Sonography of the Cervical Vagus Nerve: Normal Appearance and Abnormal Findings

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1 Downloaded from by on 01/20/18 from IP address opyright RRS. For personal use only; all rights reserved Francesco Giovagnorio 1 arlo Martinoli 2 Received ugust 7, 2000; accepted after revision September 15, I attedra di Radiologia, Università La Sapienza, Viale Regina Elena 324, Rome, Italy. ddress correspondence to F. Giovagnorio. 2 attedra di Radiologia R, DIMI, Università di Genova, Largo Rosanna enzi 8, Genova, Italy. JR 2001;176: X/01/ merican Roentgen Ray Society Sonography of the ervical Vagus Nerve: Normal ppearance and bnormal Findings OJETIVE. The purpose of this study was to assess the appearance of the cervical vagus nerve in healthy individuals and to investigate the potential role of sonography in revealing neck masses that cause vagal dysfunction. SUJETS ND METHODS. We examined 150 consecutive patients. In 144 patients the presence of thyroid, salivary gland, or lymph node disease was suspected. In three patients a cervical mass was palpable, and three patients had symptoms of dysfunction of the inferior laryngeal or vagal nerves. The pathologic diagnoses of the masses were obtained at biopsy. RESULTS. In 144 individuals the normal vagus nerve was recognized on each side of the neck as a thin band that occupied the posterior angle formed by the common carotid artery and the internal jugular vein. Three patients had tumors arising from the vagus nerve: one neurofibroma, one neurinoma, and one chemodectoma. These tumors were located in the neurovascular bundle and posterior to the vessels; their origin from the vagus nerve was clearly visible in all patients because of the contiguity of the mass with the nerve bundle. In the other three patients, sonography revealed an extrinsic mass that compressed and displaced the vagus nerve out of its longitudinal axis; two cases were hyperplastic nodules of the thyroid, and in one case the nodule was a branchial cyst. ONLUSION. Sonography can reveal the vagus nerve in healthy conditions and correctly reveal the vagal origin of some tumors in the parapharyngeal spaces. H igh-resolution small-parts transducers with frequencies higher than 10 MHz and sophisticated focusing in the near field have improved the diagnostic outcome of most sonographic examinations of superficial organs and structures. In the neck, for example, high spatial resolution is required to differentiate among many small anatomic structures in close contact with each other. The visibility of subtle anatomic details has been reported in many studies, some of which investigated the sonographic appearance of peripheral nerves such as the recurrent laryngeal nerve [1]. The possibility of revealing the vagus nerve as an anatomic landmark in the neck was proposed in a recent article [2]. The purpose of this study was to assess the appearance of the vagus nerve in healthy individuals and to investigate the potential value of sonography in revealing the causes of vagal dysfunction in masses arising in the neck. The cervical course of the vagus nerve starts from the foramen jugulare behind the glossopharyngeal nerve and the sinus petrosus inferior. From behind the stylohyoid ligament to the thoracic inlet, the nerve descends along the angle formed posteriorly by the internal and common carotid arteries, which are located anteromedially, and the internal jugular vein, which is located anterolaterally. The nerve, artery, and vein form the major neurovascular bundle of the neck, anatomically delimited by a common connective sheath (Fig. 1). t the lower neck, the neurovascular bundle is partially covered anteriorly by the lateral lobes of the thyroid. t the thoracic inlet, the right vagus nerve is located behind the confluence of the internal jugular vein with the subclavian vein, whereas the left vagus nerve lies posterior to the venous brachiocephalic trunk. The recurrent laryngeal nerves originate at this level and ascend into the neck in the tracheoesophageal groove, passing posteromedially to the lateral lobes of the thyroid to penetrate the larynx. Variations of the cervical course of the vagus nerve are possible but rare. The anterior location of the nerve, which passes in front of the common carotid artery, has been described [3]. JR:176, March

