Journal 7 N.vii 7

European Journal of Neurology 2010, 17: 885–889

doi:10.1111/j.1468-1331.2010.02950.x

SHORT COMMUNICATION

High-resolution ultrasound in the evaluation and prognosis of BellÕs palsy Y. L. Loa, S. Fook-Chongb, T.H. Leohc, Y. F. Danc, M. P. Leec, H. Y. Ganc and L. L. Chand a

Department of Neurology, National Neuroscience Institute, Singapore General Hospital; bDepartment of Clinical Research, Singapore

General Hospital; cDepartment of Neurology, Singapore General Hospital; and dDepartment of Diagnostic Radiology, Singapore General Hospital, Singapore, Singapore

Keywords:

Bell’s palsy, blink reflex, diagnosis, nerve conduction study, prognosis, ultrasound Received 9 October 2009 Accepted 22 December 2009

Introduction: BellÕs palsy is a commonly encountered paralysis of the facial nerve occurring worldwide. Prognosis for BellÕs palsy is good, but the proportion of patients with poor outcomes may reach 30%. Ultrasound (US) may provide a novel approach for evaluating and prognosticating BellÕs palsy, in comparison with known electrophysiological techniques. Methods: In this study, we measured the diameter of the distal facial (VII) nerve using US in patients with BellÕs palsy treated with prednisolone, in comparison with healthy controls. Blink reflex and VII nerve conduction studies were also performed. Studies were prospective and performed within 1 week of disease onset. Results: Our results have shown that diameter of the distal VII nerve is a good predictor of favorable (positive predictive value: 100%) and bad outcomes (negative predictive value: 77%) in BellÕs palsy at 3 months after clinical presentation. Furthermore, we also noted the lack of correlation of VII diameter with conventional VII nerve conduction studies (NCS) and blink reflex studies. US was superior to VII nerve conduction and blink reflex studies in outcome prediction. Conclusions: This first study utilizing US in BellÕs palsy highlights its role in outcome prediction and contributes to our understanding of recovery processes in this common neurological disorder.

BellÕs palsy is a commonly encountered paralysis of the facial nerve occurring worldwide. The etiology remains uncertain, although preceding viral infection may play a role. Prognosis for BellÕs palsy is good, but the proportion of patients with poor outcomes may reach 30%. Recently, a large multi-center trial has shown that early use of prednisolone significantly improved the chances of completely recovery [1]. Marked facial nerve enhancement in the facial canal is the characteristic MR change in BellÕs palsy [2]. However, various studies have separately documented involvement of the mastoid, [3] tympanic, [4] and pre-meatal portions [5]. Despite these observations, prognostic value of MRI remains uncertain [6]. Furthermore, MR scanning is expensive, time-consuming and necessitates the use of contrast agents. Before the advent of imaging, electrophysiological methods have been utilized to predict outcomes in BellÕs palsy. Tests employed included electromyography, facial

nerve conduction, and blink reflexes. In particular, preservation of the blink reflex and absence of spontaneous electromyographic activity were associated with good outcomes [7]. Their clinical utility has not been compared with other methods of evaluation to date. The usage of ultrasound (US) is of proven efficacy in carpal tunnel syndrome, ulnar neuropathy, and femoral neuropathy [8]. It is quick safe, painless, inexpensive and has the added capability of demonstrating structural lesions along the course of the affected nerve. We have previously demonstrated its efficacy in the localization of peroneal and radial nerve entrapment [9,10]. To our knowledge, there are no published studies detailing the use of US in BellÕs palsy. Previous experiences have been for operative workup of parotid tumors [11]. To this end, US may provide a novel approach for evaluating and prognosticating BellÕs palsy, in comparison with known electrophysiological techniques.

Methods Correspondence: Dr Y. L. Lo, Outram Road, Singapore 169608, Singapore (tel: 65 63265003; fax: 65 62203321; e-mail: [email protected]).

Ó 2010 The Author(s) Journal compilation Ó 2010 EFNS

This study was carried out prospectively after approval was obtained from our institutional review board. We

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Figure 1 Ultrasound (US) of the right (top row) and left (bottom row) VII nerve in a patient. The right VII nerve shows abnormally increased VII diameter of 0.26 cm, indicated by arrows. The left VII nerve shows a normal diameter of 0.11 cm. The flow duplex shows the facial artery related deep to the VII nerve which terminates into branches in the parotid substance. The patients had an unfavorable outcome at 3 months after clinical presentation.

