Hayoung Byun, MD; Yang-Sun Cho, MD, PhD; Jeon Yeob Jang, MD; Kyu Whan Chung, MD; Soojin Hwang, BA; Won-Ho Chung, MD, PhD; Sung Hwa Hong, MD, PhD

Transcription

1 The Laryngoscope VC 2013 The American Laryngological, Rhinological and Otological Society, Inc. Value of Electroneurography as a Prognostic Indicator for Recovery in Acute Severe Inflammatory Facial Paralysis: A Prospective Study of Bell s Palsy and Ramsay Hunt Syndrome Hayoung Byun, MD; Yang-Sun Cho, MD, PhD; Jeon Yeob Jang, MD; Kyu Whan Chung, MD; Soojin Hwang, BA; Won-Ho Chung, MD, PhD; Sung Hwa Hong, MD, PhD Objectives/Hypothesis: To evaluate the prognostic and predictive value of electroneuronography (ENoG) in acute severe inflammatory facial paralysis, including Bell s and Ramsay Hunt syndrome (RHS). Study Design: Prospective observational study. Methods: Patients with acute severe facial paralysis of House-Brackmann (H-B) grade IV or worse and diagnosed with Bell s or RHS were enrolled from August 2007 to July After treatment with oral corticosteroid, antiviral agent, and protective eye care, patients were followed up until recovery or 12 months from onset. Results: Sixty-six patients with Bell s and 22 with RHS were included. Multiple logistic regression analysis showed significant effect of ENoG value on recovery in both Bell s and RHS. Values of ENoG were significantly worse in RHS than Bell s. Chance of early recovery within 6 weeks after correction of ENoG effect was still significantly worse in RHS. Logistic regression analysis showed 90% chance of recovery within 6 months, expected with ENoG values of 69.2% degeneration (Bell s ) and 59.3% (RHS). The receiver operating characteristics (ROC) curves showed ENoG values of 82.5% (Bell s ) and 78.0% (RHS) as a critical cutoff value of nonrecovery until 1 year, with the best sensitivity and specificity. Conclusions: A higher chance of recovery was expected with better ENoG in Bell s and RHS. Based on our data, nonrecovery is predicted in patients with ENoG value greater than 82.5% in Bell s, and 78% in RHS. Key Words: Acute facial paralysis, electroneurography, Bell s, Ramsay Hunt Syndrome, logistic regression, Kaplan- Meier survival analysis, receiver operating characteristics. Level of Evidence: 4. Laryngoscope, 123: , 2013 INTRODUCTION Facial electroneurography (ENoG) is the objective electrophysiologic measurement of a muscle compound action potential used to assess nerve degeneration. Since the technique was developed and introduced into otolaryngology by Esslen 1 and Fisch, 2 a number of studies to evaluate the prognostic value of ENoG have been reported. May and colleagues 3 showed that ENoG amplitude reductions to less than 10% of the unaffected side were highly associated with incomplete recovery. Fisch 4 reported that patients reaching 95% degeneration within From the Department of Otorhinolaryngology Head and Neck Surgery (H.B., Y-S.C., J.Y.J., S.H., W-H.C., S.H.H.), Sungkyunkwan University School of Medicine, Samsung Medical Center, Seoul; and the Department of Otolaryngology Head and Neck Surgery (K.W.C.), Inje University College of Medicine, Haeundae Paik Hospital, Busan, Korea. Editor s Note: This Manuscript was accepted for publication December 18, Presented at the 28th Politzer Society Meeting, Athens, Greece, Sep 28 Oct 1, This work was supported by grant from the Strategic Technology Development Program of Ministry of Knowledge Economy ( ), and grant of Seoul R&D Program (SS100022). The authors have no other funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Yang-Sun Cho, MD, PhD, Department of Otorhinolaryngology Head and Neck Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, 50 Ilwon-Dong, Gangnam-Gu, Seoul , South Korea. yscho@skku.edu DOI: /lary weeks had a 50% chance of a poor recovery. Gantz et al. 5 showed that subjects who did not reach 90% degeneration on ENoG within 14 days of paralysis returned to House-Brackmann (H-B) grade I or II at 7 months after onset of the paralysis. In terms of threshold criteria, although the end point of denervation reaching 95% is reported to be the most reliable prognostic sign of nonrecovery, it is too late for surgical decompression if one expects the maximal denervation to occur. 