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Imaging of muscular denervation secondary to motor cranial nerve dysfunction
Clinical Radiology (2006) 61, 659e669
PICTORIAL REVIEW
Imaging of muscular denervation secondary to motor cranial nerve dysfunction S.E.J. Connor*, N. Chaudhary, S. Fareedi, E.K. Woo Neuroradiology Department, Kings College Hospital, Denmark Hill, London SE5 9RS, UK Received 11 February 2006; received in revised form 30 March 2006; accepted 4 April 2006
The effects of motor cranial nerve dysfunction on the computed tomography (CT) and magnetic resonance imaging (MRI) appearances of head and neck muscles are reviewed. Patterns of denervation changes are described and illustrated for V, VII, X, XI and XII cranial nerves. Recognition of the range of imaging manifestations, including the temporal changes in muscular appearances and associated muscular grafting or compensatory hypertrophy, will avoid misinterpretation as local disease. It will also prompt the radiologist to search for underlying cranial nerve pathology, which may be clinically occult. The relevant cranial nerve motor division anatomy will be described to enable a focussed search for such a structural abnormality. ª 2006 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction Lower motor cranial nerve dysfunction has a profound effect on the muscles that it innervates. It results in an alteration of morphology, either due to reduced bulk of muscle or due to the loss of tone and position. The magnetic resonance imaging (MRI) signal, computed tomography (CT) attenuation and contrast medium enhancement are also affected. Moreover, compensatory hypertrophy of associated muscles, distortion of adjacent normal structures and therapeutic insertion of muscle grafts may all be misinterpreted as local pathology. Although cranial nerve dysfunction often leads to clinical manifestations, these may be non-specific and the identification of muscular denervation changes on imaging studies provides objective evidence of a lesion. Occasionally, the radiological changes in deep inaccessible muscle groups are clinically occult. By recognizing the patterns of muscular involvement, and understanding the relevant motor cranial nerve anatomy, the * Guarantor and correspondent: S.E.J. Connor, Neuroradiology Department, Kings College Hospital, Denmark Hill, London SE5 9RS, UK. Tel.: þ44 208 761 8344; fax: þ44 207 346 3120. E-mail address: [email protected] (S.E.J. Connor).
radiological search and scan volume may be focused appropriately. The imaging appearances of muscular denervation secondary to V, VII, X, XI and XII motor cranial nerve dysfunction have been studied1e17 and will form the basis of this review. As there are only isolated imaging reports of denervation in the extraocular muscles (cranial nerves III, IV, VI)18,19 and no reports of the stylopharyngeus muscle (cranial nerve IX), these will not be discussed. Appearances that may be misconstrued as local pathology will be emphasized.
Muscular denervation in the head and neck: general concepts and temporal changes Denervation of skeletal muscle leads to alterations in histology, biochemistry, enzymes and structure.20e25 The MRI appearances of denervated peripheral skeletal muscle have been described.25e27 They have been divided into the acute phase (<1 month), subacute phase (1 month to 1 year) and the chronic phase (>1 year). Appearances are frequently normal in the acute phase. The subacute phase is manifest by
0009-9260/$ - see front matter ª 2006 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.crad.2006.04.003
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a prolonged T1 and T2 relaxation time. These imaging findings are attributed to relatively increased tissue water within the enlarged interstitial space of the affected muscle, which is created by decreased muscle fibril size.25e27 Increased contrast medium enhancement is also described in the subacute phase. This has been explained by an increased blood flow to the denervated muscle and increased accumulation in the enlarged extracellular space. Subacute denervation changes occasionally return to normal but usually progress to a chronic phase of fatty replacement with atrophy.6 This stage is easily recognized using CT (fat attenuation) or MRI (increased T1-weighted signal) in the larger muscle groups, although changes in smaller muscles may only be detected using MRI.10e11 The progression of denervation imaging changes secondary to trigeminal (V) nerve and hypoglossal (XII) nerve dysfunction have received most attention in the head and neck, as the corresponding masticator and tongue muscles are easily recognized on imaging studies.1,2,6,7,12e14,16,17 It does appear that different muscles develop the changes evident using MRI at different rates, and it is postulated that there are earlier and more conspicuous changes with muscles supplied by a single nerve.5 In view of the variable degree of neural damage and difficulties in defining the exact onset of dysfunction, it is unsurprising that there is marked variation in the reported timing and appearance of the MRI changes of muscular denervation. In general terms, the muscles of the head and neck also conform to patterns of early enhancing ‘‘oedema-like’’ change and later ‘‘fatty atrophic’’ change. Detailed descriptions of the temporal course in trigeminal and hypoglossal nerve related motor denervation are found in the appropriate sections.
Imaging changes due to trigeminal (V) nerve dysfunction The mandibular division of the trigeminal nerve provides motor supply to the masticator muscles (medial and lateral pterygoid, masseter and temporalis muscles), anterior belly of digastric, mylohyoid, tensor tympani and tensor veli palatini muscles28e30 (Fig. 1). Denervation changes in the muscles supplied by the trigeminal nerve may be secondary to a lesion along the course of motor fibres from brainstem to muscle. A review of the anatomy (Fig. 1) helps separate two distinct patterns, which may help localize a lesion. A proximal pattern of changes in all the muscles supplied by the trigeminal nerve indicates
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an injury to the nerve between the brainstem and the bifurcation into anterior and posterior trunks. A distal pattern, that affects only the mylohyoid and anterior belly of digastric muscles, indicates a lesion distal to the bifurcation (involving the posterior trunk, inferior alveolar or mylohyoid nerves). The MRI appearance of masticator muscle denervation6,7,9,16,17,31 has been divided into four categories16 (Table 1). Early (acute and subacute) phases are manifest by increased T2-weighted, short tau inversion recovery (STIR) signal and enhancement (Fig. 2) with an ‘‘oedema-like’’ appearance, whereas the chronic phase shows T1 hyperintense fatty infiltration and later atrophy (Fig. 3). There is considerable overlap in the timing and progression of the MRI appearances.6,7,9,16,17 A useful clue to the presence of a proximal pattern of trigeminal nerve damage, is the presence of serous otitis media (Fig. 3) secondary to tensor veli palatini and medial pterygoid dysfunction.7,32 Tensor veli palatini loss of tone may also be recognized as asymmetry of the torus tubarius. The distal pattern of isolated mylohyoid and anterior belly of digastric muscle involvement has only been described in the chronic atrophic phase6 (Fig. 4). Changes of masticator muscle denervation should not be confused with local pathology. The subacute ‘‘oedema-like’’ phase may mimic an inflammatory, neoplastic or traumatic aetiology, particularly if there is swelling. Such a process is less likely to involve all the relevant muscles diffusely. The differential diagnosis of atrophy and fatty infiltration of the muscles of mastication includes disuse, post-traumatic reflex sympathetic dystrophy, and congenital facial asymmetry and connective tissue disorders.17 It should be ensured that the contralateral normal muscle is not diagnosed as a mass. There are a myriad of lesions that may result in trigeminal nerve dysfunction and a full discussion is beyond the scope of this review.28e30,33 Typical imaging findings of muscular denervation changes have been described in the setting of brain stem lesions (bulbar poliomyelitis, cavernoma, haemorrhage, glioma), cavernous sinus lesions (neurogenic tumours, lymphoma, meningioma, metastasis, perineural tumour spread), skull-base lesions (chordoma, carcinoma, rhabdomyosarcoma) or secondary to rhizotomy and trauma.6,7,9,16,17,31
Imaging changes due to facial (VII) nerve dysfunction The facial somatic motor root innervates the muscles of facial expression, occipitalis, buccinator, platysma, stylohyoid and stapedius muscles.
