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Clinical and Electromyographic Characteristics of Unilateral Vocal Fold Paralysis With Lower Cranial Nerve Injury
ARTICLE IN PRESS Clinical and Electromyographic Characteristics of Unilateral Vocal Fold Paralysis With Lower Cranial Nerve Injury *Rong Hu, *Yun Li, Wen Xu, Liyu Cheng, and Hui Ren, Beijing, China Summary: Objectives. The aim was to investigate the clinical and electromyographic characteristics of patients with unilateral vocal fold paralysis (UVFP) combined with lower cranial nerve injury. Study design. This is a case series with chart review. Methods. Among 368 patients with idiopathic UVFP, 31 patients (8.4%) were eventually diagnosed with lower cranial nerve palsy after examinations of the head and neck, radiology, and electromyogram (EMG). The clinical and electromyographic characteristics of these patients were analyzed. Results. Of the 31 patients, 27 patients exhibited obvious abnormal lower cranial nerve injury physical signs, and 4 patients showed atypical physical signs, identified by EMG. Ultimately, 41.9% (13/31) were diagnosed with idiopathic causes, 38.7% (12/31) with intracranial or skull-base lesions on radiology, 12.9% (4/31) with lower cranial neuritis, and 6.4% (2/31) with radiation-induced lower cranial nerve palsy. Among the cranial lesions, lesions of the jugular foramen region were the most common (50%, 6/12). All 26 patients who underwent EMG tests were confirmed to have vagus nerve impairments (11 complete and 15 incomplete) and accessory nerve impairments (16 complete and 10 incomplete), whereas only 13 patients (50%) exhibited hypoglossal nerve injuries (5 complete and 8 incomplete). Conclusions. For patients with clinically “idiopathic” UVFP, physical examinations of the lower cranial nerves are essential screening procedures. For patients with abnormal or suspicious physical signs, radiology should be performed to detect possible cranial or cervical lesions. EMG tests were strongly recommended to identify suspicious lower cranial nerve injury and its severity, and may help to predict the prognosis. Key Words: Vocal fold paralysis–Lower cranial nerve injury–Radiology–Laryngeal electromyogram–Nuchal electromyogram.
INTRODUCTION The etiologies of unilateral vocal fold paralysis (UVFP) are very complicated and include neoplasms, iatrogenic factors, infections, trauma, and idiopathic causes. In addition to recurrent laryngeal nerve (vagus nerve) palsy, lesions located in the brain stem or skull base are often associated with impairments of the other lower cranial nerves (ie, cranial nerves IX, XI, and XII). The symptom of hoarseness caused by UVFP may be the easiest to perceive; however, the symptomatology resulting from impairments of the lower cranial nerves is often inconspicuous, and signs of lower cranial nerve palsy may easily be overlooked by otolaryngologists or misdiagnosed as “idiopathic” or “sole” UVFP.1–5 Moreover, there are few published studies related to the detailed clinical and electromyographic features of UVFP combined with lower cranial nerve palsy. Thus, the objective of the present study was to investigate the clinical
Accepted for publication December 24, 2015. Conflict of interest: None. The research was presented orally at the Voice Foundation’s 43rd Annual Symposium, Philadelphia, PA, USA, May 28–June 1, 2014. Source of financial support or funding: Programs of Beijing Health Foundation of Highlevel Technical Personnel (2014-2-004) and Programs of National Natural Science Foundation of China (81170901). *The first two authors contributed equally to this work, and each is considered first author. From the Department of Otorhinolaryngology—Head and Neck Surgery, Beijing Tongren Hospital, Capital Medical University, Beijing, China. Address correspondence and reprint requests to Wen Xu, Department of Otorhinolaryngology—Head and Neck Surgery, Beijing Tongren Hospital, 1 Dongjiaominxiang, Beijing, 100730, China. E-mail: [email protected] Journal of Voice, Vol. ■■, No. ■■, pp. ■■-■■ 0892-1997 © 2015 The Voice Foundation. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jvoice.2015.12.016
and electromyographic characteristics of the patients with UVFP combined with lower cranial nerve palsy.
MATERIALS AND METHODS From April 2008 to October 2013, a consecutive series of 368 patients with initial diagnoses of idiopathic UVFP from the Department of Otorhinolaryngology—Head and Neck Surgery, Beijing Tongren Hospital, China, were included. Physical examinations of the head and neck including the lower cranial nerves and laryngostroboscopy were performed in all patients. The examined physical signs of the lower cranial nerves included the position and symmetry of the palate and uvula (the vagus nerve), shoulder shrugging and head rotation against resistance (the accessory nerve), and tongue position during protrusion and tongue atrophy or fasciculation (the hypoglossal nerve). Stroboscopic signs were evaluated by a laryngologist for the following characteristics: shape and movement of the vocal fold, glottal closure, mucosal wave, and supraglottic involvement. We conducted an interobserver study with blinded reviewers. A total of 31 patients (8.4%) were eventually diagnosed with UFVP with lower cranial nerve palsy by the physical examination and electromyogram (EMG) tests. The patients ranged in age from 19 to 61 years, and there were 9 females and 22 males. All patients were examined with radiological scans, and neurologists were consulted to determine the possible causes of the patients’ conditions. The entire set of EMG tests was performed in 26 patients with lower cranial nerve palsy. A four-channel Nicolet VikingQuest Electromyographic Instrument (Nicolet Biomedical, Madison,
ARTICLE IN PRESS 2 WI, USA) was used for recording. For the laryngeal EMG (LEMG), concentric needle electrodes were placed percutaneously into the thyroarytenoid muscle, the cricothyroid muscle, and the posterior cricoarytenoid (PCA) muscle. The evoked response potentials (Eps) of the laryngeal muscles were investigated with monopolar needle electrodes that stimulated the recurrent laryngeal nerve, superior laryngeal nerve, and vagus nerve. The details of the LEMG techniques and interpretations have been described in our previous study.6,7 The spontaneous potential activity patterns, motor unit potential (MUP) characteristics, and recruitment patterns of the involved laryngeal muscles were assessed. The amplitudes, latencies, durations, and waveforms of the Eps were evaluated. The measurement parameters for the lower cranial nerve-related EMG were similar to those used for LEMG. The recording electrodes were placed percutaneously into the following muscles: the sternocleidomastoid muscle (SCM), the trapezius muscle (TRA), and the genioglossus muscle. For the accessory nerve-evoked EMG of the SCM and TRA, the stimulating electrode was inserted percutaneously at the median point of the SCM posterior border. For the hypoglossal nerveevoked EMG of the genioglossus muscle, the stimulating electrode was inserted percutaneously at the mandibular angle from the submandibular surface. The EMG data from the healthy sides were used as the normal controls. All subjects, including the patients and control subjects, agreed