2 Giovagnorio and Martinoli Downloaded from by on 01/20/18 from IP address opyright RRS. For personal use only; all rights reserved Subjects and Methods We examined 150 consecutive patients (87 females, 63 males; age range, years) undergoing sonographic examination of the neck for a variety of reasons. In 144 patients the presence of thyroid, salivary gland, or lymph node disease was suspected; in three patients a cervical mass was palpable; and three patients had symptoms of dysfunction of the inferior laryngeal or vagal nerves, including dysphonia and dysphagia. Sonographic studies were performed on two scanners (HDI-3000, dvanced Technology Laboratories, othell, W; u5-idea, EsaOte Fig. 1. Drawing shows vagus nerve (arrows) inside major neurovascular bundle, and behind common carotid artery (anteromedially) and internal jugular vein (anterolaterally). D iomedica, Genoa, Italy) equipped with broadband (12 15, , MHz) linear array transducers. Examinations were performed with the patients supine and the neck hyperextended. The region of interest (lateral margins of the anterior cervical region beneath the sternocleidomastoidei muscles) was scanned in the transverse plane. thin (<2 mm in cross-sectional diameter) cordlike structure, centrally hypoechoic, which occupied the angle formed posteriorly by the common carotid artery and the internal jugular vein, inside the major neurovascular bundle, was visualized and, according to a previously published experience [2], identified as the vagus nerve. The scanning plane was then oriented longitudinally to elongate and optimally display the nerve. Nerves were imaged along their transverse and longitudinal axes. Images were obtained by one of the authors and were later examined by the other. oth authors agreed on all the interpretations proposed. In one patient with chemodectoma, T was performed to better evaluate the anatomic relationship of the mass to the surrounding organs and the presence of calcifications. The pathologic diagnosis of the masses was made at biopsy performed with fine-needle aspiration under sonographic guidance. Results Normal Findings In the 144 patients who underwent sonography, the vagus nerve was visible bilaterally and was clearly recognizable throughout its cervical course (approximately cm in craniocaudal direction) (Fig. 2). The sonographic appearance of the vagus nerve varied depending on the equipment used. With MHz frequency probes, the nerve exhibited a striated arrangement of its internal structure, which was made of hypoechoic Fig year-old man with no signs of vagal disease., xial sonogram (10 MHz) of left neurovascular bundle shows internal jugular vein (IJV), common carotid artery (), and vagus nerve (arrow). TR = trachea., Sagittal sonogram (10 MHz) shows vagus nerve (arrowheads) and internal jugular vein (IJV)., xial sonogram (15 MHz) of right neurovascular bundle shows vagus nerve (arrow) with honeycomb appearance and two to four hypoechoic rounded fascicles surrounded by hyperechoic epineurium. D, Sagittal sonogram (15 MHz) clearly shows internal structure made of some hypoechoic parallel fascicles separated by hyperechoic envelope (arrowheads). 746 JR:176, March 2001

3 Sonography of the ervical Vagus Nerve Downloaded from by on 01/20/18 from IP address opyright RRS. For personal use only; all rights reserved parallel fascicles separated by a hyperechoic envelope. On transverse scans, the nerve assumed a honeycomb appearance with two to four hypoechoic rounded fascicles surrounded by hyperechoic epineurium. On lower sonographic frequencies, the image of the fascicles was poorly defined as a result of decrease in image resolution. However, recognition of the vagus nerve was still possible at frequencies as low as 7.5 MHz. In addition, difficulty recognizing the nerve structure was encountered in patients with large, short necks or with coincident postsurgical scarring in the cervical area. Whatever the frequency used, the outer boundaries of the nerve appeared undefined because a similar hyperechoic appearance of the superficial epineurium and the surrounding connective tissue of cervical spaces. n abnormal course was observed in two (0.7%) of 288 nerves examined: the nerve