6 Although cutoff ENoG value of 90% degeneration within 14 days has been commonly accepted for the surgical intervention, other values can also be considered a critical prognostic point. Chow et al. 7 reported that ENoG degeneration less than 72.63% implied a greater than 90% chance of recovery in Bell s. Recent report by Takemoto et al. 8 showed that more than 85% degeneration on ENoG had the highest specificity and sensitivity to predict nonrecovery when the patients with Bell s and Ramsay Hunt syndrome (RHS) were analyzed together. According to their prospective data, recovery rate of patients with ENoG values of 80% to 85% and 85% to 90% were 83.3% and 36.4%, respectively. Fisch 6 reported that 12% of patients with 80% to 89% degeneration showed unsatisfactory recovery, and May et al. 9 showed that 16% of patients with 76% to 89% of degeneration had an unsatisfactory result in Bell s. On the other hand, there 2526

2 are several studies which did not show any predictive role of ENoG in acute facial paralysis. Canter and associates 10 could find no association of final outcome with ENoG in complete paralysis. Lee and colleagues 11 showed that ENoG does not provide accurate information on the prognosis or recovery rate of the acute facial paralysis. Although RHS is the second most common inflammatory cause of acute facial paralysis, generally showing more severe symptoms and a poor outcome, previous literature mostly focused on prognostic value of ENoG in Bell s, or analyzed patients with Bell s or RHS together. In addition, previous studies included patients with facial of various severities from mild to complete, which may have distorted the prognostic value of ENoG for severe facial paralysis. As the prognosis of incomplete is usually excellent, predicting the outcome of complete is clinically more demanding. The purpose of this study was to evaluate the prognostic and predictive value of ENoG in acute severe peripheral facial paralysis focused on Bell s and RHS separately. A prospective study was designed to assess the recovery outcome of severely paralyzed patients who underwent uniform evaluation and treatment. MATERIALS AND METHODS Patients Patients complaining of acute facial weakness and diagnosed with Bell s or RHS were invited to enroll in the outpatient clinic of the Department of Otorhinolaryngology Head and Neck Surgery in Samsung Medical Center, Seoul, South Korea, from August 2007 to July Among subjects with severe facial paralysis of initial H-B grade IV (incomplete eye closure with effort) or worse, patients who presented to the clinic within the first 10 days from the onset and complied with our treatment protocol were included. Diagnosis of Bell s was made when no other cause of facial paralysis could be identified by clinical tests. RHS was diagnosed in patients with acute peripheral facial paralysis and typical clinical findings of herpes zoster oticus, including skin vesicles. Any patient who got another treatment earlier for the same episode was excluded from the study. Subjects with central nervous system disorder or other causes of facial paralysis, such as trauma, tumor, or iatrogenic event, were also excluded. Treatment & Follow-Up Protocol All patients who meet the inclusion criteria were treated with oral corticosteroid (1 mg/kg/day for 7 days, followed by 4 days of tapering), oral antiviral agent (acyclovir or famciclovir for 1 week), and protective eye care (artificial eye drop, ointment, taping of paralyzed eyelid during nights, and education of patients). Basic medical information was obtained, including concurrent traditional therapy (acupuncture, herb medicine) and related hearing loss or dizziness. ENoG was performed between 5 and 14 days from the onset of facial weakness using Nicolet Viking Select (Madison, WI) by a single highly experienced examiner. After skin preparation, the electrodes were placed with optimized lead placement (OLP) technique. 