to participate in this study and provided written informed consent. The study was approved by our local ethics committee and institutional review board. The SPSS/PC 11.5 package (SPSS Inc., Chicago, IL, USA) was used for the statistical analyses of the data. The EMG results from all groups were tested with one-way analyses of variance. All tests were two sided, and a P value of <0.05 was considered statistically significant. RESULTS Clinical characteristics A total of 31 patients (31/368, 8.4%) were eventually diagnosed with UVFP combined with lower cranial nerve palsy by physical examination and EMG tests. The main complaints of the patients were moderate to severe persistent hoarseness with breathiness, vocal fatigue, effortful phonation, and aspiration. The durations ranged from 20 days to 38 years (median 10.5 months). The durations of the 12 patients with intracranial or skull-base lesions ranged from 1 month to 9 years (median 18 months), and these patients exhibited longer overall durations than the other patients. On laryngostroboscopy, 14 patients exhibited left-side VFP, and 17 patients exhibited rightside VFP. The affected vocal folds of all of the patients were found to be completely fixed in the paramedian or abduction positions with accompanying glottic insufficiency. Based on the physical examinations and EMG, all 31 of the patients were found to have vagus nerve involvement (100%). A total of 27 patients (80.6%) were found with obvious abnormal physical examination of the accessory nerve injury. However, four patients (12.9%) who showed suspicious accessory nerve involvement had the atypical history and physical examination:
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TABLE 1. The Intracranial or Skull-base Lesions Caused Lower Cranial Nerve Palsy Location Skull-base region Intracranial region
Lesions
Cases
Glomus jugular tumors Schwannoma Meningioma Vertebral artery aneurysm Brainstem meningioma Cerebellopontine angle tumor Medulla oblongata infarction
4 3 1 1 1 1 1
two of them had no obvious causes, one had a history of a cold, and one may had congenital causes. And their SCM and TRA muscles atrophy was not so obvious. But the definite diagnoses of them were still neuropathic injury by EMG. The hypoglossal nerve involvement was observed in 13 cases (41.9%). Further radiological examinations revealed intracranial or skullbase lesions in 12 cases (38.7%; Table 1). Four patients (4/31, 12.9%) were ultimately diagnosed with infectious lower cranial neuritis by the neurologist. Two cases (6.4%) had previous histories of radiotherapy due to the malignant tonsil tumor 28 years prior and a malignant parotid gland tumor 2 years prior. No causes were identified in the other 13 cases (41.9%). The clinical characteristics of the patients with lower cranial nerve palsy are summarized in Table 2. EMG characteristics Based on our previous LEMG study,6 the involved nerve impairments were grouped into complete and incomplete injuries. The EMG characteristics of incomplete impairments included reduced MUP amplitudes without abnormal MUP patterns or spontaneous electrical activity, mixed or pathological interference recruitment patterns with decreased amplitudes, and abnormal Eps of the target muscles (ie, delayed latency, prolonged duration, or decreased amplitude). The EMG characteristics of the complete impairments included denervation potential patterns (ie, electrical silence, fibrillation potentials, or positive sharp waves) or regeneration potential, mixed or simple recruitment patterns, and the absence of Eps in the target muscles. The general and evoked electromyography parameters of the SCM, TRA, and genioglossus muscles are listed in Tables 3 and 4. The fibrillation potentials or positive sharp waves can be observed in 7 patients with the course of 20 days to 2 months. The denervation potentials gradually reduce with the time. The regeneration potential of laryngeal muscles and SCM can be first seen in the patient with duration of 2 months. And most patients (14 patients) with regeneration potential had the duration of more than 6 months. The EMG patterns were showed in Figure 1. Among the 26 patients who underwent EMG tests, all (100%) exhibited the vagus nerve and the accessory nerve involvement, and 13 patients (50%) also exhibited hypoglossal nerve involvement. All of the patients with accessory nerve impairments exhibited both SCM and TRA muscle involvement. The synkinesia was only seen in the PCA muscles, in which the vagus nerves
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Characteristics of UVFP with Lower Cranial Nerve Injury
TABLE 2. Clinical Characteristics of Patients with Lower Cranial Nerve Palsy Group Characteristics Duration (months) Median (Range) Impaired side Left Right Neurologic involvement Vagus nerve Accessory nerve Hypoglossal nerve
n = 31
Cranial or Cervical Lesions (n = 12)
Cranial Neuritis (n = 4)
Radiation Induced (n = 2)
Idiopathic (n = 13)
10.5 (0.67–456)
18 (1–108)
7 (0.67–360)
– (1–54)
1.5 (1–456)
14 17
3 9
3 1
1 1
8 5
31 29 13
12 12 8
4 4 2
2 1 1
13 12 2
were completely injured. The EMG characteristics of the involved lower cranial nerves are presented in Figure 2. Among the 10 patients with intracranial or skull-base lesions, the majority (8 patients; 80%) exhibited complete impairments of both the vagus and accessory nerves, and 6 patients (60%) exhibited hypoglossal nerve complete impairment. The laryngeal synkinesia (PCA muscles) can be found in 8 patients (80%). Among the 10 patients with idiopathic lower cranial nerve palsy without any cause, incomplete impairments were observed in the majority (100% of the vagus nerves and 60% of the accessory nerves). The hypoglossal nerves were normal or exhibited incomplete impairment (60% and 20%, respectively). The four patients with atypical physical signs were all in this group and demonstrated the vagus nerve and accessory nerve incomplete injury. The laryngeal synkinesia (PCA muscles) can be found in two patients (20%). Among the four patients with lower cranial neuritis who were diagnosed by the neurologist, the nerve impairments were relatively more frequent in the accessory nerve (three patients were
completely impaired) than the vagus nerve (one patient were completely impaired). The hypoglossal nerves appeared normal or exhibited incomplete impairments (50% each). One patient with an acute stage in the duration of 20 days received the antiviral and nerve nutritional therapy for 1 month. Three months later, the patient undertook the re-EMG tests and showed that the fibrillation potentials disappeared, and the EMG signals were nearly normal. The laryngeal synkinesia (PCA muscles) can be found only in one patient. In one patient with a history of radiotherapy due to a malignant tumor in the right tonsil 28 years prior, the right vagus nerve and the accessory nerve were both completely impaired, but the hypoglossal nerve was not involved. In another patient with a history of radiotherapy due to a malignant tumor of the left parotid gland 2 years prior, the left vagus nerve was completely impaired, whereas the accessory nerve and the hypoglossal nerve were both incompletely impaired. Myokymic discharges and laryngeal synkinesia (PCA muscles) were observed in both of these patients.