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Figure 1 The course of the motor supply of the trigeminal nerve. The motor root emerges from the ventral pons and bypasses the gasserian ganglion, joining the mandibular division (V3) as it exits the skull base through the foramen ovale. All the motor fibres are distributed along this division. Immediately after supplying a small nerve to the medial pterygoid muscle (with fibres subsequently extending to tensor veli palatini and tensor tympani muscles via the otic ganglion) the mandibular nerve divides into a predominantly motor anterior trunk and a predominantly sensory posterior trunk. The former supplies temporalis, masseter and lateral pterygoid muscles, whilst the latter supplies the anterior belly of digastric and mylohyoid muscles via the inferior alveolar/mylohyoid nerves.
The muscles of facial expression are diminutive muscles. The course of the facial nerve may be divided into its pontine segment; the cisternal segment, which traverses the cerebellopontine angle cistern and internal auditory meatus; the intratemporal segment; and the extracranial segment, which enters the parotid gland.34,35 Table 1
Changes of denervation atrophy secondary to facial nerve dysfunction have been described using both CT and MRI.4,6,10,11 Lower motor neuron facial nerve dysfunction is usually clinically obvious, however, some patients with muscle atrophy revealed by MRI have had normal facial function.10,11 Changes in the orbicularis oculi,
Temporal sequence of denervation changes in masticator muscles described by Russo et al16
Acute Subacute Early chronic Late chronic
T1
T2
Size
Enhancement
Timing
Intermediate Increased Increased Markedly increased
Increased Increased Intermediate or increased Intermediate or increased
Increased Unchanged Unchanged Decreased
Yes Yes No No
Days to weeks 6e20 months* Not well defined >2 years**
Other authors describe a similar progression of MRI findings with the exception of: * Subacute denervations has been demonstrated within one month of symptom onset7 ** Muscle atrophy has been described at three months.7,9
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Figure 2 Gadolinium-enhanced fat-saturated T1weighted axial MRI. Imaging changes due to subacute trigeminal nerve dysfunction. Increased bulk and gadolinium enhancement is seen within the left lateral pterygoid muscle (arrowhead), masseter and temporalis muscles secondary to subacute denervation. A lesion within the cavernous sinus was detected more superiorly and perineural spread of adenoid cystic carcinoma along the trigeminal nerve was diagnosed. Symptoms had been present for 2 months at the time of the MRI and the muscles of mastication atrophied on imaging follow-up.
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Figure 4 T1-weighted axial MRI. Imaging changes due to chronic distal (inferior alveolar nerve) trigeminal nerve dysfunction. There is atrophy of the left anterior belly of digastric muscle (arrowhead indicates normal right side) due to sacrifice of the left inferior alveolar nerve at the time of resection and grafting for a left oropharyngeal salivary gland malignancy.
Figure 3 (a) T1-weighted gadolinium-enhanced MRI and (b) T2-weighted axial MRI. Imaging changes due to chronic trigeminal nerve dysfunction. A right parasellar trigeminal nerve Schwannoma with longstanding symptoms of trigeminal nerve dysfunction. Atrophy and T2-weighted hyperintensity (there was also T1-weighted hyperintensity) is demonstrated within the right medial and lateral pterygoid muscles (black arrowhead). Note the right middle ear effusion (white arrowhead) due to tensor veli palatini and medial pterygoid (eustachian tube) dysfunction.
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quadratus labii, platysma and buccinator muscles have all been illustrated (Fig. 5). In addition, one report has demonstrated T2 prolongation and contrast medium enhancement suggestive of subacute denervation changes. Due to the multiple connections between branches of the facial nerve, it is not expected that selective muscle denervation will be appreciated unless nerve damage is very peripheral. It is unlikely that imaging changes in these small muscles will mimic pathology, however, regional and free muscle flap transfers used for the treatment of chronic facial nerve paralysis may simulate a mass lesion within the facial soft tissues (Fig. 6). Although viral infection and trauma (typically related to temporal bone or parotid surgery) are the most common pathologies to affect the facial nerve,10,11,34,35 the effects are usually transient. Denervation changes in the facial muscles have only been described in the context of facial nerve dysfunction due to malignant infiltration of the parotid and after skull-base surgery.4,6,10,11 However, imaging is usually directed to establishing the aetiology of facial nerve palsy within the posterior fossa, petrous bone and parotid gland rather than the end organ effects.
Imaging changes due to vagal (X) nerve dysfunction The motor fibres of the vagus supply the soft palate, constrictor muscles, as well as the intrinsic and extrinsic laryngeal muscles (Fig. 7). The
Figure 5 T2-weighted axial MRI. Imaging changes due to longstanding left facial nerve dysfunction. There is atrophy of the left quadratus labii superioris (arrowhead indicated normal bulk on contralateral side).
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Figure 6 STIR coronal MRI. Imaging changes due to muscular grafting for chronic facial nerve dysfunction. There had been extensive infiltration of the nerve without primary grafting at the time of resection of a left malignant parotid tumour. Buccinator muscle atrophy is seen (arrow). Paradoxical volume loss within the left anterior belly of digastric is likely due to dysfunction of the posterior belly, which is supplied by the facial nerve. There is soft tissue seen in the left buccal region (arrowhead) due to a pectoralis minor free flap. If the facial nerve is not repaired or grafted at the time of surgery, the native denervated muscles undergo atrophy and scarring. Free muscle transfer may be necessary if regional muscle (temporalis muscle) has failed or does not provide adequate bulk. Other muscles have been utilized for free tissue transfer (gracilis, latissimus dorsi, the serratus anterior and the rectus abdominis muscles).