1,6 The reference electrodes and recording electrodes for orbicularis oculi and orbicularis oris were placed at just above and below the orbital rim and just lateral to the nasolabial fold, respectively. The ground electrode was placed at left distal arm. The stimulating electrodes were applied at the stylomastoid foramen area of the unaffected side first, with a starting current of 10 ma, increasing by 10 ma to maximal peak up to 80 ma, with 0.1msec duration of stimulus (resistance 5000X). The results were interpreted by peak-topeak methods and reported as percentage (%) of degeneration of affected side compared to unaffected side. The mean value of two subsites, orbicularis oculi and oris, was used in the analysis. Facial movement was described using H-B facial grading system 12 and also documented by photo images. All H-B grades of enrolled subjects were carefully reviewed by blinded two senior otolaryngologists to minimize bias in grading. The completion of follow-up was made at 12 months from the onset of facial paralysis, or by recovery defined as H-B grade I or II. This study was approved by the Institutional Review Board at the Samsung Medical Center in accordance with the Declaration of Helsinki. Statistical Analysis Data were analyzed with the use of IBM SPSS Statistics, version 19.0 (IBM Corp., NY). The comparison of demographic data between Bell s and RHS was performed by the chisquare test or two-tailed Mann-Whitney U test at an alpha level of 5%. To assess the correlation between independent variables, Spearman s correlation analysis was used. Comparison of two categorical variables was conducted by Fisher s exact test (2- sided). Multiple logistic regression analysis was used to evaluate the effect of possible prognostic indicators on recovery at each follow-up point. Kaplan-Meier survival analysis with log-rank significance test was performed to plot and compare the cumulative recovery rate of Bell s and RHS. P values of less than 0.05 were considered to indicate statistical significance. To assess the cutoff ENoG value, scatter dot plots and receiver operating characteristic (ROC) curves were drawn by Prism Software, version 5.0 (GraphPad Software, San Diego, CA). RESULTS Demographics Among 81 BP and 28 RHS patients who were initially enrolled, a total of 88 patients including 66 Bell s and 22 RHS subjects completed this study. There was no significant difference of baseline characteristics between two etiologic groups except the value of ENoG, which was worse in RHS than Bell s (p by 2-tailed Mann-Whitney test) (Table I). Bell s Palsy The majority of patients showed favorable outcome, with 65 of 66 subjects recovering within 1 year from onset. One nonrecovery patient whose ENoG value was 83% had reached H-B grade III in 6 months and stayed (Table II, Fig. 1A). Logistic regression analysis was conducted to evaluate the effect of possible prognostic factors on recovery at each follow-up point. Significant predictive indicators of early recovery within 6 weeks were ENoG value (p50.002) and age group (under 65 versus over) (p50.014) (R ). ENoG value was the only 2527

3 TABLE I. Demographics of Bell s Palsy and Ramsay Hunt Syndrome Patients. Characteristic Bell s Palsy (N566) RHS * (N522) P Value Age (yr) Median (Mean6SD) 51 (5162.3) 55 (4664.4) Range Sex (M : F) 44 : : Affected side (right : left) 37 : 29 8: Initial H-B grade: no (%) IV 28 (42.4) 5 (22.7) V 30 (45.5) 11 (50.0) VI 8 (12.1) 6 (27.3) Days from onset to treatment start Median 2 3 Range Days from the onset to ENoG test Median 7 8 Range Value of ENoG: degeneration (%) Median Range Traditional treatment: no. (%) Any concurrent 18 (27.3) 10 (45.5) therapy None 48 (72.7) 12 (55.5) *RHS5Ramsay Hunt syndrome P values were calculated with the use of the chi-square test or twotailed Mann-Whitney U test. significant indicator of recovery within 3 months (p50.031; R ) and 6 months (p50.043; R ) (Fig. 2A). Other variables such as sex, concurrent traditional treatment, days from the onset to treatment start, and initial H-B grade were not associated with recovery. Patient TABLE II. ENoG Values and H-B Grades of Nonrecovery Patients at 3 months. Diagnosis Sex/ Age ENoG value Initial Facial movement (H-B grade) 6 weeks 3 months 6 months 1 year No. 1 RHS F/ No. 2 RHS F/ No. 8 RHS F/ No. 13 Bell s M/ No. 21 Bell s M/ No. 35 RHS F/ No. 52 Bell s M/ No. 62 