TABLE 3. Nuchal Electromyography Parameters Nerves The vagus nerve
The accessory nerve
The hypoglossal nerve
Muscles Thyroarytenoid muscles Cricothyroid muscles Posterior cricoaryntenoid muscles Sternocleidomastoid muscles Trapezius muscles Genioglossus muscles
Groups
No. of Cases
Amplitude (μV)
Duration (ms)
Maximum Amplitude (μV)
Nerve impaired Normal Nerve impaired Normal Nerve impaired Normal
26 26 26 26 26 26
132.6 ± 69.3* 194.8 ± 99.0 158.5 ± 185.7 183.4 ± 93.7 141.7 ± 118.5** 234.6 ± 90.7
3.8 ± 1.6 4.0 ± 1.0 4.4 ± 1.5 3.9 ± 1.0 5.5 ± 5.7 4.2 ± 0.9
261.2 ± 172.1** 1618.0 ± 187.4 313.2 ± 154.8** 1208.0 ± 412.2 316.7 ± 260.2 1383.3 ± 541.9**
Nerve impaired Normal Nerve impaired Normal Nerve impaired Normal
26 26 26 26 13 26
121.7 ± 82.0 198.0 ± 121.0 103.1 ± 62.4* 201.7 ± 133.3 153.0 ± 79.1* 202.0 ± 59.5
3.9 ± 1.5 4.0 ± 1.1 4.3 ± 2.1 4.0 ± 1.2 4.9 ± 1.2 3.9 ± 0.7
368.6 ± 352.8** 1031.7 ± 771.0 418.2 ± 380.0* 1052.1 ± 795.0 713.1 ± 662.6** 1195.8 ± 336.8
Note: Data are mean ± standard deviation. * Compared with normal subjects, P < 0.05. **Compared with normal subjects, P < 0.01.
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TABLE 4. Evoked Nuchal Electromyography Parameters Nerves The vagus nerve
Muscles
Groups
No. of Cases
Latent Period (ms)
Duration (ms)
Amplitude (mv)
Thyroarytenoid muscles
Completely impaired Incompletely impaired Normal Completely impaired Incompletely impaired Normal Completely impaired Incompletely impaired Normal Completely impaired Incompletely impaired Normal Completely impaired Incompletely impaired Normal Completely impaired Incompletely impaired Normal
17 9 26 17 9 26 17 9 26 11 15 26 11 15 26 5 8 26
– 1.9 ± 0.2* 1.6 ± 0.3 – 1.8 ± 0.2** 1.6 ± 0.1 – 2.6 ± 0.8** 1.6 ± 0.1 – 4.4 ± 1.2** 2.0 ± 0.5 – 4.5 ± 1.3** 1.4 ± 1.0 – 2.8 ± 1.1** 1.7 ± 0.4
– 8.3 ± 3.5** 6.1 ± 0.9 – 7.3 ± 2.4 6.2 ± 1.2 – 12.0 ± 3.8** 6.0 ± 1.2 – 10.8 ± 6.1** 7.1 ± 1.9 – 11.2 ± 4.8** 5.1 ± 4.6 – 9.3 ± 2.5** 5.7 ± 1.4
– 1.1 ± 0.6** 8.6 ± 4.5 – 3.1 ± 1.7** 8.1 ± 3.4 – 2.0 ± 1.7** 6.4 ± 2.9 – 2.0 ± 0.8** 8.7 ± 8.8 – 1.6 ± 0.7** 7.2 ± 1.5 – 3.6 ± 1.8** 10.4 ± 5.4
Cricothyroid muscles
Posterior cricoaryntenoid muscles The accessory nerve
Sternocleidomastoid muscles Trapezius muscles
The hypoglossal nerve
Genioglossal muscles
Note: Data are mean ± standard deviation. * Compared with normal subjects, P < 0.05. **Compared with normal subjects, P < 0.01.
FIGURE 1. The EMG patterns of patients with an acute and a chronic duration. (A1~A5) One patient with idiopathic lower cranial nerve injury with the duration of 1 month showed the fibrillation potentials in the TA, TRA, and genioglossus muscles, and the positive sharp waves in the PCA and SCM muscles. (B1~B4) One patient with lower cranial nerve injury due to the jugular foramen schwannoma with the duration of 2 years showed the regeneration potentials in the CT, TA, SCM, and TRA muscles. CT, cricothyroid; EMG, electromyogram; PCA, posterior cricoarytenoid; SCM, sternocleidomastoid muscle; TA, thyroarytenoid; TRA, trapezius muscle.
ARTICLE IN PRESS Rong Hu et al
Characteristics of UVFP with Lower Cranial Nerve Injury
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FIGURE 2. The EMG characteristics of nerve impairment. EMG, electromyogram; IC, intracranial or skull-base lesions; ID, idiopathic; LCN, lower cranial neuritis; RA, radiation induced.
DISCUSSION Lesions affecting the recurrent laryngeal nerve in the cervicothoracic region are easier to detect during routine examinations that include ultrasound of the thyroid gland, chest X-ray, and upper gastrointestinal radiography. However, some cases of UVFP due to intracranial or skull-base lesions with combined lower cranial nerve palsy may easily be missed or misdiagnosed as “idiopathic” or “sole” recurrent nerve injury by otolaryngologists due to insidious onset, long duration, and hidden lesions. Among our consecutive series of 368 idiopathic UVFP patients acquired over 5 years, 8.4% exhibited combined lower cranial nerve palsy. The most common cause was idiopathic (13 patients, 41.9%), followed in order of decreasing frequency by intracranial or skull-base lesions (12 patients, 38.7%), infectious lower cranial neuritis (4 patients, 12.9%), and radiotherapy (2 patients, 6.5%). Abnormal physical signs of the lower cranial nerves can actually be readily observed; these signs include asymmetry of the uvula and palate (vagus nerve palsy), excursion of the tongue to the affected side during protrusion and atrophy of tongue muscles (hypoglossal nerve palsy), and atrophy of the SCM and TRA (accessory nerve palsy). Among our 368 consecutive patients who were initially diagnosed with idiopathic UVFP, 31 patients (8.4%) were eventually diagnosed with lower cranial nerve palsy with abnormal physical signs of the lower cranial nerves and EMG tests. Regular physical examinations of the lower cranial nerves are preliminary screenings for idiopathic UVFP patients, which are necessary to exclude other cranial nerve injuries. For the patients with suspicious or abnormal physical and EMG signs of the lower cranial nerves, magnetic resonance imaging (MRI) or computed tomography (CT) scans of the skull and neck are essential to exclude cranial or cervical lesions. In our study, 12 of 31 patients (38.7%) had abnormal radiologic findings that included jugular foramen region lesions (50%), parapharyngeal space tumors (16.7%), vertebral artery aneurysms (8.3%), brainstem neoplasms (8.3%), cerebellopontine angle tumors (8.3%), and medulla oblongata infarctions (8.3%). The most common
location in our study was jugular foramen region; these lesions always affect the cranial nerves IX, X, and XI. For the patients with suspicious lower cranial nerve involvement who had the atypical history and physical examination making a definite diagnosis, EMG tests helped to clarify the diagnosis. In this study, four patients could not be defined only by history and physical examination. But EMG revealed that the lower cranial nerve had incomplete neuropathic injuries. So, the EMG tests were also strongly recommended to investigate the nerve injured and its severity. According to our EMG tests, all the vagus nerves were involved and showed severe injury. Among the other lower cranial nerves, the accessory nerve was the most vulnerable as indicated by its relatively more severe impairment, and the hypoglossal nerve was relatively mildly impaired. The EMG test has been used to confirm peripheral nerve impairment and subsequently to determine the degree of injury and predict the prognosis. The spontaneous potentials and waveform morphologies on EMG can be utilized as qualitative diagnostic indicators of nerve injury.8–10 Our EMG results also revealed that although all of the affected vocal folds were completely fixed, the severity of combined lower cranial nerve injuries were varied in different causes. Two patients (20%) with intracranial or skull-base lesions exhibited incomplete lower cranial nerve injuries, which may have been due to early detections and short disease durations. The other eight patients (80%) with neoplasms exhibited the most severe degree of injury that included complete impairments of the vagus combined with the accessory nerves on EMG. This finding may have been to the gradual development and longer durations (median 18 months) of these intracranial lesions, which would lead to consistent and progressive damage to the affected nerve and worse prognoses. Thus, we considered that for the patients with the occupying lesions, nerves damage was more serious and gradually increased with the extension of the course. The majority of the patients with lower cranial neuritis and idiopathic factors always presented with incomplete nerve injuries, particularly in the vagus nerve, but showed more severe injury
ARTICLE IN PRESS 6 in accessory nerve. These conditions primarily caused incomplete impairments and may require active treatment as soon as possible. The nerve function may be restored after the treatment. In our study, one patient of lower cranial neuritis with incomplete nerve injury received antiviral and nerve nutritional therapy 20 days after onset for 1 month, and recovered generally normal EMG signals 3 months later, which indicates that the outcome of some incomplete nerve injuries may be better. So, the EMG also can predict the prognosis, but further follow up is still needed. Radiation treatments in the head and neck region can cause delayed injuries to the lower cranial nerves that often occur 5–8 years after radiotherapy.11–13 In our study, radiation-induced impairment of the vagus nerve and accessory nerve was always complete, and the hypoglossal nerve was the least extensive; these impairments occurred 2 and 28 years after radiotherapy. Abnormal spontaneous electrical activities characteristic of radiationinduced peripheral neuropathy,12 such as myokymic discharges, were also observed. Our study also found that the EMG characteristics of lower cranial nerve injury were similar to that of laryngeal nerve injury. In the early stage of the injury, the spontaneous potentials were mainly denervation potential patterns, whereas in the chronic stage, the spontaneous potentials were mainly regeneration potential patterns. The synkinesia was only seen in the PCA muscles, whose vagus nerve showed complete injury, which indicated that the synkinesia may reflect the severity of nerve injury. In addition, we found that there were no synkinesia observed in SCM and TRA muscles. This may be because there were plentiful traffic branches between the accessory nerve and the cervical plexus. After the accessory nerve injury, some motor branches of cervical plexus can replace parts of the accessory nerve function. So, the accessory nerves may not have the fault regeneration of nerve fibers. In genioglossus muscles, the synkinesia was not found either, which may be due to the incomplete hypoglossal nerve injury in our study. Our study still needs further research with large sample. CONCLUSIONS Among all of the patients in our study, 8.4% with “idiopathic” UVFP also exhibited injuries in the other lower cranial nerves. The most common cause was idiopathic (41.9%), followed by intracranial or skull-base lesions (38.7%), infectious lower cranial neuritis (12.9%), and radiotherapy (6.5%). The most common location of skull-base lesion in our study was the jugular foramen region. For the patients with atypical history and physical examination, EMG tests were strongly recommended to identify
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whether there is suspicious lower cranial nerve involvement. Based on the physical examinations and EMG, the vagus and accessory nerves were the most vulnerable to injury, followed by the hypoglossal nerve. Due to insidious onset and long duration, these conditions may be easy to be missed or misdiagnosed as “idiopathic” or “sole” vocal fold paralysis. The lower cranial nerve impairments caused by intracranial or skull-base lesions and radiation are generally complete and have poor prognoses. Lower cranial neuritis and idiopathic conditions predominately lead to incomplete impairments, and active treatment should be applied as early as possible to achieve good prognoses. Therefore, for the patients with clinically “idiopathic” vocal fold immobility, head, neck, and lower cranial nerve examinations, cranial radiology, and especially EMG tests should be performed to identify other lower cranial nerve injuries and their severities. REFERENCES 1. Hayward D, Morgan C, Emami B, et al. Jugular foramen syndrome as initial presentation of metastatic lung cancer. J Neurol Surg Rep. 2012;73:14–18. 2. Al-Khayat H, Beshay J, Manner D, et al. Vertebral artery-posteroinferior cerebellar artery aneurysms: clinical and lower cranial nerve outcomes in 52 patients. Neurosurgery. 2005;56:2–10. 3. Lv X, Jiang C, Li Y, et al. Clinical outcomes of lower cranial nerve palsies caused by vertebral artery-posteroinferior cerebellar artery aneurysms after endovascular embolization. Neurol Res. 2010;32:796–800. 4. Dqbrowska A, Jałowin´ski R, Tarnowska C, et al. Paralysis of vocal fold as the first symptom of Vernet’s syndrome in the course of jugular chemodectoma. Otolaryngol Pol. 2006;60:773–777. 5. Lo Casto A, Spataro R, Purpura P, et al. Unilateral laryngeal and hypoglossal paralysis (Tapia’s syndrome) in a patient with an inflammatory pseudotumor of the neck. Clin Neurol Neurosurg. 2013;115:1499–1501. 6. Xu W, Han D, Hou L, et al. Value of Laryngeal electromyography in diagnosis of vocal fold immobility. Ann Otol Rhinol Laryngol. 2007;116:576–581. 7. Xu W, Han D, Hou L, et al. Clinical and electrophysiological characteristics of larynx in myasthenia gravis. Ann Otol Rhinol Laryngol. 2009;118:656– 661. 8. Xu W, Han D, Hu R, et al. Characteristics of vocal fold immobility following endotracheal intubation. Ann Otol Rhinol Laryngol. 2012;121:689–694. 9. Simpson DM, Sternman D, Graves-Wright J, et al. Vocal cord paralysis: clinical and electrophysiologic features. Muscle Nerve. 1993;16:952–957. 10. Kupfer RA, Old MO, Oh SS, et al. Spontaneous laryngeal reinnervation following chronic recurrent laryngeal nerve injury. Laryngoscope. 2013;123:2216–2227. 11. Lin YS, Jen YM, Lin JC. Radiation-related cranial nerve palsy in patients with nasopharyngeal carcinoma. Cancer. 2002;95:404–409. 12. Shin HY, Park HJ, Choi YC, et al. Clinical and electromyographic features of radiation-induced lower cranial neuropathy. Clin Neurophysiol. 2013;124:598–602. 13. Hsieh YL, Chang MH, Wang CC. Laryngeal electromyography findings of vocal fold immobility in patients after radiotherapy for nasopharyngeal carcinoma. Head Neck. 2014;36:867–872.