peripheral motor divisions of the vagus may be considered as proximal and distal branches.8,34,36 Dysfunction of the vagus nerve paralyses the larynx and is manifested by a hoarse voice. It has been suggested that the presence of additional oropharyngeal symptoms is useful in identifying a proximal vagal lesion.8 A proximal vagal lesion should be investigated using MRI of the skull base, and a distal vagal (or recurrent laryngeal nerve) lesion should be investigated using CT of the skull base through to the upper mediastinum.8,37 Imaging patterns of muscular denervation changes may also contribute to the differentiation of a proximal from distal (or recurrent laryngeal nerve) lesion and so focus the imager and imaging appropriately. As the patient’s voice may occasionally be unaffected, the imaging findings of denervation changes may be the first indication to the presence of vagal nerve palsy. Distal vagal neuropathy is most common, accounting for 90% of cases.3 Cross-sectional imaging has found thickening and medial positioning of the
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Figure 7 The course of the motor supply of the vagus nerve. The motor fibres of the vagus originate in the nucleus ambiguous of the medulla. The roots exit the posterolateral sulcus of the medulla and traverse the basilar cistern to the pars vascularis of the jugular foramen. The proximal extracranial vagus nerve descends in the nasopharyngeal carotid space with the IX, XI and XII cranial nerves. The vagus then continues inferiorly along the posterolateral aspect of the carotid artery to the aortic arch. The proximal motor branches arise from the nodose ganglion and supply the pharyngeal plexus (motor function to the superior and middle constrictor muscles and soft palate apart from the tensor veli palatini muscle) and the superior/external laryngeal nerve (motor function to the inferior constrictor and cricothyroid muscle). The distal branches relevant to the head and neck structures are the recurrent laryngeal nerves. The right recurrent laryngeal nerve leaves the vagus at the level of the right subclavian artery, whilst that on the left loops through the aortopulmonary window. Both nerves ascend within the tracheooesophageal groove and pass posterior to the thyroid gland before terminating in the larynx (motor function to the intrinsic muscles of the larynx).
ipsilateral aryepiglottic fold, dilatation of the ipsilateral pyriform sinus and ventricle, anteromedial positioning of the ipsilateral arytenoid cartilage, atrophy of the ipsilateral posterior cricoarytenoid muscle or thyroarytenoid muscle and fullness of the ipsilateral vocal cord to be the most consistently demonstrated features3,15 (Fig. 8). In addition to the laryngeal changes, a proximal vagal neuropathy may result in radiological changes in the ipsilateral constrictor muscles due to associated pharyngeal plexopathy (Fig. 9). Atrophy and T1-weighted hyperintensity is usually associated with symptoms of over 6 months duration.8 It
also results in ipsilateral pharyngeal dilatation with fatty infiltration of the ipsilateral soft palate.3,6 As the cricothyroid muscle is the only laryngeal muscle to be innervated by proximal vagal branches, atrophy would be a useful indicator of a proximal lesion, although it is rarely detected.15 The paralysed vocal cord due to a proximal vagal lesion assumes an ‘‘intermediate’’ position (almost completely abducted), as opposed to a ‘‘paramedian’’ position of a distal lesion, due to the absence of cricothyroid adduction. Finally, the presence of other lower cranial nerve denervation changes would imply a proximal vagal nerve lesion,
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Figure 8 (aeb) Axial post-contrast CT images and (c) axial T2-weighted MRI. Imaging changes due to idiopathic chronic recurrent laryngeal nerve palsy (distal vagal nerve dysfunction). There is medial positioning of the ipsilateral aryepiglottic fold (a), dilatation of the ipsilateral pyriform sinus (a) and anteromedial positioning of the ipsilateral arytenoid cartilage (arrowhead in a). There is widening of the ipsilateral ventricle (b) and atrophy of the ipsilateral posterior cricoarytenoid muscle (arrowhead in b). Atrophy of the thyroarytenoid muscle and paramedian position of the ipsilateral vocal cord is demonstrated (c).
Figure 9 (a) T1-weighted axial post-gadolinium MRI and (b) STIR coronal MRI. Imaging changes due to proximal subacute vagal nerve dysfunction. Partial surgical resection of a right glomus temporale (a) has resulted in STIR hyperintensity within the right superior and middle constrictor muscles (arrowhead in b) as a result of proximal vagal damage.
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whereas bilateral changes would suggest a brainstem lesion. Most of the imaging changes of motor vagal nerve dysfunction described rely on the presence of decreased muscle volume and tone. Subacute muscular denervation changes have not been described but may be seen (Fig. 9). The imaging changes may be appreciated within a few weeks of neural injury, however, it is likely that they become clearer with a longer duration of paralysis.15 The alteration in morphology of the hemilarynx should not be misinterpreted. A fixed immobile cord due to mechanical interference from tumour infiltration of the thyroarytenoid muscle will often result in visible tumour within the paralaryngeal fat. A paramedian vocal cord may also result from arytenoid cartilage dislocation (typically secondary to traumatic intubation), and inflammatory pathology of the cricoarytenoid joint. However, in the setting of dislocation, the arytenoid cartilage would be situated anterior to the cricoid margin. Additional laryngeal muscle atrophy may be present with neural dysfunction but is unlikely to be exhibited with these other pathologies.15 As with the endolaryngeal changes, pharyngeal wall atrophy and MRI signal alteration should not be misconstrued as contralateral wall thickening due to inflammation or neoplasm. Acute vagal neuropathy and vocal cord paralysis is often idiopathic whereas chronic dysfunction is usually due to malignancy, surgical injury or idiopathic causes. An extensive list of structural lesions leading to vagal neuropathy have been identified on imaging studies, some of which are occult on clinical examination.3,6,8,15,34,35,38 Proximal vagal lesions include intracranial lesions (e.g. brainstem glioma), skull-base lesions (e.g. glomus
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jugulare and metastasis) and extracranial lesions (e.g. metastatic lymph nodes, vagal Schwannoma, parapharyngeal squamous cell carcinoma or salivary gland malignancy). Distal vagal (or recurrent laryngeal nerve) lesions may be extrathyroid neck tumours, thyoid masses or mediastinal masses (e.g. Pancoast tumour, lymphoma, aortic aneurysm).
Imaging changes due to spinal accessory (XI) nerve dysfunction The spinal accessory nerve arises from the spinal accessory nucleus in the anterolateral grey matter of the upper cervical cord. The nerve then ascends through the foramen magnum and exits the skull base through the jugular foramen. Within the jugular foramen, it exchanges fibres with the cranial part of the accessory nerve (bulbar motor supply). The spinal accessory nerve initially lies adjacent to the internal jugular vein and descends obliquely across the posterior triangle. It innervates the sternocleidomastoid muscle and together with the upper cervical nerves, it supplies the trapezius muscle.34,36,39 The radiological findings of denervation are only described in the later stages where there is atrophy of the ipsilateral trapezius and sternocleidomastoid muscles. A common feature is of associated compensatory hypertrophy of the levator scapulae muscle, which assumes the role of the major elevator and stabiliser of the scapula (Fig. 10). This muscle may also enhance slightly more than normal in the subacute phase.40 If the denervation results from a classical radical neck dissection, then the internal jugular vein and
Figure 10 (a) Contrast-enhanced coronal CT reformat (b) contrast-enhanced axial CT. Imaging changes due to spinal accessory nerve dysfunction. A right-sided classical neck dissection had been performed (note the surgical clips and sacrifice of sternocleidomastoid muscle and internal jugular vein). There is atrophy of the right trapezius muscle (arrowhead in a) and hypertrophy of the right levator scapulae muscle (arrowhead in b).
