is large enough [10]. With both modalities, the HC is said to be invaded when neoplastic tissue spreads beyond the wall of the HC, directly invades it, or expands or destroys the canal walls. The hypoglossal nerve has a long course that begins into the brain stem and extends until the tongue. It can be divided in five segments: (1) medullary, (2) cisternal, (3) skull base, (4) nasopharyngeal/ oropharyngeal carotid space, and (5) sublingual [11]. It is important to know the anatomy of the hypoglossal nerve to make a reasonable differential diagnosis because different types of diseases affect particular segment of the hypoglossal nerve. However, many lesions can also be located in more than one segment. GJs can be located in the cisternal and skull base segments in addition to suprahyoid compartment. The majority of XII nerve palsies on presentation are caused by invasion of the tumor into the skull base in the region of the HC. PGs, and especially GJs, commonly affect lower CNs at the level of skull base when they invade the jugular foramen or the HC. GVs arise from tissue rests within the nodose (inferior) ganglion and CBTs are located in the carotid space. Since these tumors are not close to the skull base, they commonly do not involve the HC. However, large GVs that arise from the superior ganglion can extend intracranially to the HC [12]. Besides PGs, meningiomas, nerve sheath tumors, chordomas, metastases, and nasopharyngeal squamous cell carcinomas and lymphomas are the other neoplastic diseases that may involve the HC. Meningiomas that originate in the posterior fossa can extend to involve the internal auditory canal, HC, or middle ear [13]. Schwannomas, which occur in the HC, remodel and expand the canal rather than destroy it. Clivus chordomas can cause lower CN palsies when they involve the jugular

Fig. 1. (A–C) GJ in a 59-year-old male with nausea and deficits involving CNs IX–XII of the left side. Axial T2W MR image (A) shows mild hyperintensity of the left-sided mass. Axial T1W MR image (B) reveals soft tissue signal intensity involving HC with numerous flow voids indicating its hypervascular nature. White arrows indicate the border of HC on the normal side. Axial T1W postcontrast image (C) shows multilobulated intensely enhancing mass extending into left cerebellopontine angle, pons, left internal auditory canal, petrous bone, and middle ear cavity.

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Fig. 2. (A–C) GJ in a 51-year-old female with an asymptomatic right-sided suprahyoid neck mass. CNs are intact. On the axial CT image using bone review algorithm (A, left image), there is no definite evidence of HC bony erosion but the right HC is minimally wider than left (white arrow). Axial CT image using soft tissue algorithm (A, right image) shows enhancing soft tissue mass extending into the HC (doted arrow). Axial T1W postcontrast image (B) shows avidly enhancing right-sided soft tissue mass involving the HC. Mass also shows indentation on the right longus coli muscle (white arrow). Coronal T1W postcontrast image (C) again demonstrates the invasion of HC (white arrow).

foramen or HC. Metastatic disease can cause lower CN dysfunction by perineural spread or skull base involvement [14]. The hypoglossal nerve supplies motor innervations to all of the muscles to the tongue except the palatoglossus muscle that is innervated by the vagus nerve [15,16]. Twelfth-nerve palsies usually appear as signs rather than symptoms. Patients who have hypoglossal nerve paresis present with atrophy and deviation of tongue. Corticobulbar neurons are predominantly crossed. Therefore, if a lesion involves the cerebral cortex, its impact will be on the contralateral side of the tongue. Thus, one can say that when a lesion affects the upper motor neurons of the motor cortex, deviation of the tongue is toward the side opposite the lesion. Conversely when the lesion invades the lower motor neurons, i.e., the HC or nerve, deviation of tongue is toward the side of the lesion. The pattern of the atrophy varies according to the severity and duration of denervation. Muscles of tongue become atrophic in 4–6 weeks after injury [16]. Lesions of the HC can be safely and effectively resected using one of several skull base strategies. The surgical approach is decided based on multiple factors such as tumor type, size, patient age, symptoms, and comorbid conditions. The surgical options include the infratemporal fossa approach, the far lateral transcondylar approach, or the transjugular craniotomy for tumor resection [17]. Thus, if the surgeon treating a PG is apprised by the neuroradiologist that the HC is involved, the surgeon may alter the approach to accommodate this dissection (most commonly transjugular). In all types of approaches, preservation of the nerve and its function is difficult if the CNs are adherent to the tumor capsule or encased in tumor. Mechanical damage during surgery also can result in cranial neuropathy when the tumor capsule is retracted or compressed or violated [18]. The aim of this study was to assess the rate of HC invasion for GJ tumors and to correlate CT and MRI findings of HC invasion with clinical evidence of CN XII dysfunction. Thirteen of 31 patients (41.9%) had clinically evident CN XII dysfunction symptoms and all 13 showed imaging evidence of HC invasion on MR. CT showed 87.5% Sn with 1 false negative and MRI 100% Sn with no false-negative detection of HC invasion. There were 7 false-positive cases with an Sp of 59% for MRI and 1 false-positive case with an Sp of 66.6% for CT. Acc rates for MRI 76.7% (23/30) and CT 78.6% (11/14) in predicting such dysfunction were comparable. What can one say about the cases where the HC appeared invaded but the patient was devoid of symptoms? Is that early disease before XII nerve dysfunction? Is it disease that is not truly invading the canal, a radiologist’s overcall? Is it slowly growing disease that will displace rather than infiltrate the nerve, hence the patient is asymptomatic? This study cannot explain all the causes of the false-positive cases because they are likely multifactorial.

The study has some other limitations. CT and MRI findings of HC invasion were correlated with clinical evidence of CN XII dysfunction. Because of the retrospective nature of the study and the failure of surgeons to specifically talk about the HC in the operative report, the imaging findings could not be correlated with surgical findings. A prospective study would yield more accurate study. Most imaging studies did not include the tongue to assess for ipsilateral tongue atrophy or other findings of denervation that might suggest dysfunction even without clinical findings. Finally, the study numbers were not large, but, as a series, this ranks as the largest group of GJs to be evaluated for HC invasion. HC invasion occurs in the majority (71.0%) of cases of GJ tumors. Imaging findings of invasion on MRI and CT correlate well (76.7–78.5%) with clinical findings of hypoglossal nerve dysfunction. In identifying HC tumor proximity, a more directed neurologic examination of tongue dysfunction may elucidate subtle findings that may otherwise be overlooked. This pathway of spread must be carefully addressed at the time of surgery for eradication of the tumor as well as to ensure that inadvertent intraoperative damage to the hypoglossal nerve does not occur. This may also be a site where residual tumor may reside if not addressed appropriately on initial treatment. Many people would not associate a glomus tumor with HC invasion. However, it happens at a high rate. At surgery, involvement of the HC will mean a different approach than disease that does not encroach on this area. Furthermore, relying just on clinical symptoms to suggest whether or not the HC is invaded at imaging may not be reliable.

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Hypoglossal canal invasion by glomus jugulare tumors: clinico-radiological correlation.

The aim of this retrospective study is to assess the rate at which glomus jugulare tumors invade the hypoglossal canal (HC) and to correlate computed ...
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