INTRODUCTION The etiologies of unilateral vocal fold paralysis (UVFP) are very complicated and include neoplasms, iatrogenic factors, infections, trauma, and idiopathic causes. In addition to recurrent laryngeal nerve (vagus nerve) palsy, lesions located in the brain stem or skull base are often associated with impairments of the other lower cranial nerves (ie, cranial nerves IX, XI, and XII). The symptom of hoarseness caused by UVFP may be the easiest to perceive; however, the symptomatology resulting from impairments of the lower cranial nerves is often inconspicuous, and signs of lower cranial nerve palsy may easily be overlooked by otolaryngologists or misdiagnosed as “idiopathic” or “sole” UVFP.1–5 Moreover, there are few published studies related to the detailed clinical and electromyographic features of UVFP combined with lower cranial nerve palsy. Thus, the objective of the present study was to investigate the clinical
Accepted for publication December 24, 2015. Conflict of interest: None. The research was presented orally at the Voice Foundation’s 43rd Annual Symposium, Philadelphia, PA, USA, May 28–June 1, 2014. Source of financial support or funding: Programs of Beijing Health Foundation of Highlevel Technical Personnel (2014-2-004) and Programs of National Natural Science Foundation of China (81170901). *The first two authors contributed equally to this work, and each is considered first author. From the Department of Otorhinolaryngology—Head and Neck Surgery, Beijing Tongren Hospital, Capital Medical University, Beijing, China. Address correspondence and reprint requests to Wen Xu, Department of Otorhinolaryngology—Head and Neck Surgery, Beijing Tongren Hospital, 1 Dongjiaominxiang, Beijing, 100730, China. E-mail: [email protected] Journal of Voice, Vol. ■■, No. ■■, pp. ■■-■■ 0892-1997 © 2015 The Voice Foundation. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jvoice.2015.12.016
and electromyographic characteristics of the patients with UVFP combined with lower cranial nerve palsy.
MATERIALS AND METHODS From April 2008 to October 2013, a consecutive series of 368 patients with initial diagnoses of idiopathic UVFP from the Department of Otorhinolaryngology—Head and Neck Surgery, Beijing Tongren Hospital, China, were included. Physical examinations of the head and neck including the lower cranial nerves and laryngostroboscopy were performed in all patients. The examined physical signs of the lower cranial nerves included the position and symmetry of the palate and uvula (the vagus nerve), shoulder shrugging and head rotation against resistance (the accessory nerve), and tongue position during protrusion and tongue atrophy or fasciculation (the hypoglossal nerve). Stroboscopic signs were evaluated by a laryngologist for the following characteristics: shape and movement of the vocal fold, glottal closure, mucosal wave, and supraglottic involvement. We conducted an interobserver study with blinded reviewers. A total of 31 patients (8.4%) were eventually diagnosed with UFVP with lower cranial nerve palsy by the physical examination and electromyogram (EMG) tests. The patients ranged in age from 19 to 61 years, and there were 9 females and 22 males. All patients were examined with radiological scans, and neurologists were consulted to determine the possible causes of the patients’ conditions. The entire set of EMG tests was performed in 26 patients with lower cranial nerve palsy. A four-channel Nicolet VikingQuest Electromyographic Instrument (Nicolet Biomedical, Madison,
ARTICLE IN PRESS 2 WI, USA) was used for recording. For the laryngeal EMG (LEMG), concentric needle electrodes were placed percutaneously into the thyroarytenoid muscle, the cricothyroid muscle, and the posterior cricoarytenoid (PCA) muscle. The evoked response potentials (Eps) of the laryngeal muscles were investigated with monopolar needle electrodes that stimulated the recurrent laryngeal nerve, superior laryngeal nerve, and vagus nerve. The details of the LEMG techniques and interpretations have been described in our previous study.6,7 The spontaneous potential activity patterns, motor unit potential (MUP) characteristics, and recruitment patterns of the involved laryngeal muscles were assessed. The amplitudes, latencies, durations, and waveforms of the Eps were evaluated. The measurement parameters for the lower cranial nerve-related EMG were similar to those used for LEMG. The recording electrodes were placed percutaneously into the following muscles: the sternocleidomastoid muscle (SCM), the trapezius muscle (TRA), and the genioglossus muscle. For the accessory nerve-evoked EMG of the SCM and TRA, the stimulating electrode was inserted percutaneously at the median point of the SCM posterior border. For the hypoglossal nerveevoked EMG of the genioglossus muscle, the stimulating electrode was inserted percutaneously at the mandibular angle from the submandibular surface. The EMG data from the healthy sides were used as the normal controls. All subjects, including the patients and control subjects, agreed to participate in this study and provided written informed consent. The study was approved by our local ethics committee and institutional review board. The SPSS/PC 11.5 package (SPSS Inc., Chicago, IL, USA) was used for the statistical analyses of the data. The EMG results from all groups were tested with one-way analyses of variance. All tests were two sided, and a P value of <0.05 was considered statistically significant. RESULTS Clinical characteristics A total of 31 patients (31/368, 8.4%) were eventually diagnosed with UVFP combined with lower cranial nerve palsy by physical examination and EMG tests. The main complaints of the patients were moderate to severe persistent hoarseness with breathiness, vocal fatigue, effortful phonation, and aspiration. The durations ranged from 20 days to 38 years (median 10.5 months). The durations of the 12 patients with intracranial or skull-base lesions ranged from 1 month to 9 years (median 18 months), and these patients exhibited longer overall durations than the other patients. On laryngostroboscopy, 14 patients exhibited left-side VFP, and 17 patients exhibited rightside VFP. The affected vocal folds of all of the patients were found to be completely fixed in the paramedian or abduction positions with accompanying glottic insufficiency. Based on the physical examinations and EMG, all 31 of the patients were found to have vagus nerve involvement (100%). A total of 27 patients (80.6%) were found with obvious abnormal physical examination of the accessory nerve injury. However, four patients (12.9%) who showed suspicious accessory nerve involvement had the atypical history and physical examination:
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TABLE 1. The Intracranial or Skull-base Lesions Caused Lower Cranial Nerve Palsy Location Skull-base region Intracranial region
Lesions
Cases
Glomus jugular tumors Schwannoma Meningioma Vertebral artery aneurysm Brainstem meningioma Cerebellopontine angle tumor Medulla oblongata infarction
4 3 1 1 1 1 1
two of them had no obvious causes, one had a history of a cold, and one may had congenital causes. And their SCM and TRA muscles atrophy was not so obvious. But the definite diagnoses of them were still neuropathic injury by EMG. The hypoglossal nerve involvement was observed in 13 cases (41.9%). Further radiological examinations revealed intracranial or skullbase lesions in 12 cases (38.7%; Table 1). Four patients (4/31, 12.9%) were ultimately diagnosed with infectious lower cranial neuritis by the neurologist. Two cases (6.4%) had previous histories of radiotherapy due to the malignant tonsil tumor 28 years prior and a malignant parotid gland tumor 2 years prior. No causes were identified in the other 13 cases (41.9%). The clinical characteristics of the patients with lower cranial nerve palsy are summarized in Table 2. EMG characteristics Based on our previous LEMG study,6 the involved nerve impairments were grouped into complete and incomplete injuries. The EMG characteristics of incomplete impairments included reduced MUP amplitudes without abnormal MUP patterns or spontaneous electrical activity, mixed or pathological interference recruitment patterns with decreased amplitudes, and abnormal Eps of the target muscles (ie, delayed latency, prolonged duration, or decreased amplitude). The EMG characteristics of the complete impairments included denervation potential patterns (ie, electrical silence, fibrillation potentials, or positive sharp waves) or regeneration potential, mixed or simple recruitment patterns, and the absence of Eps in the target muscles. The general and evoked electromyography parameters of the SCM, TRA, and genioglossus muscles are listed in Tables 3 and 4. The fibrillation potentials or positive sharp waves can be observed in 7 patients with the course of 20 days to 2 months. The denervation potentials gradually reduce with the time. The regeneration potential of laryngeal muscles and SCM can be first seen in the patient with duration of 2 months. And most patients (14 patients) with regeneration potential had the duration of more than 6 months. The EMG patterns were showed in Figure 1. Among the 26 patients who underwent EMG tests, all (100%) exhibited the vagus nerve and the accessory nerve involvement, and 13 patients (50%) also exhibited hypoglossal nerve involvement. All of the patients with accessory nerve impairments exhibited both SCM and TRA muscle involvement. The synkinesia was only seen in the PCA muscles, in which the vagus nerves
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Characteristics of UVFP with Lower Cranial Nerve Injury
TABLE 2. Clinical Characteristics of Patients with Lower Cranial Nerve Palsy Group Characteristics Duration (months) Median (Range) Impaired side Left Right Neurologic involvement Vagus nerve Accessory nerve Hypoglossal nerve
n = 31
Cranial or Cervical Lesions (n = 12)
Cranial Neuritis (n = 4)
Radiation Induced (n = 2)
Idiopathic (n = 13)
10.5 (0.67–456)
18 (1–108)
7 (0.67–360)
– (1–54)
1.5 (1–456)
14 17
3 9
3 1
1 1
8 5
31 29 13
12 12 8
4 4 2
2 1 1
13 12 2
were completely injured. The EMG characteristics of the involved lower cranial nerves are presented in Figure 2. Among the 10 patients with intracranial or skull-base lesions, the majority (8 patients; 80%) exhibited complete impairments of both the vagus and accessory nerves, and 6 patients (60%) exhibited hypoglossal nerve complete impairment. The laryngeal synkinesia (PCA muscles) can be found in 8 patients (80%). Among the 10 patients with idiopathic lower cranial nerve palsy without any cause, incomplete impairments were observed in the majority (100% of the vagus nerves and 60% of the accessory nerves). The hypoglossal nerves were normal or exhibited incomplete impairment (60% and 20%, respectively). The four patients with atypical physical signs were all in this group and demonstrated the vagus nerve and accessory nerve incomplete injury. The laryngeal synkinesia (PCA muscles) can be found in two patients (20%). Among the four patients with lower cranial neuritis who were diagnosed by the neurologist, the nerve impairments were relatively more frequent in the accessory nerve (three patients were
completely impaired) than the vagus nerve (one patient were completely impaired). The hypoglossal nerves appeared normal or exhibited incomplete impairments (50% each). One patient with an acute stage in the duration of 20 days received the antiviral and nerve nutritional therapy for 1 month. Three months later, the patient undertook the re-EMG tests and showed that the fibrillation potentials disappeared, and the EMG signals were nearly normal. The laryngeal synkinesia (PCA muscles) can be found only in one patient. In one patient with a history of radiotherapy due to a malignant tumor in the right tonsil 28 years prior, the right vagus nerve and the accessory nerve were both completely impaired, but the hypoglossal nerve was not involved. In another patient with a history of radiotherapy due to a malignant tumor of the left parotid gland 2 years prior, the left vagus nerve was completely impaired, whereas the accessory nerve and the hypoglossal nerve were both incompletely impaired. Myokymic discharges and laryngeal synkinesia (PCA muscles) were observed in both of these patients.
TABLE 3. Nuchal Electromyography Parameters Nerves The vagus nerve
The accessory nerve
The hypoglossal nerve
Muscles Thyroarytenoid muscles Cricothyroid muscles Posterior cricoaryntenoid muscles Sternocleidomastoid muscles Trapezius muscles Genioglossus muscles
Groups
No. of Cases
Amplitude (μV)
Duration (ms)
Maximum Amplitude (μV)
Nerve impaired Normal Nerve impaired Normal Nerve impaired Normal
26 26 26 26 26 26
132.6 ± 69.3* 194.8 ± 99.0 158.5 ± 185.7 183.4 ± 93.7 141.7 ± 118.5** 234.6 ± 90.7
3.8 ± 1.6 4.0 ± 1.0 4.4 ± 1.5 3.9 ± 1.0 5.5 ± 5.7 4.2 ± 0.9
261.2 ± 172.1** 1618.0 ± 187.4 313.2 ± 154.8** 1208.0 ± 412.2 316.7 ± 260.2 1383.3 ± 541.9**
Nerve impaired Normal Nerve impaired Normal Nerve impaired Normal
26 26 26 26 13 26
121.7 ± 82.0 198.0 ± 121.0 103.1 ± 62.4* 201.7 ± 133.3 153.0 ± 79.1* 202.0 ± 59.5
3.9 ± 1.5 4.0 ± 1.1 4.3 ± 2.1 4.0 ± 1.2 4.9 ± 1.2 3.9 ± 0.7
368.6 ± 352.8** 1031.7 ± 771.0 418.2 ± 380.0* 1052.1 ± 795.0 713.1 ± 662.6** 1195.8 ± 336.8
Note: Data are mean ± standard deviation. * Compared with normal subjects, P < 0.05. **Compared with normal subjects, P < 0.01.
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TABLE 4. Evoked Nuchal Electromyography Parameters Nerves The vagus nerve
Muscles
Groups
No. of Cases
Latent Period (ms)
Duration (ms)
Amplitude (mv)
Thyroarytenoid muscles
Completely impaired Incompletely impaired Normal Completely impaired Incompletely impaired Normal Completely impaired Incompletely impaired Normal Completely impaired Incompletely impaired Normal Completely impaired Incompletely impaired Normal Completely impaired Incompletely impaired Normal
17 9 26 17 9 26 17 9 26 11 15 26 11 15 26 5 8 26
– 1.9 ± 0.2* 1.6 ± 0.3 – 1.8 ± 0.2** 1.6 ± 0.1 – 2.6 ± 0.8** 1.6 ± 0.1 – 4.4 ± 1.2** 2.0 ± 0.5 – 4.5 ± 1.3** 1.4 ± 1.0 – 2.8 ± 1.1** 1.7 ± 0.4
– 8.3 ± 3.5** 6.1 ± 0.9 – 7.3 ± 2.4 6.2 ± 1.2 – 12.0 ± 3.8** 6.0 ± 1.2 – 10.8 ± 6.1** 7.1 ± 1.9 – 11.2 ± 4.8** 5.1 ± 4.6 – 9.3 ± 2.5** 5.7 ± 1.4
– 1.1 ± 0.6** 8.6 ± 4.5 – 3.1 ± 1.7** 8.1 ± 3.4 – 2.0 ± 1.7** 6.4 ± 2.9 – 2.0 ± 0.8** 8.7 ± 8.8 – 1.6 ± 0.7** 7.2 ± 1.5 – 3.6 ± 1.8** 10.4 ± 5.4
Cricothyroid muscles
Posterior cricoaryntenoid muscles The accessory nerve
Sternocleidomastoid muscles Trapezius muscles
The hypoglossal nerve
Genioglossal muscles
Note: Data are mean ± standard deviation. * Compared with normal subjects, P < 0.05. **Compared with normal subjects, P < 0.01.
FIGURE 1. The EMG patterns of patients with an acute and a chronic duration. (A1~A5) One patient with idiopathic lower cranial nerve injury with the duration of 1 month showed the fibrillation potentials in the TA, TRA, and genioglossus muscles, and the positive sharp waves in the PCA and SCM muscles. (B1~B4) One patient with lower cranial nerve injury due to the jugular foramen schwannoma with the duration of 2 years showed the regeneration potentials in the CT, TA, SCM, and TRA muscles. CT, cricothyroid; EMG, electromyogram; PCA, posterior cricoarytenoid; SCM, sternocleidomastoid muscle; TA, thyroarytenoid; TRA, trapezius muscle.
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Characteristics of UVFP with Lower Cranial Nerve Injury
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FIGURE 2. The EMG characteristics of nerve impairment. EMG, electromyogram; IC, intracranial or skull-base lesions; ID, idiopathic; LCN, lower cranial neuritis; RA, radiation induced.
DISCUSSION Lesions affecting the recurrent laryngeal nerve in the cervicothoracic region are easier to detect during routine examinations that include ultrasound of the thyroid gland, chest X-ray, and upper gastrointestinal radiography. However, some cases of UVFP due to intracranial or skull-base lesions with combined lower cranial nerve palsy may easily be missed or misdiagnosed as “idiopathic” or “sole” recurrent nerve injury by otolaryngologists due to insidious onset, long duration, and hidden lesions. Among our consecutive series of 368 idiopathic UVFP patients acquired over 5 years, 8.4% exhibited combined lower cranial nerve palsy. The most common cause was idiopathic (13 patients, 41.9%), followed in order of decreasing frequency by intracranial or skull-base lesions (12 patients, 38.7%), infectious lower cranial neuritis (4 patients, 12.9%), and radiotherapy (2 patients, 6.5%). Abnormal physical signs of the lower cranial nerves can actually be readily observed; these signs include asymmetry of the uvula and palate (vagus nerve palsy), excursion of the tongue to the affected side during protrusion and atrophy of tongue muscles (hypoglossal nerve palsy), and atrophy of the SCM and TRA (accessory nerve palsy). Among our 368 consecutive patients who were initially diagnosed with idiopathic UVFP, 31 patients (8.4%) were eventually diagnosed with lower cranial nerve palsy with abnormal physical signs of the lower cranial nerves and EMG tests. Regular physical examinations of the lower cranial nerves are preliminary screenings for idiopathic UVFP patients, which are necessary to exclude other cranial nerve injuries. For the patients with suspicious or abnormal physical and EMG signs of the lower cranial nerves, magnetic resonance imaging (MRI) or computed tomography (CT) scans of the skull and neck are essential to exclude cranial or cervical lesions. In our study, 12 of 31 patients (38.7%) had abnormal radiologic findings that included jugular foramen region lesions (50%), parapharyngeal space tumors (16.7%), vertebral artery aneurysms (8.3%), brainstem neoplasms (8.3%), cerebellopontine angle tumors (8.3%), and medulla oblongata infarctions (8.3%). The most common
location in our study was jugular foramen region; these lesions always affect the cranial nerves IX, X, and XI. For the patients with suspicious lower cranial nerve involvement who had the atypical history and physical examination making a definite diagnosis, EMG tests helped to clarify the diagnosis. In this study, four patients could not be defined only by history and physical examination. But EMG revealed that the lower cranial nerve had incomplete neuropathic injuries. So, the EMG tests were also strongly recommended to investigate the nerve injured and its severity. According to our EMG tests, all the vagus nerves were involved and showed severe injury. Among the other lower cranial nerves, the accessory nerve was the most vulnerable as indicated by its relatively more severe impairment, and the hypoglossal nerve was relatively mildly impaired. The EMG test has been used to confirm peripheral nerve impairment and subsequently to determine the degree of injury and predict the prognosis. The spontaneous potentials and waveform morphologies on EMG can be utilized as qualitative diagnostic indicators of nerve injury.8–10 Our EMG results also revealed that although all of the affected vocal folds were completely fixed, the severity of combined lower cranial nerve injuries were varied in different causes. Two patients (20%) with intracranial or skull-base lesions exhibited incomplete lower cranial nerve injuries, which may have been due to early detections and short disease durations. The other eight patients (80%) with neoplasms exhibited the most severe degree of injury that included complete impairments of the vagus combined with the accessory nerves on EMG. This finding may have been to the gradual development and longer durations (median 18 months) of these intracranial lesions, which would lead to consistent and progressive damage to the affected nerve and worse prognoses. Thus, we considered that for the patients with the occupying lesions, nerves damage was more serious and gradually increased with the extension of the course. The majority of the patients with lower cranial neuritis and idiopathic factors always presented with incomplete nerve injuries, particularly in the vagus nerve, but showed more severe injury