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sternocleidomastoid muscle will also have been resected. An underlying lesion may be evident from the posterior fossa superiorly to the posterior triangle inferiorly. The effects of spinal accessory nerve dysfunction may mimic pathology within the posterior neck muscles. The asymmetry produced by muscle atrophy may be misconstrued as an enlarged ‘‘normal’’ trapezius or sternocleidomastoid muscle. Alternatively, the compensatory enlargement of the levator scapulae muscle may present as an inflammatory or neoplastic pseudolesion, both clinically and radiologically. Spinal accessory nerve dysfunction is usually secondary to neck dissection with surgical sacrifice6 or tumour infiltration in the presence of gross metastatic nodal disease of the posterior triangle, high jugulodigastric region or skull base.
Imaging changes due to hypoglossal (X11) nerve dysfunction The hypoglossal nerve is almost completely formed by somatic motor fibres.34,41 The nucleus of the hypoglossal nerve in the medulla and 10e15 nerve rootlets exit the medulla in the antero-lateral (preolivary) sulcus. These traverse the premedullary cistern and unite after passing through the hypoglossal canal in the occipital bone. From here
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the hypoglossal nerve passes into the carotid space between the internal carotid artery and internal jugular vein and loops inferiorly to the level of the hyoid bone.34,41 It then travels upward to the sublingual space where it gives off branches to supply the intrinsic and extrinsic muscles of the tongue (genioglossus, styloglossus, and hyoglossus). Additional branches to the strap muscles, omohyoid muscle (arising in the mid neck) and geniohyoid muscle (within the sublingual space) are principally derived from a supply to the hypoglossal nerve from the first and second cervical nerves, which run with the hypoglossal nerve within the mid neck. Clinical findings of ipsilateral tongue weakness usually predate imaging changes, however, they may not be communicated by the referring clinician. There may be two patterns of muscle involvement due to proximal and distal nerve damage. With proximal lesions, the extrinsic and intrinsic tongue muscles will be effected, however, if the nerve is damaged in the mid-neck (also encompassing fibres supplied by the first and second cervical nerves) then the strap muscles and geniohyoid muscle will also be denervated. However, the latter pattern42 has rarely been described as a separate entity and denervation changes generally refer to altered appearances of the ipsilateral hemitongue. This finding should prompt inspection of the path of the hypoglossal
Figure 11 (a) T2-weighted axial MRI and (b) contrast-enhanced axial CT in a different patient. Imaging changes due to hypoglossal nerve dysfunction. A left hypoglossal nerve palsy (idiopathic) results in posterior prolapse of the left tongue base and a bulky appearance to the left palatine tonsil (a). Malignant squamous cell carcinoma adenopathy in relation to the right carotid sheath (patient had been symptomatic neck pain for 2 years) resulting in severe atrophy and fatty infiltration of the right tongue, which outlines the right lingual vessels (b).
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nerve from medulla to the sublingual space and posterior fossa to the hyoid bone. Evidence of other lower cranial nerve denervation changes localizes pathology proximal to the carotid sheath. The temporal changes of MRI findings in the denervated tongue have been studied.9,12,13e16 The sequence of ‘‘oedema-like’’ early changes and ‘‘fatty atrophic’’ changes are again described. The increased T1-weighted signal is generally appreciated earlier,9,13 and it has been recognized at 2 weeks.12,16 Other features noted are of a T1-weighted hypointense subacute phase13 and atrophy without signal change.12 Although muscle enlargement is rarely a feature,7,12 there is frequently prolapse of the affected hemitongue into the oropharynx due to loss of muscle tone (Fig. 11a). In longstanding denervation, the muscle bulk will no longer be visible on CT or MRI with only veins and arteries remaining intact (Fig. 11b). The T2-weighted hyperintensity and enhancement may be confused with inflammation, neoplasm or traumatic damage (including that induced by radiation) in the subacute phase.2 Heterogeneous appearance, extension across the midline, and changes in adjacent tissues will help distinguish these aetiologies. It is common for the flaccid tongue to present as a ‘‘pseudomass’’ in the tongue base with a distorted appearance to the ipsilateral pharyngeal tonsil. In addition, the atrophic denervated tongue may lead to misdiagnosis of a tumour mass in the contralateral normal tongue.6 Other articles provide comprehensive lists of lesions in the hypoglossal nerve34,41,43 and approximately half of these are due to tumours.43 In the literature describing imaging changes in the denervated tongue, skull-base tumours (meningioma, nasopharyngeal tumour extension, metastasis, sarcoma, chordoma, glomus tumour), hypoglossal nerve schwannoma, surgery, radiotherapy, metastatic nodal disease in the carotid sheath and upper aerodigestive tract or salivary carcinoma are featured.6,7,9,12e14,16
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4. Fischbein NJ, Kaplan MJ, Jackler RK, et al. MR imaging in two cases of subacute denervation changes in the muscles of facial expression. AJNR Am J Neuroradiol 2001;22: 880e4. 5. Fleckenstein JL, Watumull D, Conner KE, et al. Denervated human skeletal muscle: MR imaging evaluation. Radiology 1993;187:213e8. 6. Harnsberger HR, Dillon WP. Major motor atrophic patterns in the face and neck: CT evaluation. Radiology 1985;155: 665e70. 7. Ho TL, Lee KW, Lee HJ. Subacute mandibular and hypoglossal nerve denervation causing oedema of the masticator space and tongue. Neuroradiology 2003;45:262e6. 8. Jacobs CJ, Harnsberger HR, Lufkin RB, et al. Vagal neuropathy: evaluation with CT and MR imaging. Radiology 1987; 164:97e102. 9. Kato K, Tomura N, Takahashi S, et al. Motor denervation of tumours of the head and neck: changes in MR appearance. Magn Reson Med Sci 2002;1:157e64. 10. Kaylie DM, Jackson CG, Aulino JM, et al. Preoperative appearance of facial muscles on magnetic resonance predicts final facial function after acoustic neuroma surgery. Otol Neurotol 2004;25:622e6. 11. Kaylie DM, Wax MK, Weissman JL. Preoperative facial muscle imaging predicts final facial function after facial nerve grafting. AJNR Am J Neuroradiol 2003;24:326e30. 12. King AD, Ahuja A, Leung SF, et al. MR features of the denervated tongue in radiation induced neuropathy. Br J Radiol 1999;72:349e53. 13. Murakami R, Baba Y, Nishimura R, et al. MR of denervated tongue: temporal changes after radical neck dissection. AJNR Am J Neuroradiol 1998;19:515e8. 14. Murakami R, Baba Y, Nishimura R, et al. CT and MR findings of denervated tongue after radical neck dissection. AJNR Am J Neuroradiol 1998;18:747e50. 15. Romo LV, Curtin HD. Atrophy of the posterior cricoarytenoid muscle as an indicator of recurrent laryngeal nerve palsy. AJNR Am J Neuroradiol 1999;20:467e71. 16. Russo CP, Smoker WRK, Weissman JL. MR appearance of trigeminal and hypoglossal motor denervation. AJNR Am J Neuroradiol 1997;18:1375e83. 17. Schellhas KP. MR imaging of muscles of mastication. AJR Am J Roentgenol 1989;153:847e55. 18. Silverberg M, Demer J. Duane’s syndrome with compressive denervation of the lateral rectus muscle. Am J Ophthalmol 2001;131:146e8. 19. Sato M, Yagasaki T, Kora T, et al. Comparison of muscle volume between congenital and acquired superior oblique palsies by magnetic resonance imaging. Jpn J Ophthalmol 1998;42:466e70. 20. Hassler O. The angioarchitecture of normal and denervated skeletal muscle. An experimental microangiopathic study of the rabbit. Neurology 1970;20:1161e4. 21. Hudlicka O. Blood flow and oxygen consumption in muscles after section of ventral roots. Circ Res 1967;20: 570e7. 22. Polak JF, Jolesz FA, Adams DF. Magnetic resonance imaging of skeletal muscle prolongation of T1 and T2 subsequent to denervation. Invest Radiol 1988;23:365e9. 23. Romanul FC, Hogan EL. Enzymatic changes in denervated muscle. Arch Neurol 1965;13:263e82. 24. Stonnington HH, Engel AG. Normal and denervated muscle: a morphometric study of fine structure. Neurology 1973;23: 714e24. 25. Petersilge CA, Pathria MN, Gentili A, et al. Denervation hypertrophy of muscle: MR features. J Comput Assist Tomogr 1995;19:596e600.