included patients with acute onset of unilateral BellÕs palsy, all seen within a 1-week period from onset of symptoms. We excluded patients with diabetes mellitus, traumatic facial palsy, or other causes of polyneuropathy that may confound the diagnosis. Each patient was seen initially by an experienced neurologist who confirmed the diagnosis and classified severity according to the House-Brackmann grading of I to VI [12]. All patients were treated with prednisolone 50 mg a day for a period of 10 days [1]. Patients were followed up by the same neurologist blinded to US findings when a final grading at 3 months was obtained. US examination was conducted with a General Electric Logiq 7 Pro (GE Company, New York, USA) machine, employing a 5 to 10 MHz linear array transducer by an experienced staff. With the subject in a supine left or right lateral position, the facial nerve in the longitudinal view can be identified at the mastoid region as it emerges from the stylomastoid foramen. At this site, it is visualized to traverse anteriorly into the parotid gland substance before dividing into five branches. Using color Doppler, the facial artery can be identified deep to the facial nerve. We obtained the diameter of the facial nerve from an average diameter at the most proximal and distal visualized portions, as well as midway between these two points. The normal nerve in this plane has a relatively hyperechoic neurilemoma compared to

surrounding muscle and exhibits a linear fascicular appearance. In contrast, the abnormal facial nerve is often swollen, with loss of hyperechoic appearance and fascicular pattern. Each study was performed within the first week of clinical presentation. US images were stored and analyzed offline by a separate blinded examiner. Figure 1 shows an actual example of US examination in a patient. In addition, blink reflex studies were performed by stimulating the facial nerve at the pre-auricular region, and recordings were made at the orbicularis oculi muscles. We recorded both early (R1) and late (R2) components, and results were considered abnormal if corresponding to the pathological side showed either prolonged latency (R1: >12 ms; R2: >35 ms) or absent response. We also obtained direct facial nerve conduction studies (VII NCS) recording supramaximal compound muscle action potentials from the nasalis bilaterally. Data from patients consisting of distal latency and baseline to peak amplitude were compared with those from 25 healthy controls, as were US findings. All electrophysiological studies were performed with a Medtronic Keypoint system (Medtronic, Skovlunde, Denmark), where amplifier filter settings were 5 to 5000 Hz. Data analysis was performed using SPSS for Windows package. In healthy controls, normality of parameters was regarded as a value within two standard

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deviations from the mean. A P value of less than 0.05 was considered statistically significant.

Results We studied 37 patients (mean age: 46; range: 25–69; 18 men) and 25 healthy controls (mean age: 45; range: 24–71; 9 men) whose normal values are depicted in Table 1. Table 2 summarizes results in all patients. Abnormalities in US diameter were 35% compared with VII NCS latency (32%), VII NCS amplitude (46%), and blink reflex (73%). No significant correlations were found for severity grading at examination with US diameter, VII latency, amplitude, or blink reflex findings. Neither was there significant correlation of US diameter with VII latency, amplitude, or blink reflex findings (PearsonÕs correlation, P > 0.05 all). We did not find any significant correlation of initial severity grading with patients with abnormal US diameter (r = 0.32, P = 0.29), VII latency (r = 0.05, P = 0.88), and VII amplitude (r = 0.33, P = 0.19). Using logistic regression, we did not find any significant correlation of timing (mean: 5.14 days, standard deviation: 1.69 days, range: 2–7 days) with US examination (P = 0.46), VII latency (P = 0.94), VII amplitude (P = 0.36), or blink reflex (P = 0.1) with outcome prediction. For cases with poor outcome, similar negative findings were obtained (P = 0.33) with US examination. Overall, 27 of the 37 patients (73%) had good recovery (Grade I) at 3 months. Chi-squared tests were utilized to test the association of clinical grade outcomes with US, VII latency, VII amplitude, and blink reflex. US was highly correlated with clinical grade outcomes (v2 = 25.3, df = 1, Table 1 US and VII nerve conduction studies in controls Parameter

Mean

SD

Mean + or )2SD

US diameter (cm) VII latency (ms) VII amplitude (mV)

0.14 2.95 2.39

0.02 0.33 0.74

0.18 3.61 0.91

Total number for each parameter = 50 (pool left- and right-sided values). US, ultrasound; VII, facial nerve; SD, standard deviation.

Table 2 US and VII nerve conduction studies in patients Parameter

Mean

SD

Range

US diameter (cm) VII latency (ms) VII amplitude (mV)

0.17 3.22 1.63

0.2 0.6 0.84

0.09 to 0.35 2 to 5.1 0.2 to 3.8

US, ultrasound; VII, facial nerve; SD, standard deviation.