ARTICLE IN PRESS 6 in accessory nerve. These conditions primarily caused incomplete impairments and may require active treatment as soon as possible. The nerve function may be restored after the treatment. In our study, one patient of lower cranial neuritis with incomplete nerve injury received antiviral and nerve nutritional therapy 20 days after onset for 1 month, and recovered generally normal EMG signals 3 months later, which indicates that the outcome of some incomplete nerve injuries may be better. So, the EMG also can predict the prognosis, but further follow up is still needed. Radiation treatments in the head and neck region can cause delayed injuries to the lower cranial nerves that often occur 5–8 years after radiotherapy.11–13 In our study, radiation-induced impairment of the vagus nerve and accessory nerve was always complete, and the hypoglossal nerve was the least extensive; these impairments occurred 2 and 28 years after radiotherapy. Abnormal spontaneous electrical activities characteristic of radiationinduced peripheral neuropathy,12 such as myokymic discharges, were also observed. Our study also found that the EMG characteristics of lower cranial nerve injury were similar to that of laryngeal nerve injury. In the early stage of the injury, the spontaneous potentials were mainly denervation potential patterns, whereas in the chronic stage, the spontaneous potentials were mainly regeneration potential patterns. The synkinesia was only seen in the PCA muscles, whose vagus nerve showed complete injury, which indicated that the synkinesia may reflect the severity of nerve injury. In addition, we found that there were no synkinesia observed in SCM and TRA muscles. This may be because there were plentiful traffic branches between the accessory nerve and the cervical plexus. After the accessory nerve injury, some motor branches of cervical plexus can replace parts of the accessory nerve function. So, the accessory nerves may not have the fault regeneration of nerve fibers. In genioglossus muscles, the synkinesia was not found either, which may be due to the incomplete hypoglossal nerve injury in our study. Our study still needs further research with large sample. CONCLUSIONS Among all of the patients in our study, 8.4% with “idiopathic” UVFP also exhibited injuries in the other lower cranial nerves. The most common cause was idiopathic (41.9%), followed by intracranial or skull-base lesions (38.7%), infectious lower cranial neuritis (12.9%), and radiotherapy (6.5%). The most common location of skull-base lesion in our study was the jugular foramen region. For the patients with atypical history and physical examination, EMG tests were strongly recommended to identify
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whether there is suspicious lower cranial nerve involvement. Based on the physical examinations and EMG, the vagus and accessory nerves were the most vulnerable to injury, followed by the hypoglossal nerve. Due to insidious onset and long duration, these conditions may be easy to be missed or misdiagnosed as “idiopathic” or “sole” vocal fold paralysis. The lower cranial nerve impairments caused by intracranial or skull-base lesions and radiation are generally complete and have poor prognoses. Lower cranial neuritis and idiopathic conditions predominately lead to incomplete impairments, and active treatment should be applied as early as possible to achieve good prognoses. Therefore, for the patients with clinically “idiopathic” vocal fold immobility, head, neck, and lower cranial nerve examinations, cranial radiology, and especially EMG tests should be performed to identify other lower cranial nerve injuries and their severities. REFERENCES 1. Hayward D, Morgan C, Emami B, et al. Jugular foramen syndrome as initial presentation of metastatic lung cancer. J Neurol Surg Rep. 2012;73:14–18. 2. Al-Khayat H, Beshay J, Manner D, et al. Vertebral artery-posteroinferior cerebellar artery aneurysms: clinical and lower cranial nerve outcomes in 52 patients. Neurosurgery. 2005;56:2–10. 3. Lv X, Jiang C, Li Y, et al. Clinical outcomes of lower cranial nerve palsies caused by vertebral artery-posteroinferior cerebellar artery aneurysms after endovascular embolization. Neurol Res. 2010;32:796–800. 4. Dqbrowska A, Jałowin´ski R, Tarnowska C, et al. Paralysis of vocal fold as the first symptom of Vernet’s syndrome in the course of jugular chemodectoma. Otolaryngol Pol. 2006;60:773–777. 5. Lo Casto A, Spataro R, Purpura P, et al. Unilateral laryngeal and hypoglossal paralysis (Tapia’s syndrome) in a patient with an inflammatory pseudotumor of the neck. Clin Neurol Neurosurg. 2013;115:1499–1501. 6. Xu W, Han D, Hou L, et al. Value of Laryngeal electromyography in diagnosis of vocal fold immobility. Ann Otol Rhinol Laryngol. 2007;116:576–581. 7. Xu W, Han D, Hou L, et al. Clinical and electrophysiological characteristics of larynx in myasthenia gravis. Ann Otol Rhinol Laryngol. 2009;118:656– 661. 8. Xu W, Han D, Hu R, et al. Characteristics of vocal fold immobility following endotracheal intubation. Ann Otol Rhinol Laryngol. 2012;121:689–694. 9. Simpson DM, Sternman D, Graves-Wright J, et al. Vocal cord paralysis: clinical and electrophysiologic features. Muscle Nerve. 1993;16:952–957. 10. Kupfer RA, Old MO, Oh SS, et al. Spontaneous laryngeal reinnervation following chronic recurrent laryngeal nerve injury. Laryngoscope. 2013;123:2216–2227. 11. Lin YS, Jen YM, Lin JC. Radiation-related cranial nerve palsy in patients with nasopharyngeal carcinoma. Cancer. 2002;95:404–409. 12. Shin HY, Park HJ, Choi YC, et al. Clinical and electromyographic features of radiation-induced lower cranial neuropathy. Clin Neurophysiol. 2013;124:598–602. 13. Hsieh YL, Chang MH, Wang CC. Laryngeal electromyography findings of vocal fold immobility in patients after radiotherapy for nasopharyngeal carcinoma. Head Neck. 2014;36:867–872.