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35. Phillips CD, Bubash LA. The facial nerve: anatomy and common pathology. Semin Ultrasound CT MR 2002;23:202e17. 36. Larson III TC, Aulino JM, Laine FJ. Imaging of the glossopharyngeal, vagus and accessory nerves. Semin Ultrasound CT MR 2002;23:238e55. 37. Richardson BE, Bastian RW. Clinical evaluation of vocal fold paralysis. Otolaryngol Clin North Am 2004;37: 45e58. 38. Agha FP. Recurrent laryngeal nerve paralysis: a laryngographic and computed tomographic study. Radiology 1983; 148:149e55. 39. Chandawarker RY, Cervino AL, Pennington GA. Management of iatrogenic injury to the spinal accessory nerve. Plast Reconstr Surg 2003;111:611e7. 40. Shpizner BA, Holliday RA. Levator scapulae muscle asymmetry presenting as a palpable neck mass: CT evaluation. ANJR Am J Neuroradiol 1993;14:461e4. 41. Loh C, Maya MM, Go JL. Cranial nerve XII: the hypoglossal nerve. Semin Ultrasound CT MR 2002;23:256e65. 42. Smoker WRK. The oral cavity. In: Som PM, Curtin HD, editors. Head and neck imaging. 4th ed. St Louis: Mosby; 2003. p. 1377e464. 43. Keane JR. Twelfth-nerve palsy. Analysis of 100 cases. Arch Neurol 1996;53:561e6.
PICTORIAL REVIEW
Imaging of muscular denervation secondary to motor cranial nerve dysfunction S.E.J. Connor*, N. Chaudhary, S. Fareedi, E.K. Woo Neuroradiology Department, Kings College Hospital, Denmark Hill, London SE5 9RS, UK Received 11 February 2006; received in revised form 30 March 2006; accepted 4 April 2006
The effects of motor cranial nerve dysfunction on the computed tomography (CT) and magnetic resonance imaging (MRI) appearances of head and neck muscles are reviewed. Patterns of denervation changes are described and illustrated for V, VII, X, XI and XII cranial nerves. Recognition of the range of imaging manifestations, including the temporal changes in muscular appearances and associated muscular grafting or compensatory hypertrophy, will avoid misinterpretation as local disease. It will also prompt the radiologist to search for underlying cranial nerve pathology, which may be clinically occult. The relevant cranial nerve motor division anatomy will be described to enable a focussed search for such a structural abnormality. ª 2006 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction Lower motor cranial nerve dysfunction has a profound effect on the muscles that it innervates. It results in an alteration of morphology, either due to reduced bulk of muscle or due to the loss of tone and position. The magnetic resonance imaging (MRI) signal, computed tomography (CT) attenuation and contrast medium enhancement are also affected. Moreover, compensatory hypertrophy of associated muscles, distortion of adjacent normal structures and therapeutic insertion of muscle grafts may all be misinterpreted as local pathology. Although cranial nerve dysfunction often leads to clinical manifestations, these may be non-specific and the identification of muscular denervation changes on imaging studies provides objective evidence of a lesion. Occasionally, the radiological changes in deep inaccessible muscle groups are clinically occult. By recognizing the patterns of muscular involvement, and understanding the relevant motor cranial nerve anatomy, the * Guarantor and correspondent: S.E.J. Connor, Neuroradiology Department, Kings College Hospital, Denmark Hill, London SE5 9RS, UK. Tel.: þ44 208 761 8344; fax: þ44 207 346 3120. E-mail address: [email protected] (S.E.J. Connor).
radiological search and scan volume may be focused appropriately. The imaging appearances of muscular denervation secondary to V, VII, X, XI and XII motor cranial nerve dysfunction have been studied1e17 and will form the basis of this review. As there are only isolated imaging reports of denervation in the extraocular muscles (cranial nerves III, IV, VI)18,19 and no reports of the stylopharyngeus muscle (cranial nerve IX), these will not be discussed. Appearances that may be misconstrued as local pathology will be emphasized.
Muscular denervation in the head and neck: general concepts and temporal changes Denervation of skeletal muscle leads to alterations in histology, biochemistry, enzymes and structure.20e25 The MRI appearances of denervated peripheral skeletal muscle have been described.25e27 They have been divided into the acute phase (<1 month), subacute phase (1 month to 1 year) and the chronic phase (>1 year). Appearances are frequently normal in the acute phase. The subacute phase is manifest by
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a prolonged T1 and T2 relaxation time. These imaging findings are attributed to relatively increased tissue water within the enlarged interstitial space of the affected muscle, which is created by decreased muscle fibril size.25e27 Increased contrast medium enhancement is also described in the subacute phase. This has been explained by an increased blood flow to the denervated muscle and increased accumulation in the enlarged extracellular space. Subacute denervation changes occasionally return to normal but usually progress to a chronic phase of fatty replacement with atrophy.6 This stage is easily recognized using CT (fat attenuation) or MRI (increased T1-weighted signal) in the larger muscle groups, although changes in smaller muscles may only be detected using MRI.10e11 The progression of denervation imaging changes secondary to trigeminal (V) nerve and hypoglossal (XII) nerve dysfunction have received most attention in the head and neck, as the corresponding masticator and tongue muscles are easily recognized on imaging studies.1,2,6,7,12e14,16,17 It does appear that different muscles develop the changes evident using MRI at different rates, and it is postulated that there are earlier and more conspicuous changes with muscles supplied by a single nerve.5 In view of the variable degree of neural damage and difficulties in defining the exact onset of dysfunction, it is unsurprising that there is marked variation in the reported timing and appearance of the MRI changes of muscular denervation. In general terms, the muscles of the head and neck also conform to patterns of early enhancing ‘‘oedema-like’’ change and later ‘‘fatty atrophic’’ change. Detailed descriptions of the temporal course in trigeminal and hypoglossal nerve related motor denervation are found in the appropriate sections.
Imaging changes due to trigeminal (V) nerve dysfunction The mandibular division of the trigeminal nerve provides motor supply to the masticator muscles (medial and lateral pterygoid, masseter and temporalis muscles), anterior belly of digastric, mylohyoid, tensor tympani and tensor veli palatini muscles28e30 (Fig. 1). Denervation changes in the muscles supplied by the trigeminal nerve may be secondary to a lesion along the course of motor fibres from brainstem to muscle. A review of the anatomy (Fig. 1) helps separate two distinct patterns, which may help localize a lesion. A proximal pattern of changes in all the muscles supplied by the trigeminal nerve indicates
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an injury to the nerve between the brainstem and the bifurcation into anterior and posterior trunks. A distal pattern, that affects only the mylohyoid and anterior belly of digastric muscles, indicates a lesion distal to the bifurcation (involving the posterior trunk, inferior alveolar or mylohyoid nerves). The MRI appearance of masticator muscle denervation6,7,9,16,17,31 has been divided into four categories16 (Table 1). Early (acute and subacute) phases are manifest by increased T2-weighted, short tau inversion recovery (STIR) signal and enhancement (Fig. 2) with an ‘‘oedema-like’’ appearance, whereas the chronic phase shows T1 hyperintense fatty infiltration and later atrophy (Fig. 3). There is considerable overlap in the timing and progression of the MRI appearances.6,7,9,16,17 A useful clue to the presence of a proximal pattern of trigeminal nerve damage, is the presence of serous otitis media (Fig. 3) secondary to tensor veli palatini and medial pterygoid dysfunction.7,32 Tensor veli palatini loss of tone may also be recognized as asymmetry of the torus tubarius. The distal pattern of isolated mylohyoid and anterior belly of digastric muscle involvement has only been described in the chronic atrophic phase6 (Fig. 4). Changes of masticator muscle denervation should not be confused with local pathology. The subacute ‘‘oedema-like’’ phase may mimic an inflammatory, neoplastic or traumatic aetiology, particularly if there is swelling. Such a process is less likely to involve all the relevant muscles diffusely. The differential diagnosis of atrophy and fatty infiltration of the muscles of mastication includes disuse, post-traumatic reflex sympathetic dystrophy, and congenital facial asymmetry and connective tissue disorders.17 It should be ensured that the contralateral normal muscle is not diagnosed as a mass. There are a myriad of lesions that may result in trigeminal nerve dysfunction and a full discussion is beyond the scope of this review.28e30,33 Typical imaging findings of muscular denervation changes have been described in the setting of brain stem lesions (bulbar poliomyelitis, cavernoma, haemorrhage, glioma), cavernous sinus lesions (neurogenic tumours, lymphoma, meningioma, metastasis, perineural tumour spread), skull-base lesions (chordoma, carcinoma, rhabdomyosarcoma) or secondary to rhizotomy and trauma.6,7,9,16,17,31
Imaging changes due to facial (VII) nerve dysfunction The facial somatic motor root innervates the muscles of facial expression, occipitalis, buccinator, platysma, stylohyoid and stapedius muscles.
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Figure 1 The course of the motor supply of the trigeminal nerve. The motor root emerges from the ventral pons and bypasses the gasserian ganglion, joining the mandibular division (V3) as it exits the skull base through the foramen ovale. All the motor fibres are distributed along this division. Immediately after supplying a small nerve to the medial pterygoid muscle (with fibres subsequently extending to tensor veli palatini and tensor tympani muscles via the otic ganglion) the mandibular nerve divides into a predominantly motor anterior trunk and a predominantly sensory posterior trunk. The former supplies temporalis, masseter and lateral pterygoid muscles, whilst the latter supplies the anterior belly of digastric and mylohyoid muscles via the inferior alveolar/mylohyoid nerves.
The muscles of facial expression are diminutive muscles. The course of the facial nerve may be divided into its pontine segment; the cisternal segment, which traverses the cerebellopontine angle cistern and internal auditory meatus; the intratemporal segment; and the extracranial segment, which enters the parotid gland.34,35 Table 1
Changes of denervation atrophy secondary to facial nerve dysfunction have been described using both CT and MRI.4,6,10,11 Lower motor neuron facial nerve dysfunction is usually clinically obvious, however, some patients with muscle atrophy revealed by MRI have had normal facial function.10,11 Changes in the orbicularis oculi,
Temporal sequence of denervation changes in masticator muscles described by Russo et al16
Acute Subacute Early chronic Late chronic
T1
T2
Size
Enhancement
Timing
Intermediate Increased Increased Markedly increased
Increased Increased Intermediate or increased Intermediate or increased
Increased Unchanged Unchanged Decreased
Yes Yes No No
Days to weeks 6e20 months* Not well defined >2 years**
Other authors describe a similar progression of MRI findings with the exception of: * Subacute denervations has been demonstrated within one month of symptom onset7 ** Muscle atrophy has been described at three months.7,9
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Figure 2 Gadolinium-enhanced fat-saturated T1weighted axial MRI. Imaging changes due to subacute trigeminal nerve dysfunction. Increased bulk and gadolinium enhancement is seen within the left lateral pterygoid muscle (arrowhead), masseter and temporalis muscles secondary to subacute denervation. A lesion within the cavernous sinus was detected more superiorly and perineural spread of adenoid cystic carcinoma along the trigeminal nerve was diagnosed. Symptoms had been present for 2 months at the time of the MRI and the muscles of mastication atrophied on imaging follow-up.
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Figure 4 T1-weighted axial MRI. Imaging changes due to chronic distal (inferior alveolar nerve) trigeminal nerve dysfunction. There is atrophy of the left anterior belly of digastric muscle (arrowhead indicates normal right side) due to sacrifice of the left inferior alveolar nerve at the time of resection and grafting for a left oropharyngeal salivary gland malignancy.
Figure 3 (a) T1-weighted gadolinium-enhanced MRI and (b) T2-weighted axial MRI. Imaging changes due to chronic trigeminal nerve dysfunction. A right parasellar trigeminal nerve Schwannoma with longstanding symptoms of trigeminal nerve dysfunction. Atrophy and T2-weighted hyperintensity (there was also T1-weighted hyperintensity) is demonstrated within the right medial and lateral pterygoid muscles (black arrowhead). Note the right middle ear effusion (white arrowhead) due to tensor veli palatini and medial pterygoid (eustachian tube) dysfunction.
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quadratus labii, platysma and buccinator muscles have all been illustrated (Fig. 5). In addition, one report has demonstrated T2 prolongation and contrast medium enhancement suggestive of subacute denervation changes. Due to the multiple connections between branches of the facial nerve, it is not expected that selective muscle denervation will be appreciated unless nerve damage is very peripheral. It is unlikely that imaging changes in these small muscles will mimic pathology, however, regional and free muscle flap transfers used for the treatment of chronic facial nerve paralysis may simulate a mass lesion within the facial soft tissues (Fig. 6). Although viral infection and trauma (typically related to temporal bone or parotid surgery) are the most common pathologies to affect the facial nerve,10,11,34,35 the effects are usually transient. Denervation changes in the facial muscles have only been described in the context of facial nerve dysfunction due to malignant infiltration of the parotid and after skull-base surgery.4,6,10,11 However, imaging is usually directed to establishing the aetiology of facial nerve palsy within the posterior fossa, petrous bone and parotid gland rather than the end organ effects.