RHS F/ No. 69 RHS M/ No. 80 RHS M/ No. 82 Bell s M/ Ramsay Hunt Syndrome Eighteen (81.8%) of 22 RHS patients had recovered within 1 year from the onset. Three (cases no. 1, 8, and 62) out of four nonrecovery patients had reached H-B grade III, while one case (no. 69) had remained at H-B grade VI (Table II, Fig. 1B). The ENoG values of four nonrecovery patients were greater than 80% degeneration. Multiple logistic regression model showed a significant effect of ENoG value on recovery at each follow-up point: 6 weeks (p50.015; R ), 3 months (p50.037; R ), and 6 months (p50.048; R ) (Fig. 2B). Patient s age, sex, concurrent traditional treatment, days from the onset to treatment start, and initial H-B grade did not show statistical significance. In terms of early recovery within 6 weeks, only 10 of 22 RHS patients (45.5%) have recovered. Chance of early recovery after correction of ENoG effect was still significantly worse than Bell s (p50.028). Fig. 1. Histogram showing the distribution of ENoG values in patients with Bell s (A) and Ramsay Hunt syndrome (B). Four different filling patterns indicate the time to recovery during the follow-up. All nonrecovery patients at 12 months (filled black) had ENoG values greater than 80%. 2528

4 Fig. 2. Chance of recovery(%) of facial movement within 6 weeks, 3 months, and 6 months by logistic regression model in Bell s (A) and Ramsay Hunt syndrome (B). Ninety percent chance of recovery within 6 months could be expected in ENoG value of 69.2% in Bell s and 59.3% in RHS. There were six RHS patients with associated symptoms: three patients with related dizziness, one patient with hearing loss, and two patients with both. These related symptoms are not necessarily accompanied by worse ENoG values; and three out of them (50%) had not recovered within a year. Statistical analysis showed that patients with associated vestibulocochlear symptoms had worse recovery outcome than subjects without them (p50.05 at 6 weeks; p50.02 at 3 months; and p at 6 months by 2-tailed Fisher s exact test). Therefore, it is expected that dizziness and hearing loss possibly have a role as independent prognostic factors. Comparison of Bell s Palsy and Ramsay Hunt Syndrome In overall, sixty-three patients (71.6% of total; 80.3% of Bell s ; and 45.5% of RHS) recovered within 6 weeks from onset and 83 patients (94.3% of total; 98.5% of Bell s ; and 81.8% of RHS) within 12 months (Fig. 1). The cumulative recovery curves which account for all initially enrolled patients including lost subjects are shown in Figure 3. These curves reveal significantly poor recovery outcome in RHS than Bell s. A lower chance of early recovery was expected in patients with RHS (p50.028), older than age of 65 (p50.014), and worse ENoG value (p<0.001) (R ). According to the curves shown in Figure 2, 90% chance of recovery within 6 months is expected in patients with ENoG values of 69.2% in Bell s and 59.3% in RHS. Among 11 patients who did not recover within 3 months, three out of four cases with Bell s, and three out of seven RHS recovered within 1 year (Table II). Cutoff Value of ENoG for Predicting Nonrecovery Differences of ENoG values between recovery and nonrecovery patients were statistically significant in both Bell s and RHS (Fig. 4A, 4C). Based on the ROC curve shown in Figure 4, the best sensitivity/specificity of ENoG value to predict nonrecovery within 6 weeks were 76.9%/84.9% at ENoG value of 61.5% in Bell s and 75.0%/90.0% at ENoG 67.5% in RHS. In predicting final nonrecovery within 1 year, ENoG value of 81.5% showed best sensitivity/specificity of nearly 100%/100% in Bell s and ENoG 78.0% showed 100%/94.4% in RHS. DISCUSSION The prognosis of Bell s is excellent, especially in patients with incomplete. 13,14 Even though the prognosis of RHS is generally poor, the recovery outcome of incomplete is much better. 15 Therefore, this study focused on patients with severe facial paralysis whose recovery has more clinical importance. Facial paralysis of H-B grade IV or V was included as some Fig. 3. Cumulative percent recovery of acute severe peripheral facial paralysis by Kaplan-Meier survival analysis. These curves account for all initially enrolled patients including lost subjects. The recovery rate of Bell s was significantly better than RHS (chi-square 9.601; P by log-rank test). 2529