was in the normal position in the cranial half of its cervical course, then the nerve crossed the space between the vessels at the level of the thyroid to run in the anterior angle formed by the common carotid artery and the Fig year-old woman with no signs of vagal disease., xial sonogram (7.5 MHz) of left neurovascular bundle at level of superior third of thyroid shows vagus nerve in its normal position (arrow)., xial sonogram (7.5 MHz) at level of middle third of thyroid shows vagus nerve crossing space between internal jugular vein and common carotid artery (arrow)., xial sonogram (7.5 MHz) at level of inferior third of the thyroid shows vagus nerve in abnormal anterior position (arrow). Fig year-old boy with type I neurofibromatosis and no signs of vagal disease., xial sonogram (10 MHz) of right neurovascular bundle at level of superior third of thyroid shows multiple hypoechoic nodules (asterisks and arrows) in neurovascular bundle displacing internal jugular vein (IJV) externally and common carotid artery () medially., Longitudinal sonogram (10 MHz) clearly shows vagal origin of two nodules (asterisks). Normal vagus nerve cranial to tumors is indicated by arrowheads. internal jugular vein before entering the thoracic inlet (Fig. 3). This alteration was not associated with any significant disease. bnormal onditions Three patients with occasional symptoms of laryngeal dysfunction (cough, dysphonia) had tumors arising from the left (two patients) and right (one patient) vagus nerves: one plexiform neurofibroma (multiple nodules 1 2 cm in diameter) in a 15-year-old boy with a type I neurofibromatosis (Fig. 4), one neurinoma (1.5 cm in diameter) in a 45-yearold man (Fig. 5), and one chemodectoma (1.2 cm in diameter) in a 43-year-old man (Fig. 6). Two masses (neurinoma and neurofibroma) were hypoechoic and oval, with regular and well-defined margins; one mass (chemodectoma) was poorly defined on sonography because of the presence of coarse calcifications that was confirmed on T. In these three patients, the tumors were located inside the neurovascular bundle, posterior to the vessels, which were stretched apart by the masses (the common carotid artery was displaced anteromedially and the internal jugular vein anterolaterally). The origin from the vagus nerve was clearly shown in all patients. presumptive diagnosis of the intrinsic neurogenic nature of the tumor was made on sonography by showing the direct connection of the mass with the nerve bundle at its proximal and distal poles, which required careful scanning. Outside the tumor, the entering and exiting nerve may be thickened and have loss of fascicular structure, thus producing a tapering appearance of the oval mass. In three patients, sonography showed a prominent extrinsic mass that invaded the anatomic location of the vagus nerve, which was compressed and displaced externally. In two patients (two women, who were 56 and 65 years old, with persistent coughs), the masses originated from the posterolateral aspect of the left lobe of the thyroid, had diameters of 2.5 and 3.5 cm, and were diagnosed at biopsy as hyperplastic nodules. In a 25- year-old woman with mild dysphagia, an oval 1.5-cm hypoechoic nodule in the right parapharyngeal space was diagnosed as a branchial cyst at biopsy (Fig. 7). JR:176, March

4 Giovagnorio and Martinoli Fig year-old man with cough and dysphonia. Longitudinal sonogram (7.5 MHz) of left vagus nerve shows hypoechoic nodule (T) arising from nerve (arrowheads). iopsy revealed neurinoma. Downloaded from by on 01/20/18 from IP address opyright RRS. For personal use only; all rights reserved Fig year-old man with cough, dysphonia, and biopsy-proven chemodectoma., xial sonogram (10 MHz) of right neurovascular bundle at level of superior third of thyroid shows poorly defined tumor (T) (arrows) inside neurovascular bundle that is displacing internal jugular vein (IJV) and common carotid artery () anteriorly., Longitudinal sonogram (10 MHz) clearly shows vagal origin of tumor (T) (arrows). Normal vagus nerve cranial to tumor is indicated by arrowheads. IJV = internal jugular vein., T scan at lower anatomic plane than and shows calcified tumor (arrow) in anatomic location of vagus nerve, with evident separation of common carotid artery from internal