Imaging changes due to vagal (X) nerve dysfunction The motor fibres of the vagus supply the soft palate, constrictor muscles, as well as the intrinsic and extrinsic laryngeal muscles (Fig. 7). The
Figure 5 T2-weighted axial MRI. Imaging changes due to longstanding left facial nerve dysfunction. There is atrophy of the left quadratus labii superioris (arrowhead indicated normal bulk on contralateral side).
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Figure 6 STIR coronal MRI. Imaging changes due to muscular grafting for chronic facial nerve dysfunction. There had been extensive infiltration of the nerve without primary grafting at the time of resection of a left malignant parotid tumour. Buccinator muscle atrophy is seen (arrow). Paradoxical volume loss within the left anterior belly of digastric is likely due to dysfunction of the posterior belly, which is supplied by the facial nerve. There is soft tissue seen in the left buccal region (arrowhead) due to a pectoralis minor free flap. If the facial nerve is not repaired or grafted at the time of surgery, the native denervated muscles undergo atrophy and scarring. Free muscle transfer may be necessary if regional muscle (temporalis muscle) has failed or does not provide adequate bulk. Other muscles have been utilized for free tissue transfer (gracilis, latissimus dorsi, the serratus anterior and the rectus abdominis muscles).
peripheral motor divisions of the vagus may be considered as proximal and distal branches.8,34,36 Dysfunction of the vagus nerve paralyses the larynx and is manifested by a hoarse voice. It has been suggested that the presence of additional oropharyngeal symptoms is useful in identifying a proximal vagal lesion.8 A proximal vagal lesion should be investigated using MRI of the skull base, and a distal vagal (or recurrent laryngeal nerve) lesion should be investigated using CT of the skull base through to the upper mediastinum.8,37 Imaging patterns of muscular denervation changes may also contribute to the differentiation of a proximal from distal (or recurrent laryngeal nerve) lesion and so focus the imager and imaging appropriately. As the patient’s voice may occasionally be unaffected, the imaging findings of denervation changes may be the first indication to the presence of vagal nerve palsy. Distal vagal neuropathy is most common, accounting for 90% of cases.3 Cross-sectional imaging has found thickening and medial positioning of the
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Figure 7 The course of the motor supply of the vagus nerve. The motor fibres of the vagus originate in the nucleus ambiguous of the medulla. The roots exit the posterolateral sulcus of the medulla and traverse the basilar cistern to the pars vascularis of the jugular foramen. The proximal extracranial vagus nerve descends in the nasopharyngeal carotid space with the IX, XI and XII cranial nerves. The vagus then continues inferiorly along the posterolateral aspect of the carotid artery to the aortic arch. The proximal motor branches arise from the nodose ganglion and supply the pharyngeal plexus (motor function to the superior and middle constrictor muscles and soft palate apart from the tensor veli palatini muscle) and the superior/external laryngeal nerve (motor function to the inferior constrictor and cricothyroid muscle). The distal branches relevant to the head and neck structures are the recurrent laryngeal nerves. The right recurrent laryngeal nerve leaves the vagus at the level of the right subclavian artery, whilst that on the left loops through the aortopulmonary window. Both nerves ascend within the tracheooesophageal groove and pass posterior to the thyroid gland before terminating in the larynx (motor function to the intrinsic muscles of the larynx).
ipsilateral aryepiglottic fold, dilatation of the ipsilateral pyriform sinus and ventricle, anteromedial positioning of the ipsilateral arytenoid cartilage, atrophy of the ipsilateral posterior cricoarytenoid muscle or thyroarytenoid muscle and fullness of the ipsilateral vocal cord to be the most consistently demonstrated features3,15 (Fig. 8). In addition to the laryngeal changes, a proximal vagal neuropathy may result in radiological changes in the ipsilateral constrictor muscles due to associated pharyngeal plexopathy (Fig. 9). Atrophy and T1-weighted hyperintensity is usually associated with symptoms of over 6 months duration.8 It
also results in ipsilateral pharyngeal dilatation with fatty infiltration of the ipsilateral soft palate.3,6 As the cricothyroid muscle is the only laryngeal muscle to be innervated by proximal vagal branches, atrophy would be a useful indicator of a proximal lesion, although it is rarely detected.15 The paralysed vocal cord due to a proximal vagal lesion assumes an ‘‘intermediate’’ position (almost completely abducted), as opposed to a ‘‘paramedian’’ position of a distal lesion, due to the absence of cricothyroid adduction. Finally, the presence of other lower cranial nerve denervation changes would imply a proximal vagal nerve lesion,
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Figure 8 (aeb) Axial post-contrast CT images and (c) axial T2-weighted MRI. Imaging changes due to idiopathic chronic recurrent laryngeal nerve palsy (distal vagal nerve dysfunction). There is medial positioning of the ipsilateral aryepiglottic fold (a), dilatation of the ipsilateral pyriform sinus (a) and anteromedial positioning of the ipsilateral arytenoid cartilage (arrowhead in a). There is widening of the ipsilateral ventricle (b) and atrophy of the ipsilateral posterior cricoarytenoid muscle (arrowhead in b). Atrophy of the thyroarytenoid muscle and paramedian position of the ipsilateral vocal cord is demonstrated (c).
Figure 9 (a) T1-weighted axial post-gadolinium MRI and (b) STIR coronal MRI. Imaging changes due to proximal subacute vagal nerve dysfunction. Partial surgical resection of a right glomus temporale (a) has resulted in STIR hyperintensity within the right superior and middle constrictor muscles (arrowhead in b) as a result of proximal vagal damage.
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whereas bilateral changes would suggest a brainstem lesion. Most of the imaging changes of motor vagal nerve dysfunction described rely on the presence of decreased muscle volume and tone. Subacute muscular denervation changes have not been described but may be seen (Fig. 9). The imaging changes may be appreciated within a few weeks of neural injury, however, it is likely that they become clearer with a longer duration of paralysis.15 The alteration in morphology of the hemilarynx should not be misinterpreted. A fixed immobile cord due to mechanical interference from tumour infiltration of the thyroarytenoid muscle will often result in visible tumour within the paralaryngeal fat. A paramedian vocal cord may also result from arytenoid cartilage dislocation (typically secondary to traumatic intubation), and inflammatory pathology of the cricoarytenoid joint. However, in the setting of dislocation, the arytenoid cartilage would be situated anterior to the cricoid margin. Additional laryngeal muscle atrophy may be present with neural dysfunction but is unlikely to be exhibited with these other pathologies.15 As with the endolaryngeal changes, pharyngeal wall atrophy and MRI signal alteration should not be misconstrued as contralateral wall thickening due to inflammation or neoplasm. Acute vagal neuropathy and vocal cord paralysis is often idiopathic whereas chronic dysfunction is usually due to malignancy, surgical injury or idiopathic causes. An extensive list of structural lesions leading to vagal neuropathy have been identified on imaging studies, some of which are occult on clinical examination.3,6,8,15,34,35,38 Proximal vagal lesions include intracranial lesions (e.g. brainstem glioma), skull-base lesions (e.g. glomus
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jugulare and metastasis) and extracranial lesions (e.g. metastatic lymph nodes, vagal Schwannoma, parapharyngeal squamous cell carcinoma or salivary gland malignancy). Distal vagal (or recurrent laryngeal nerve) lesions may be extrathyroid neck tumours, thyoid masses or mediastinal masses (e.g. Pancoast tumour, lymphoma, aortic aneurysm).