5 Fig. 4. Scatter dot plots showing ENoG values of recovery versus nonrecovery patients at 6 weeks and 1 year follow-up in Bell s (A) and RHS (C). Horizontal lines indicate Mean6SEM. ENoG difference between two groups were statistically significant (Bell s : P value<0.001 at 6 weeks; RHS: P value at 6 weeks; at 1 year). A receiver operating characteristic (ROC) curve showing sensitivity and specificity of ENoG value as a predictor of nonrecovery in Bell s (B) and RHS (D). Points closest to the upper left top are regions of maximal sensitivity and specificity. ENoG values of several critical points were indicated at the graphs: (B) ENoG value of 61.5% best predicted nonrecovery within 6 weeks and 81.5% within 1 year, (D) ENoG value of 67.5% within 6 weeks and 78% within 1 year. *P<0.05 by two-tailed Mann-Whitney U test. complete paralysis may be graded as H-B grade IV or V by the physician according to the skin thickness or facial appearance. Overall prognosis of acute severe peripheral facial paralysis was good, as 65 out of 66 patients (98.5%) with Bell s and 18 out of 22 (81.8%) RHS patients recovered to H-B grade I or II within 1 year from the onset. The outcomes were better than what is typically reported, especially in case of RHS. As the patients enrolled in this study were uniformly managed with steroids and antivirals within 1 week (median 3 days) from onset, they might have a better prognosis than those who were enrolled in other studies, including retrospective analysis. Other possible explanations may include host factor and clinical presentation. No obvious medically ill condition or malignancy that can cause immunocompromised status was accompanied by the enrolled patients. In addition, vesicles preceding the paralysis, which is known to be a good prognostic factor, were observed in 13 patients (59.1%), and it might contribute to the better result in this study. Regarding the 6-month outcome (95.5% of Bell s ; 72.7% of RHS recovered), 2530 there was a considerable portion of patients showing delayed improvement (Table II). Analysis showed that chance of early recovery within 6 weeks was higher in Bell s than RHS. In Bell s, greater ENoG value and age of older than 65 showed significant negative effects on outcome, while only ENoG value was significant in RHS. Finally, long-term recovery of facial movement within 1 year was significantly associated only with ENoG value, regardless of diagnosis, age group, sex, initial H-B grade, days from the onset to treatment start, and concurrent traditional treatment. Initial H-B grade had weak correlation with ENoG value (p<0.001; q ), which may explain the results from previous works considering it as a prognostic factor. 8,16 18 Regarding the traditional treatment, we recommended that patients not have any concurrent herb medicine or acupuncture treatment because of the possible adverse effect or interaction. However, as it is widely believed in Korea that traditional medicine is an effective therapy for neurologic disorder, complete control was not possible. Recovery outcome of patients who received any concurrent traditional treatment was not

6 different than the others. Fisher s exact test showed significantly worse recovery outcome in RHS patients with dizziness or hearing loss, although logistic regression model did not show any significant effect on recovery, probably due to the effect of another variable and the small number of cases. ENoG values were widely distributed from 9% to 88% in this study. A patient with Bell s who met indications for surgical decompression (more than 90% degeneration on ENoG with no voluntary motor unit potential on EMG within 14 days) underwent surgical decompression and was excluded from the study. Decompression surgery of facial nerve is generally considered in patients with low recovery chance. Based on this study, the critical ENoG value to identify nonrecovery patients after 1 year was calculated to be 81.5% in Bell s and 78.0% in RHS, within 14 days from the onset. Although