jugular vein. Discussion The cervical portion of the vagus nerve is cranial to the origin of the recurrent laryngeal nerve, hence tumors arising from the vagus nerve or cervical masses that compress or infiltrate the nerve may cause symptoms as a result of dysfunction of the inferior recurrent laryngeal nerve (cough, dysphonia) or dysfunction of the vagus nerve itself (arrhythmia, dysphagia, dyspnea, nausea, hiccups). These symptoms are not specific and are not commonly attributed to a malfunctioning vagus nerve; therefore, significant diagnostic delays may occur and patients may undergo unnecessary examinations. Visibility of the cervical vagus nerve on sonography has been reported by Knappertz et al. [2], who describe a centrally hypoechoic and peripherally hyperechoic structure between the common carotid artery and the jugular vein and inside the carotid sheath on transverse -mode images of the neck. This structure was also identified in a nonpreserved cadaver and was marked with a hypodermic needle by means of a transdermal approach. Neck dissection was performed, which showed the vagus nerve as the target of the needle. In our experience, the sonographic appearance of the vagus nerve varies depending on the equipment used: with lower frequencies ( MHz) the nerve is visible as a cordlike structure, centrally hypoechoic, whereas higher frequencies (13 15 MHz) show an internal structure composed of hypoechoic parallel fascicles separated by a hyperechoic envelope. Tumors arising from the vagus nerve are rare and generally benign. Schwannoma, neu- 748 JR:176, March 2001

5 Sonography of the ervical Vagus Nerve Downloaded from by on 01/20/18 from IP address opyright RRS. For personal use only; all rights reserved Fig year-old woman with mild dysphagia. Longitudinal sonogram (7.5 MHz) of right vagus nerve shows hypoechoic nodule () compressing vagus nerve (arrowheads). Surgical excision revealed branchial cyst. rinoma, and neurofibroma are histologically similar and may arise from the vagus nerve or other peripheral nerves (neurofibromas are generally found in patients affected by von Recklinghausen s disease). Paraganglioma, also referred to as chemodectoma, is less common, arises from either the vagus nerve or the carotid body, and is rarely malignant [4 8]. Paragangliomas derive from stem cells of the neural crest and can be found in any part of the body in which there are sympathetic ganglia, including chemoreceptors, adrenal medulla, retroperitoneal ganglia, and the vagus nerve. familial tendency has been reported, and in these patients bilateral tumors are often present [7]. Multiple tumors arising from different sites are common. When the tumor arises from the vagus nerve, it presents as a painless neck mass behind the carotid artery that compresses the internal jugular vein with normal cranial nerve function [7]. Vocal cord paralysis has been described as an associated finding in 47% of cases. The literature contains few reports of imaging of paragangliomas of the vagus nerve [9, 10]. Sonographically, this tumor has been described as a solid hypoechoic and heterogeneous lesion containing small vascular structures. In our patient, the mass presented with a medium-level echogenicity similar to that of the thyroid, a hypervascular pattern with low-velocity arterial flows on color Doppler sonography, and coarse calcifications. Further experience is needed to establish whether this tumor has differential features on sonography compared with those of other neurogenic tumors arising from a nerve, such as schwannomas and neurofibromas. Intrinsic tumors of the vagus nerve do not have a specific appearance on sonography because they present as fusiform hypoechoic masses with well-defined margins; therefore, it is impossible to differentiate masses arising from the vagus nerve from other common neck masses such as lymph node enlargements on the basis of sonographic appearance alone. bsence of an echogenic hilum has been proposed as a criterion to differentiate a lymph node from a peripheral nerve tumor [11], but this sign can generally be found with most other malignant nodes [12]. The direct visualization of a contiguity between the nerve and the tumor on longitudinal scan, is therefore the only pathognomonic sign of the vagal