Imaging changes due to spinal accessory (XI) nerve dysfunction The spinal accessory nerve arises from the spinal accessory nucleus in the anterolateral grey matter of the upper cervical cord. The nerve then ascends through the foramen magnum and exits the skull base through the jugular foramen. Within the jugular foramen, it exchanges fibres with the cranial part of the accessory nerve (bulbar motor supply). The spinal accessory nerve initially lies adjacent to the internal jugular vein and descends obliquely across the posterior triangle. It innervates the sternocleidomastoid muscle and together with the upper cervical nerves, it supplies the trapezius muscle.34,36,39 The radiological findings of denervation are only described in the later stages where there is atrophy of the ipsilateral trapezius and sternocleidomastoid muscles. A common feature is of associated compensatory hypertrophy of the levator scapulae muscle, which assumes the role of the major elevator and stabiliser of the scapula (Fig. 10). This muscle may also enhance slightly more than normal in the subacute phase.40 If the denervation results from a classical radical neck dissection, then the internal jugular vein and
Figure 10 (a) Contrast-enhanced coronal CT reformat (b) contrast-enhanced axial CT. Imaging changes due to spinal accessory nerve dysfunction. A right-sided classical neck dissection had been performed (note the surgical clips and sacrifice of sternocleidomastoid muscle and internal jugular vein). There is atrophy of the right trapezius muscle (arrowhead in a) and hypertrophy of the right levator scapulae muscle (arrowhead in b).
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sternocleidomastoid muscle will also have been resected. An underlying lesion may be evident from the posterior fossa superiorly to the posterior triangle inferiorly. The effects of spinal accessory nerve dysfunction may mimic pathology within the posterior neck muscles. The asymmetry produced by muscle atrophy may be misconstrued as an enlarged ‘‘normal’’ trapezius or sternocleidomastoid muscle. Alternatively, the compensatory enlargement of the levator scapulae muscle may present as an inflammatory or neoplastic pseudolesion, both clinically and radiologically. Spinal accessory nerve dysfunction is usually secondary to neck dissection with surgical sacrifice6 or tumour infiltration in the presence of gross metastatic nodal disease of the posterior triangle, high jugulodigastric region or skull base.
Imaging changes due to hypoglossal (X11) nerve dysfunction The hypoglossal nerve is almost completely formed by somatic motor fibres.34,41 The nucleus of the hypoglossal nerve in the medulla and 10e15 nerve rootlets exit the medulla in the antero-lateral (preolivary) sulcus. These traverse the premedullary cistern and unite after passing through the hypoglossal canal in the occipital bone. From here
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the hypoglossal nerve passes into the carotid space between the internal carotid artery and internal jugular vein and loops inferiorly to the level of the hyoid bone.34,41 It then travels upward to the sublingual space where it gives off branches to supply the intrinsic and extrinsic muscles of the tongue (genioglossus, styloglossus, and hyoglossus). Additional branches to the strap muscles, omohyoid muscle (arising in the mid neck) and geniohyoid muscle (within the sublingual space) are principally derived from a supply to the hypoglossal nerve from the first and second cervical nerves, which run with the hypoglossal nerve within the mid neck. Clinical findings of ipsilateral tongue weakness usually predate imaging changes, however, they may not be communicated by the referring clinician. There may be two patterns of muscle involvement due to proximal and distal nerve damage. With proximal lesions, the extrinsic and intrinsic tongue muscles will be effected, however, if the nerve is damaged in the mid-neck (also encompassing fibres supplied by the first and second cervical nerves) then the strap muscles and geniohyoid muscle will also be denervated. However, the latter pattern42 has rarely been described as a separate entity and denervation changes generally refer to altered appearances of the ipsilateral hemitongue. This finding should prompt inspection of the path of the hypoglossal
Figure 11 (a) T2-weighted axial MRI and (b) contrast-enhanced axial CT in a different patient. Imaging changes due to hypoglossal nerve dysfunction. A left hypoglossal nerve palsy (idiopathic) results in posterior prolapse of the left tongue base and a bulky appearance to the left palatine tonsil (a). Malignant squamous cell carcinoma adenopathy in relation to the right carotid sheath (patient had been symptomatic neck pain for 2 years) resulting in severe atrophy and fatty infiltration of the right tongue, which outlines the right lingual vessels (b).
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nerve from medulla to the sublingual space and posterior fossa to the hyoid bone. Evidence of other lower cranial nerve denervation changes localizes pathology proximal to the carotid sheath. The temporal changes of MRI findings in the denervated tongue have been studied.9,12,13e16 The sequence of ‘‘oedema-like’’ early changes and ‘‘fatty atrophic’’ changes are again described. The increased T1-weighted signal is generally appreciated earlier,9,13 and it has been recognized at 2 weeks.12,16 Other features noted are of a T1-weighted hypointense subacute phase13 and atrophy without signal change.12 Although muscle enlargement is rarely a feature,7,12 there is frequently prolapse of the affected hemitongue into the oropharynx due to loss of muscle tone (Fig. 11a). In longstanding denervation, the muscle bulk will no longer be visible on CT or MRI with only veins and arteries remaining intact (Fig. 11b). The T2-weighted hyperintensity and enhancement may be confused with inflammation, neoplasm or traumatic damage (including that induced by radiation) in the subacute phase.2 Heterogeneous appearance, extension across the midline, and changes in adjacent tissues will help distinguish these aetiologies. It is common for the flaccid tongue to present as a ‘‘pseudomass’’ in the tongue base with a distorted appearance to the ipsilateral pharyngeal tonsil. In addition, the atrophic denervated tongue may lead to misdiagnosis of a tumour mass in the contralateral normal tongue.6 Other articles provide comprehensive lists of lesions in the hypoglossal nerve34,41,43 and approximately half of these are due to tumours.43 In the literature describing imaging changes in the denervated tongue, skull-base tumours (meningioma, nasopharyngeal tumour extension, metastasis, sarcoma, chordoma, glomus tumour), hypoglossal nerve schwannoma, surgery, radiotherapy, metastatic nodal disease in the carotid sheath and upper aerodigestive tract or salivary carcinoma are featured.6,7,9,12e14,16
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