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P < 0.0005). Normal US accurately predicted all patients (positive predictive value = 100%) having a good outcome of Grade I at 3 monthsÕ review. This was higher than the accurate prediction of good outcome of 72% for VII latency, 80% for VII amplitude, and 90% for blink reflex. Additionally, abnormal US accurately predicted for 77% (negative predictive value = 77%) of patients with poor outcome at 3 months (Grade II and above), but only 25% for VII latency, 35% for VII amplitude, and 33% for blink reflex.

Discussion Our results have shown that US diameter of the distal VII nerve is a good predictor of good and bad outcomes in BellÕs palsy at 3 months after clinical presentation. Furthermore, we also noted the lack of correlation of US diameter with conventional VII NCS and blink reflex studies. US was superior to these other electrophysiological tests in predicting good and poor recovery at 3 months. We have chosen the 3-month review period after steroid treatment so as to be in line with the largest trial of BellÕs palsy treatment to date [1]. Finally, US also suggested that distal abnormality of the nerve, if present, can be visualized early. From the superficial attachments to the brain, the two roots of the VII nerve travel forward with the acoustic nerve into the internal auditory meatus. At the bottom of the meatus, it enters the facial canal where it travels forward to exit the skull at the stylomastoid foramen. Distally, it enters the parotid substance where it divides into distinct branches. Specifically, US in our study had visualized the region between the stylomastoid foramen exit and the parotid gland. Overall, US was painless, quick, and technically easy to perform. Our experience with the blink reflex was similar to previous experiences, suggesting its high sensitivity in predicting a favorable outcome [13–15]. Contrarily, this test was much less accurate in predicting a poor outcome when performed within the first 10 days of onset [16]. This may be related to the indirect way of interpreting the blink reflex for VII neuropathy itself. Whereas the blink reflex pathway traverses the brainstem and would be ideal for screening abnormalities from the brainstem, and distally, it would not be adequately specific for addressing dysfunction involving the VII nerve alone. For VII NCS, other authors have previously utilized VII motor conduction velocity and evoked electromyography to highlight their value in prognosis [17,18]. However, theses patents were not treated with steroids, and the differences in methodology made each study not directly comparable with the present. It should be

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noted that VII NCS here have addressed compound muscle action potentials from the nasalis only and recording from additional muscles like the orbicularis would be technically more demanding. The study by Olsen [19] had compared VII amplitude of the affected and unaffected side as a predictor of outcome but suggested that prediction was more accurate for good rather than for bad outcomes. This is corroborated by our study. Notably, this study has shown that US examination performed at 2–7 days after onset was efficacious for outcome prediction, but the clinical utility beyond 7 days remains to be determined. However, in this context, early outcome prediction within the disease-onset period might prove most relevant clinically. As previously noted, MRI studies have been utilized to investigate the site of lesion in BellÕs palsy. Based on the main finding of nerve enhancement alone, abnormalities in the distal nerve segment appeared to be the less common abnormality compared to enhancement in the more proximal segments in the labyrinthine portion and geniculate ganglion [5,20]. Separately, Murphy [4] reported 10 cases of BellÕs palsy whereby enhancement of the facial nerve in the mastoid segment correlated with incomplete recovery compared with enhancement limited more proximal sites at the labyrinthine and geniculate ganglion segments. These results are corroborated by our findings using US examination of the distal facial nerve. It should also be highlighted that MRI findings are usually described as contrast enhancement rather than physical nerve swelling. Therefore, MRI may actually demonstrate vascular rather than structural changes seen with US. What are the possible reasons which can explain our findings? First, the lack of correlation of US with VII NCS and blink reflex suggests that US measurement of nerve diameter may not specifically point to demyelination or axon loss processes independently The pathophysiology of nerve swelling and thickening is complex and may involve endoneural edema, demyelination, axonal degeneration, and fibrosis [21,22]. Rather, US structural changes may be a surrogate indicator of a combination of these processes, or other yet unknown factors. Secondly, the efficacy of US in clinical outcome prediction could be explained by both anatomic and physiologic factors. It is possible that the affected and swollen distal VII segment is too distant to receive cell body nutrients in BellÕs palsy and involvement of this segment would thus delay recovery as seen in cases with poor recovery at 3 months. Additionally, even if regeneration has been complete in the un-visualized proximal nerve segments, abnormality in the visualized distal segments would impede efficient conduction to the facial muscles receiving innervation [23–26]. These

are certainly intriguing areas, and the answers may be apparent with future research. In conclusion, this is the first study utilizing US in the evaluation and prognosis of BellÕs palsy. The findings also contribute to our understanding of the recovery processes in this common neurological disorder.

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Ó 2010 The Author(s) Journal compilation Ó 2010 EFNS European Journal of Neurology 17, 885–889