nerve origin of the mass. When an abnormally large mass displaces the nerve so that the proximal and distal poles are not clearly visible, sonography can provide important indirect clues previously seen only on T [13, 14], such as increased distance between the internal jugular vein (displaced anterolaterally) and the carotid artery (displaced anteromedially) when the tumor arises from the vagus nerve, as opposed to lateral or medial displacement of the entire neurovascular bundle when the tumor arises from the thyroid, the carotid body, the cervical sympathetic chain, or other organs located in the parapharyngeal space. The sonographic visualization of the normal and abnormal vagus nerve may be compromised by increased thickness of the local subcutaneous fat in patients with thick, short necks and by the presence of scars in patients having undergone neck surgery. These conditions do not compromise the direct visualization of the nerve but may increase the difficulty of differentiating the displacement of the nerve by an extrinsic mass from its encasement by a mass originating from the nerve. Possible misdiagnosis can be avoided by recognizing that only tumors arising from the nerve can increase the distance between the carotid artery and the internal jugular vein, with the possible exception of masses arising from other anatomic elements in the neurovascular bundle (fat tissue, connective tissue of the external sheath, muscular or connective layers of the vessels). In this case, sonographic differentiation of tumors arising from the vagus nerve from other tumors originating in the neurovascular bundle may be impossible. In conclusion, the presented data suggest that sonography can noninvasively reveal the cervical portion of the vagus nerve and answer most of the diagnostic questions related to the nerve when a nodule of uncertain origin is encountered near the neurovascular bundle of the neck. Sonographic findings can show the origin of the nodule from the vagus nerve. Future applications of the method could also include sonographic localization of the nerve to improve the outcome of stimulation that has been proposed for seizure therapy [15]. References 1. Solbiati L, De Pra L, Ierace T, ellotti E, Derchi LE. High-resolution sonography of the recurrent laryngeal nerve: anatomic and pathologic considerations. JR 1985;145: Knappertz V, Tegeler H, Hardin SJ, McKinney WM. Vagus nerve imaging with ultrasound: anatomic and in vivo validation. Otolaryngol Head Neck Surg 1998;118: Veleanu, Dinulescu T, Zolog I. Vagus nerve passing in front of the left lobe of the thyroid gland. nat nz 1977;141: Pesavento G, Ferlito, Recher G. enign solitary schwannoma of the cervical vagus nerve: a case report with a review of the literature. J Laryngol Otol 1979;93: Wiel Marin, Zucchetti F, utti, et al. Neurinoma of the vagus nerve: description of 2 cases and review of the literature [in Italian]. G hir 1998;19: Galli J, lmadori G, Paludetti G, Rosignoli M, orina L, Ieraci. Plexiform neurofibroma of the cervical portion of the vagus nerve. J Laryngol Otol 1992;106: Netterville JL, Jackson G, Miller FR, Wanamaker JR, Glasscock ME. Vagal paraganglioma: a review of 46 patients treated during a 20-year period. rch Otolaryngol Head Neck Surg 1998; 124: Urquart, Johnson JT, Myers EN, Schechter GL. Glomus vagale: paraganglioma of the vagus nerve. Laryngoscope 1994;104: Raby N. Ultrasonographic appearances of glomus vagale tumour. r J Radiol 1988;61: Derchi LE, Serafini G, Rabbia, et al. arotid body tumors: US evaluation. Radiology 1992;182: King D, huja T, King W, et al. Sonography of peripheral nerve tumors of the neck. JR 1997;169: Rubaltelli L, Proto E, Salmaso R, ortoletto P, andiani F, agol P. Sonography of abnormal lymph nodes in vitro: correlation of sonographic and histologic findings. JR 1990;155: Furukawa M, Furukawa MK, Katoh K, Tsukuda M. Differentiation between schwannoma of the vagus nerve and schwannoma of the cervical sympathetic chain by imaging diagnosis. Laryngoscope 1996;106: Silver J, Mawad ME, Hilal SK, scherl GF Jr, hynn KY, aredes S. omputed tomography of the carotid space and related cervical spaces. II. Neurogenic tumors. Radiology 1984;150: innie D. Vagus nerve stimulation for epilepsy: a review. Seizure 2000;9: JR:176, March