Value of electroneurography as a prognostic indicator for recovery in acute severe inflammatory...

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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 acutesevere inflammatory facial paralysis, including Bell’s palsy 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 palsy or RHS were enrolled from August 2007 to July 2011. 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 palsy and 22 with RHS were included. Multiple logistic regression analysis showedsignificant effect of ENoG value on recovery in both Bell’s palsy and RHS. Values of ENoG were significantly worse in RHSthan Bell’s palsy. 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% degenera-tion (Bell’s palsy) and 59.3% (RHS). The receiver operating characteristics (ROC) curves showed ENoG values of 82.5% (Bell’spalsy) 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 palsy and RHS. Based on our data,nonrecovery is predicted in patients with ENoG value greater than 82.5% in Bell’s palsy, and 78% in RHS.

Key Words: Acute facial paralysis, electroneurography, Bell’s palsy, Ramsay Hunt Syndrome, logistic regression, Kaplan-Meier survival analysis, receiver operating characteristics.

Level of Evidence: 4.Laryngoscope, 00:000–000, 2013

INTRODUCTIONFacial electroneurography (ENoG) is the objective

electrophysiologic measurement of a muscle compoundaction potential used to assess nerve degeneration. Sincethe technique was developed and introduced into otolar-yngology by Esslen1 and Fisch,2 a number of studies toevaluate the prognostic value of ENoG have beenreported. May and colleagues3 showed that ENoG ampli-tude reductions to less than 10% of the unaffected sidewere highly associated with incomplete recovery. Fisch4

reported that patients reaching 95% degeneration within

2 weeks had a 50% chance of a poor recovery. Gantzet al.5 showed that subjects who did not reach 90%degeneration on ENoG within 14 days of paralysisreturned to House-Brackmann (H-B) grade I or II at 7months after onset of the paralysis.

In terms of threshold criteria, although the endpoint of denervation reaching 95% is reported to be themost reliable prognostic sign of nonrecovery, it is too latefor surgical decompression if one expects the maximaldenervation to occur.6 Although cutoff ENoG value of90% degeneration within 14 days has been commonlyaccepted for the surgical intervention, other values canalso be considered a critical prognostic point. Chowet al.7 reported that ENoG degeneration less than72.63% implied a greater than 90% chance of recovery inBell’s palsy. Recent report by Takemoto et al.8 showedthat more than 85% degeneration on ENoG had thehighest specificity and sensitivity to predict nonrecoverywhen the patients with Bell’s palsy and Ramsay Huntsyndrome (RHS) were analyzed together. According totheir prospective data, recovery rate of patients withENoG values of 80% to 85% and 85% to 90% were 83.3%and 36.4%, respectively. Fisch6 reported that 12% ofpatients with 80% to 89% degeneration showed unsatis-factory recovery, and May et al.9 showed that 16% ofpatients with 76% to 89% of degeneration had an unsat-isfactory result in Bell’s palsy. On the other hand, there

From the Department of Otorhinolaryngology–Head and NeckSurgery (H.B., Y-S.C., J.Y.J., S.H., W-H.C., S.H.H.), Sungkyunkwan UniversitySchool of Medicine, Samsung Medical Center, Seoul; and the Depart-ment of Otolaryngology–Head and Neck Surgery (K.W.C.), Inje UniversityCollege of Medicine, Haeundae Paik Hospital, Busan, Korea.

Editor’s Note: This Manuscript was accepted for publicationDecember 18, 2012.

Presented at the 28th Politzer Society Meeting, Athens, Greece,Sep 28–Oct 1, 2011.

This work was supported by grant from the Strategic TechnologyDevelopment Program of Ministry of Knowledge Economy (10031764),and grant of Seoul R&D Program (SS100022). The authors have no otherfunding, financial relationships, or conflicts of interest to disclose.

Send correspondence to Yang-Sun Cho, MD, PhD, Department ofOtorhinolaryngology–Head and Neck Surgery, Samsung Medical Center,Sungkyunkwan University School of Medicine, 50 Ilwon-Dong,Gangnam-Gu, Seoul 135-710, South Korea. E-mail: [email protected]

DOI: 10.1002/lary.23988

Laryngoscope 00: Month 2013 Byun et al.: ENoG in Bell’s Palsy and Ramsay Hunt Syndrome

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are several studies which did not show any predictive

role of ENoG in acute facial paralysis. Canter and asso-

ciates10 could find no association of final outcome with

ENoG in complete paralysis. Lee and colleagues11

showed that ENoG does not provide accurate informa-

tion on the prognosis or recovery rate of the acute facial

paralysis.Although RHS is the second most common inflam-

matory cause of acute facial paralysis, generally showingmore severe symptoms and a poor outcome, previous lit-erature mostly focused on prognostic value of ENoG inBell’s palsy, or analyzed patients with Bell’s palsy orRHS together. In addition, previous studies includedpatients with facial palsy of various severities from mildto complete, which may have distorted the prognosticvalue of ENoG for severe facial paralysis. As the progno-sis of incomplete palsy is usually excellent, predictingthe outcome of complete palsy is clinically moredemanding.

The purpose of this study was to evaluate the prog-nostic and predictive value of ENoG in acute severe pe-ripheral facial paralysis focused on Bell’s palsy and RHSseparately. A prospective study was designed to assessthe recovery outcome of severely paralyzed patients whounderwent uniform evaluation and treatment.

MATERIALS AND METHODS

PatientsPatients complaining of acute facial weakness and diag-

nosed with Bell’s palsy or RHS were invited to enroll in the out-patient clinic of the Department of Otorhinolaryngology–Headand Neck Surgery in Samsung Medical Center, Seoul, SouthKorea, from August 2007 to July 2011. Among subjects withsevere facial paralysis of initial H-B grade IV (incomplete eyeclosure with effort) or worse, patients who presented to theclinic within the first 10 days from the onset and complied withour treatment protocol were included. Diagnosis of Bell’s palsywas made when no other cause of facial paralysis could be iden-tified by clinical tests. RHS was diagnosed in patients withacute peripheral facial paralysis and typical clinical findings ofherpes zoster oticus, including skin vesicles. Any patient whogot another treatment earlier for the same episode wasexcluded from the study. Subjects with central nervous systemdisorder or other causes of facial paralysis, such as trauma, tu-mor, or iatrogenic event, were also excluded.

Treatment & Follow-Up ProtocolAll patients who meet the inclusion criteria were treated

with oral corticosteroid (1 mg/kg/day for 7 days, followed by 4days of tapering), oral antiviral agent (acyclovir or famciclovirfor 1 week), and protective eye care (artificial eye drop, oint-ment, taping of paralyzed eyelid during nights, and educationof patients). Basic medical information was obtained, includingconcurrent traditional therapy (acupuncture, herb medicine)and related hearing loss or dizziness.

ENoG was performed between 5 and 14 days from theonset of facial weakness using Nicolet Viking Select (Madison,WI) by a single highly experienced examiner. After skin prepa-ration, the electrodes were placed with optimized lead place-ment (OLP) technique.1,6 The reference electrodes andrecording electrodes for orbicularis oculi and orbicularis oris

were placed at just above and below the orbital rim and just lat-eral to the nasolabial fold, respectively. The ground electrodewas placed at left distal arm. The stimulating electrodes wereapplied at the stylomastoid foramen area of the unaffected sidefirst, with a starting current of 10 mA, increasing by 10 mA tomaximal peak up to 80 mA, with 0.1msec duration of stimulus(resistance 5000X). The results were interpreted by peak-to-peak methods and reported as percentage (%) of degeneration ofaffected side compared to unaffected side. The mean value oftwo subsites, orbicularis oculi and oris, was used in theanalysis.

Facial movement was described using H-B facial gradingsystem12 and also documented by photo images. All H-B gradesof enrolled subjects were carefully reviewed by blinded two sen-ior otolaryngologists to minimize bias in grading. The comple-tion of follow-up was made at 12 months from the onset offacial paralysis, or by recovery defined as H-B grade I or II.

This study was approved by the Institutional ReviewBoard at the Samsung Medical Center in accordance with theDeclaration of Helsinki.

Statistical AnalysisData were analyzed with the use of IBM SPSS Statistics,

version 19.0 (IBM Corp., NY). The comparison of demographicdata between Bell’s palsy and RHS was performed by the chi-square test or two-tailed Mann-Whitney U test at an alpha levelof 5%. To assess the correlation between independent variables,Spearman’s correlation analysis was used. Comparison of twocategorical variables was conducted by Fisher’s exact test (2-sided). Multiple logistic regression analysis was used to evaluatethe effect of possible prognostic indicators on recovery at eachfollow-up point. Kaplan-Meier survival analysis with log-ranksignificance test was performed to plot and compare the cumula-tive recovery rate of Bell’s palsy and RHS. P values of less than0.05 were considered to indicate statistical significance. Toassess the cutoff ENoG value, scatter dot plots and receiveroperating characteristic (ROC) curves were drawn by PrismSoftware, version 5.0 (GraphPad Software, San Diego, CA).

RESULTS

DemographicsAmong 81 BP and 28 RHS patients who were ini-

tially enrolled, a total of 88 patients including 66 Bell’spalsy and 22 RHS subjects completed this study. Therewas no significant difference of baseline characteristicsbetween two etiologic groups except the value of ENoG,which was worse in RHS than Bell’s palsy (p50.005 by2-tailed Mann-Whitney test) (Table I).

Bell’s PalsyThe majority of patients showed favorable outcome,

with 65 of 66 subjects recovering within 1 year fromonset. One nonrecovery patient whose ENoG value was83% had reached H-B grade III in 6 months and stayed(Table II, Fig. 1A).

Logistic regression analysis was conducted to evalu-ate the effect of possible prognostic factors on recoveryat each follow-up point. Significant predictive indicatorsof early recovery within 6 weeks were ENoG value(p50.002) and age group (under 65 versus over)(p50.014) (R250.480). ENoG value was the only


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significant indicator of recovery within 3 months(p50.031; R250.541) and 6 months (p50.043;R250.531) (Fig. 2A). Other variables such as sex, con-current traditional treatment, days from the onset totreatment start, and initial H-B grade were not associ-ated with recovery.

Ramsay Hunt SyndromeEighteen (81.8%) of 22 RHS patients had recovered

within 1 year from the onset. Three (cases no. 1, 8, and62) out of four nonrecovery patients had reached H-Bgrade III, while one case (no. 69) had remained at H-Bgrade VI (Table II, Fig. 1B). The ENoG values of four non-recovery patients were greater than 80% degeneration.

Multiple logistic regression model showed a signifi-cant effect of ENoG value on recovery at each follow-uppoint: 6 weeks (p50.015; R250.480), 3 months (p50.037;R250.555), and 6 months (p50.048; R250.500) (Fig. 2B).Patient’s age, sex, concurrent traditional treatment, daysfrom the onset to treatment start, and initial H-B gradedid not show statistical significance.

In terms of early recovery within 6 weeks, only 10of 22 RHS patients (45.5%) have recovered. Chance ofearly recovery after correction of ENoG effect was stillsignificantly worse than Bell’s palsy (p50.028).

TABLE I.Demographics of Bell’s Palsy and Ramsay Hunt Syndrome

Patients.

CharacteristicBell’s

Palsy (N566)RHS*

(N522) P Value†

Age (yr) 0.415

Median (Mean6SD) 51 (5162.3) 55 (4664.4)

Range 15–84 11–82

Sex (M : F) 44 : 22 12 : 10 0.306

Affected side (right : left) 37 : 29 8: 14 0.109

Initial H-B grade: no (%) 0.125

IV 28 (42.4) 5 (22.7)

V 30 (45.5) 11 (50.0)

VI 8 (12.1) 6 (27.3)

Days from onset totreatment start

0.130

Median 2 3

Range 0–7 0–10

Days from the onset toENoG test

0.276

Median 7 8

Range 5–14 5–13

Value of ENoG:degeneration (%)

0.005

Median 44 64

Range 9–83 22–88

Traditional treatment:no. (%)

0.113

Any concurrenttherapy

18 (27.3) 10 (45.5)

None 48 (72.7) 12 (55.5)

*RHS5Ramsay Hunt syndrome†P values were calculated with the use of the chi-square test or two-

tailed Mann-Whitney U test.

TABLE II.ENoG Values and H-B Grades of Nonrecovery Patients

at 3 months.

Patient DiagnosisSex/Age

ENoGvalue

Facial movement (H-B grade)

Initial6

weeks3

months6

months1

year

No. 1 RHS F/60 81 6 5 5 4 3

No. 2 RHS F/58 82 6 6 4 3 2

No. 8 RHS F/52 88 5 5 4 3 3

No. 13 Bell’spalsy

M/24 80 6 6 4 4 2


M/72 62 5 5 5 3 2

No. 35 RHS F/39 49 5 5 5 3 2


M/44 83 6 5 5 3 3

No. 62 RHS F/67 84 6 6 6 5 3

No. 69 RHS M/67 82 6 6 6 6 6

No. 80 RHS M/82 75 5 4 4 3 2


M/56 72 6 6 3 2 2

Fig. 1. Histogram showing the distribution of ENoG values in patients with Bell’s palsy (A) and Ramsay Hunt syndrome (B). Four differentfilling patterns indicate the time to recovery during the follow-up. All nonrecovery patients at 12 months (filled black) had ENoG valuesgreater than 80%.


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There were six RHS patients with associated symp-toms: three patients with related dizziness, one patientwith hearing loss, and two patients with both. Theserelated symptoms are not necessarily accompanied byworse ENoG values; and three out of them (50%) hadnot recovered within a year. Statistical analysis showedthat patients with associated vestibulocochlear symp-toms had worse recovery outcome than subjects withoutthem (p50.05 at 6 weeks; p50.02 at 3 months; andp50.009 at 6 months by 2-tailed Fisher’s exact test).Therefore, it is expected that dizziness and hearing losspossibly have a role as independent prognostic factors.

Comparison of Bell’s Palsy and Ramsay HuntSyndrome

In overall, sixty-three patients (71.6% of total; 80.3%of Bell’s palsy; and 45.5% of RHS) recovered within 6weeks from onset and 83 patients (94.3% of total; 98.5%of Bell’s palsy; and 81.8% of RHS) within 12 months (Fig.1). The cumulative recovery curves which account for allinitially enrolled patients including lost subjects areshown in Figure 3. These curves reveal significantly poorrecovery outcome in RHS than Bell’s palsy.

A lower chance of early recovery was expected inpatients with RHS (p50.028), older than age of 65(p50.014), and worse ENoG value (p<0.001) (R250.545).According to the curves shown in Figure 2, 90% chanceof recovery within 6 months is expected in patients withENoG values of 69.2% in Bell’s palsy and 59.3% in RHS.

Among 11 patients who did not recover within 3months, three out of four cases with Bell’s palsy, and threeout of seven RHS recovered within 1 year (Table II).

Cutoff Value of ENoG for PredictingNonrecovery

Differences of ENoG values between recovery andnonrecovery patients were statistically significant in

both Bell’s palsy and RHS (Fig. 4A, 4C). Based on theROC curve shown in Figure 4, the best sensitivity/speci-ficity of ENoG value to predict nonrecovery within 6weeks were 76.9%/84.9% at ENoG value of 61.5% inBell’s palsy and 75.0%/90.0% at ENoG 67.5% in RHS. Inpredicting final nonrecovery within 1 year, ENoG valueof 81.5% showed best sensitivity/specificity of nearly100%/100% in Bell’s palsy and ENoG 78.0% showed100%/94.4% in RHS.

DISCUSSIONThe prognosis of Bell’s palsy is excellent, especially

in patients with incomplete palsy.13,14 Even though theprognosis of RHS is generally poor, the recovery outcomeof incomplete palsy is much better.15 Therefore, thisstudy focused on patients with severe facial paralysiswhose recovery has more clinical importance. Facial pa-ralysis of H-B grade IV or V was included as some

Fig. 2. Chance of recovery(%) of facial movement within 6 weeks, 3 months, and 6 months by logistic regression model in Bell’s palsy (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’spalsy and 59.3% in RHS.

Fig. 3. Cumulative percent recovery of acute severe peripheral fa-cial paralysis by Kaplan-Meier survival analysis. These curvesaccount for all initially enrolled patients including lost subjects.The recovery rate of Bell’s palsy was significantly better than RHS(chi-square 9.601; P50.002 by log-rank test).


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complete paralysis may be graded as H-B grade IV or Vby the physician according to the skin thickness or facialappearance.

Overall prognosis of acute severe peripheral facialparalysis was good, as 65 out of 66 patients (98.5%) withBell’s palsy and 18 out of 22 (81.8%) RHS patients recov-ered to H-B grade I or II within 1 year from the onset.The outcomes were better than what is typicallyreported, especially in case of RHS. As the patients en-rolled in this study were uniformly managed with ste-roids and antivirals within 1 week (median 3 days) fromonset, they might have a better prognosis than thosewho were enrolled in other studies, including retrospec-tive analysis. Other possible explanations may includehost factor and clinical presentation. No obvious medi-cally ill condition or malignancy that can cause immuno-compromised status was accompanied by the enrolledpatients. In addition, vesicles preceding the paralysis,which is known to be a good prognostic factor, wereobserved in 13 patients (59.1%), and it might contributeto the better result in this study. Regarding the 6-monthoutcome (95.5% of Bell’s palsy; 72.7% of RHS recovered),

there was a considerable portion of patients showingdelayed improvement (Table II). Analysis showed thatchance of early recovery within 6 weeks was higher inBell’s palsy than RHS. In Bell’s palsy, greater ENoGvalue and age of older than 65 showed significant nega-tive effects on outcome, while only ENoG value was sig-nificant in RHS. Finally, long-term recovery of facialmovement within 1 year was significantly associatedonly with ENoG value, regardless of diagnosis, agegroup, sex, initial H-B grade, days from the onset totreatment start, and concurrent traditional treatment.Initial H-B grade had weak correlation with ENoG value(p<0.001; q520.289), which may explain the resultsfrom previous works considering it as a prognostic fac-tor.8,16–18 Regarding the traditional treatment, we rec-ommended that patients not have any concurrent herbmedicine or acupuncture treatment because of the possi-ble adverse effect or interaction. However, as it is widelybelieved in Korea that traditional medicine is an effec-tive therapy for neurologic disorder, complete controlwas not possible. Recovery outcome of patients whoreceived any concurrent traditional treatment was not

Fig. 4. Scatter dot plots showing ENoG values of recovery versus nonrecovery patients at 6 weeks and 1 year follow-up in Bell’s palsy (A)and RHS (C). Horizontal lines indicate Mean6SEM. ENoG difference between two groups were statistically significant (Bell’s palsy: P val-ue<0.001 at 6 weeks; RHS: P value50.001 at 6 weeks; 0.002 at 1 year). A receiver operating characteristic (ROC) curve showing sensitivityand specificity of ENoG value as a predictor of nonrecovery in Bell’s palsy (B) and RHS (D). Points closest to the upper left top are regionsof maximal sensitivity and specificity. ENoG values of several critical points were indicated at the graphs: (B) ENoG value of 61.5% bestpredicted 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<0.05by two-tailed Mann-Whitney U test.


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different than the others. Fisher’s exact test showed sig-nificantly worse recovery outcome in RHS patients withdizziness or hearing loss, although logistic regressionmodel did not show any significant effect on recovery,probably due to the effect of another variable and thesmall number of cases.

ENoG values were widely distributed from 9% to88% in this study. A patient with Bell’s palsy who metindications for surgical decompression (more than 90%degeneration on ENoG with no voluntary motor unitpotential on EMG within 14 days) underwent surgicaldecompression and was excluded from the study.

Decompression surgery of facial nerve is generallyconsidered in patients with low recovery chance. Basedon this study, the critical ENoG value to identify nonre-covery patients after 1 year was calculated to be 81.5%in Bell’s palsy and 78.0% in RHS, within 14 days fromthe onset. Although those values cannot precisely indi-cate a cutoff ENoG value, the values around 80% islower than the generally accepted value of 90% for theindication of surgical intervention. In addition to thefact that patients had been eligible for surgery whenENoG was greater than 75% in the past,19 previous lit-erature showed that nonrecovery rate of the patientswith 75% to 90% degeneration on ENoG was relativelyhigh.6,8,9 Considering the possible impact of facialsequelae on patient’s life quality, 12%6 to 64%8 chanceof nonrecovery is hardly acceptable. Therefore, if a sur-gical team is qualified enough to minimize surgery-related complication, decompression surgery for patientswith ENoG values between 80% and 90% should be con-sidered carefully to improve final facial outcome in casewith Bell’s palsy. The surgical decompression for RHSis often no longer recommended for its lack ofevidence.20

Regarding the test accuracy, inter-test variabilityof ENoG and techniques to reduce test errors havebeen described in many publications. Fisch21 andEsslen1 reported less than 10% variability, on conditionthat the tests were performed by a trained technician,and test-retest variability of 11.2% was reported in aprospective study by Hughes et al.22 Attempts to stand-ardize ENoG procedure have been introduced, includingthe lead placement methods,1,22,23 submaximal nervestimulation, adjustment of skin resistance,24 and stimu-lation methods.25 Although inter-test variability couldnot be completely excluded in this study, standardizedtest procedures in our clinic by a single highly experi-enced examiner provided results as consistent aspossible.

During the study period, 130 BP and 35 RHSpatients with severe facial paralysis visited our clinic.Eighty-one (62.3%) BP and 28 (80%) RHS cases satisfiedthe inclusion criteria. Rates of loss to follow-up were 15/81 (18.5%) in BP and 6/28 (21.4%) in RHS. There was nosignificant difference in ENoG values or other potentialprognostic variables in those who complete the studycompared to those who were lost to follow-up. As treat-ment regimen was concentrated in the early period of fa-cial paralysis, some patients may have showed lowcompliance to regular visits after medication. It can also

be assumed that patients with severe symptoms mighthave visited another clinic, so-called “doctor shopping,”which is relatively easy in Korean Health InsuranceSystem, and subsequently lost to follow-up.

Further research should verify these findings withclinical data from more patients. Regarding the recoveryoutcome from the patient’s view, future study consider-ing not only H-B grades but also subject discomfortswith quality of life assessment as another outcome isalso needed for comprehensive evaluation of recovery.

CONCLUSIONThis study showed that ENoG value has an inde-

pendent role as a significant prognostic indicator for pre-dicting chances of recovery in acute severe facialparalysis caused by Bell’s palsy and RHS. Higher chanceof recovery was expected with better ENoG results, andchance of early recovery after correction of ENoG effectwas still significantly worse in RHS than in Bell’s palsy.Based on our data, nonrecovery is predicted in patientswith ENoG value worse than 81.5% degeneration inBell’s palsy and 78% in RHS.

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