those values cannot precisely indicate a cutoff ENoG value, the values around 80% is lower than the generally accepted value of 90% for the indication of surgical intervention. In addition to the fact that patients had been eligible for surgery when ENoG was greater than 75% in the past, 19 previous literature showed that nonrecovery rate of the patients with 75% to 90% degeneration on ENoG was relatively high. 6,8,9 Considering the possible impact of facial sequelae on patient s life quality, 12% 6 to 64% 8 chance of nonrecovery is hardly acceptable. Therefore, if a surgical team is qualified enough to minimize surgeryrelated complication, decompression surgery for patients with ENoG values between 80% and 90% should be considered carefully to improve final facial outcome in case with Bell s. The surgical decompression for RHS is often no longer recommended for its lack of evidence. 20 Regarding the test accuracy, inter-test variability of ENoG and techniques to reduce test errors have been described in many publications. Fisch 21 and Esslen 1 reported less than 10% variability, on condition that the tests were performed by a trained technician, and test-retest variability of 11.2% was reported in a prospective study by Hughes et al. 22 Attempts to standardize ENoG procedure have been introduced, including the lead placement methods, 1,22,23 submaximal nerve stimulation, adjustment of skin resistance, 24 and stimulation methods. 25 Although inter-test variability could not be completely excluded in this study, standardized test procedures in our clinic by a single highly experienced examiner provided results as consistent as possible. During the study period, 130 BP and 35 RHS patients with severe facial paralysis visited our clinic. Eighty-one (62.3%) BP and 28 (80%) RHS cases satisfied the inclusion criteria. Rates of loss to follow-up were 15/ 81 (18.5%) in BP and 6/28 (21.4%) in RHS. There was no significant difference in ENoG values or other potential prognostic variables in those who complete the study compared to those who were lost to follow-up. As treatment regimen was concentrated in the early period of facial paralysis, some patients may have showed low compliance to regular visits after medication. It can also be assumed that patients with severe symptoms might have visited another clinic, so-called doctor shopping, which is relatively easy in Korean Health Insurance System, and subsequently lost to follow-up. Further research should verify these findings with clinical data from more patients. Regarding the recovery outcome from the patient s view, future study considering not only H-B grades but also subject discomforts with quality of life assessment as another outcome is also needed for comprehensive evaluation of recovery. CONCLUSION This study showed that ENoG value has an independent role as a significant prognostic indicator for predicting chances of recovery in acute severe facial paralysis caused by Bell s and RHS. Higher chance of recovery was expected with better ENoG results, and chance of early recovery after correction of ENoG effect was still significantly worse in RHS than in Bell s. Based on our data, nonrecovery is predicted in patients with ENoG value worse than 81.5% degeneration in Bell s and 78% in RHS. BIBLIOGRAPHY 1. Esslen E. The acute facial palsies: investigations on the localization and pathogenesis of meato-labyrinthine facial palsies. Schriftenr Neurol 1977;18: Fisch U. Facial paralysis in fractures of the petrous bone. 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7 22. Hughes GB, Josey AF, Glasscock ME, Jackson CG, Ray WA, Sismanis A. Clinical electroneurography: statistical analysis of controlled measures in twenty-two normal subjects. Laryngoscope 1981;91: Coker NJ, Fordice JO, Moore S. Correlation of the nerve excitability test and electroneurography in acute facial paralysis. Am J Otol 1992;13: Hughes GB, Nodar RH, Williams GW. Analysis of test-retest variability in facial electroneurography. Otolaryngol Head Neck Surg 1983;91: Salzer TA, Coker NJ, Wang-Bennett LT. Stimulation variables in electroneurography of the facial nerve. Arch Otolaryngol Head Neck Surg 1990;116: