300

Neurophysiol 0 Elsevier,

Clin Paris

1997;27:300-8

Original

article

Reproducibility of normal facial motor nerve conduction studies and their relevance in the electrophysiological assessment of peripheral facial paralysis
P Di Bella I, F Logullo I, G Lagalla I, C Sirolla 2, L Provinciali
1 Isriruro delle Malatrie de1 Sistema 2 Demographic (Received Nervoso, ospedale regionale Torrerre, via Conca and srarisrical cenlre, INRCA, Ancona, Italy 13 January 1997; accepted 20 June 1997)

I, 60020 Ancona;

Summary - To determine the intra-examiner intertrial reproducibility of normal facial motor nerve conduction studies (FNCS) and their relevance in electrophysiological assessments of peripheral facial paralysis, 52 patients with acute unilateral Bells palsy were examined on two separate occasions 1 month apart. Three electroneurographic methods were assessed. On the unaffected side of the face, FWCS are reliable when performed by a single examiner over time. Nevertheless, compound muscle action potential (CMAP) baseline-to-peak and peak-to-peak amplitude showed a rather high intertrial variability. Reproducibility of the assessed surface electrode recording procedures was similar. Regarding the affected side, in patients with mild axonotmesis of the facial nerve variations of electroneurographic parameters 1 month apart fell within the range of normal intertrial variability. In patients with severe or moderate axonotmesis, the distal latency and the M wave amplitude variations showed significant intertrial variations. Reproducibility of FNCS appears to be similar to that found in limb motor nerves. Normal variability curtails the sensitivity of FNCS in detecting mild facial nerve axonotmesis, although this technique remains useful in severe cases. facial nerve conduction / reproducibility / Bells palsy / CMAP variability

RCsumC - ReproductibilitC de la rkponse P la stimulation electrique simple du nerf facial et sa pertinence dans le diagnostic de la paralysie de Bell. Cinquanre deux patients ayanr une paralysie de Bell onl eu deux examens ~lectrophysiologiques r6alisk ir I mois dinrervalle et faisanr appel ci trois techniques d@+entes avec recueil de la rkponse musculaire 6voquke ci [aide d.klectrodes-aiguilles ou de!lecrrodes de swface. Da c&e sain, bien que Iamplitude du CMAP soir rrt?s variable, les modifications de la rkponse molrice nt?raient pas significatives. Du c6te de la lesion, les paramPrres Plecrroneurographiques des patients ayant an axonotmkis mode& &aienr Pgalement dans les limites de la normale, randis que chez les patients ayanr un axonotmbis stWre, ils variaienr de faGon signijicative. La forte variabilitk intra-individuelle de la rLponse motrice ri la stimulation da nerf facial en fait un parambrre peu significatif pour levaluarion de laxonolmdsis au tours de la paralysie de Bell. Cependant, son enregistrement demeure utile dans les cas les plus s&&es. paralysie faciale pkiphkrique / rkponse motrice 1 nerf facial / stimulod&ection

Facial motor nerve conduction studies (FNCS) are routinely carried out in most electromyography (EMG) laboratories and are of clinical importance for the diagnosis and prognosis of lesions of the seventh cranial nerve. Authors, however, have not

Facial nerve yet reached

conduction

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a complete consensuson how these examinations should be performed regarding both the stimulation site (anterior or posterior to the ear lobe) and recording methods (surface or needle electrode, active and reference electrode placement) (Hughes et al, 1981; Auger, 1987; DeLisa et al, 1987; Kimura, 1989; Kelleher et al, 1990; Liveson and Ma, 1992; Gilchrist, 1993; Ongerboer de Visser and Cruccu, 1993). There is also little information regarding reproducibility, which is fundamental in the assessment follow-up of facial neuropathy (Sismanis, 1981; Kelleher et and al, 1990). Reproducibility also permits the use of electroneurographic parameters in controlled trials to ascertain the efficiency of new therapies. For example in the case of Bells palsy, the most common facial neuropathy, it is difficult to ascertain the true efficacy of therapies since sufficient quantity of data in regard to methods of assessment not available (Kames, 1993). is This study was aimed at determining the intertrial intra-examiner variability of facial nerve conduction studies carried out on different days using different electrophysiological recording methods and to evaluate its influence on the electrophysiological assessment of peripheral facial paralysis.

METHODS Subjects
We studied 52 patients (26 male and 26 female patients) with acute Bells palsy (mean age: 45.8 years; age range: 15-84); 24 patients suffered from left palsy and 28 from right palsy. Patients with other possible causes of peripheral or cranial nerve dysfunction or with bilateral facial palsy were excluded from this study. Subjects gave their informed consent and the study was approved by the local ethics committee.

Procedure
All patients had serial EMG-electroneurography (ENG) examinations according to the severity and evolution of the neuropathy. The first examination was performed within 48 h of onset of palsy, the second examination 1 month later, the third 3 months later, and the fourth 6 months later. All recordings were performed bilaterally to allow a left-right comparison. We used the first two consecutive (I month apart) examinations of the unaffected side of the face to determine the normal reproducibility of PNCS. Moreover, in order to assess the sensitivity of intertrial variations for facial nerve distal latency (DL) and compound muscle action potential (CMAP) amplitude regarding the presence and degree of axonotmesis, we also measured variations in DL and CMAP amplitude between the first and the second examination in those patients who exhibited electromyographic indicators of axonal loss in the latter. Concentric needle electromyography and FNCS were carried out on both sides of the face in all patients using a four-channel Nicolet Viking IIeTM (Madison, WI, USA). Percutaneous supramaximal electrical stimulation was performed with a hand-held bipolar stimulator placed near the stylomastoid foramen, ie, just below and anterior to the mastoid bone, beneath the earlobe (post-auricular position). The largest reproducible CMAP was recorded. Care was taken to obtain CMAP not altered by volume-conducted signals from nearby muscles and to ensure supramaximal stimulation, even if painful. In all 52 patients we used two recording techniques: - surface Ag/AgCl recording electrodes were placed over the orbicularis oculi (00~). nasalis and orbicularis oris (OOr) muscles and reference electrodes were placed over the same mus-

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Fig 1. Montage 1. Abbreviations: S: stimulating cathode electrode site; Gd: ground site.

site; Ra: active

recording

electrode

site; Rr: reference

recording

Fig 2. Montage 2. Abbreviations: S: stimulating cathode electrode site; Gd: ground site.

site; Ra: active

recording

electrode

site; Rr: reference.

recording

cles of the opposite side (montage 1). Care was taken to ensure the symmetry of electrode placement (fig 1). In 25 unselected consecutive patients FNCS were also performed, recording with surface electrodes from OOc nasalis and OOr muscles, taping a common reference electrode on the bridge of the nose (montage 2) (fig 2).

Facial nerve conduction studies reproducibility

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- a concentric needle electrode (CNE) was placed at the comer of the mouth in the OOr muscle (CNE recording). CMAP from the three muscles examined were recorded simultaneously first in montage 1 (muscle-to-contralateral muscle), then in montage 2 (muscle-to-nose), if performed. Finally, the CNE recording for the OOr muscle was used. Electrode positions were not marked on the skin during the first trial. MedelecTM standard electrodes were utilized: 25 mm length CNE, 0.3 mm diameter and 0.019 mm2 recording area; Ag/AgCl surface electrodes, 10 mm diameter with 2-mm hole, stuck with double-sided adhesive tape to the gently abraded recording sites, and filled with conductive jelly. In all recordings the ground electrode was placed on the forehead. Recording parameters were a 1-2-mV/division (div) gain, a 2-ms/div time base, a ~-HZ low-frequency and a IO-kHz high-frequency filter setting. DL was measured from the initial deflection from baseline with display gain set to 200 @/div. CMAP amplitude was measured with a I-mV/div display gain peak-to-peak and from baselineto-negative peak for surface electrode recordings, only peak-to-peak for CNE recordings. Latency and amplitude cursors were automatically placed by the electrodiagnostic instrument. Off-line, the physician who performed the study accepted or rejected the automatic measurements by manually placing the markers after visual assessment of the stored CMAP. Needle electromyography was performed in frontalis, OOc, nasalis, and OOr muscles. Fibrillations and positive waves were graded as follows: 0 (none), 1+ (persistent single trains in at least two areas), 2+ (moderate numbers of fibrillations in more than two areas), 3+ (many fibrillations in most areas), 4+ (fibrillations filling the baseline in all areas). The interference pattern was graded as suggested by the AAEM (1987). By considering the abundance of denervation potentials and of motor unit action potential (MUAP) recruitment of the muscle examined, the axonal loss was judged: mild if fibrillations and positive waves were 1+ or 2+ and the interference pattern reduced, moderate if fibrillations and positive waves were 2+ or 3+ and there was a discrete activity; severe if fibrillations and positive waves were 3+ or 4+ and there was a single unit interference pattern or no MUAP recruitment. Facial skin temperature was 3435C in all patients. Subjects, lying comfortably, were allowed 15 min to adjust to room temperature that was kept constant all year round at 22-24 C. All patients were examined between 8.30 and 11 .OO am. The same EEG/evoked potentials (EP) technician and the same experienced electromyographer conducted recording studies. The investigators were blind as to the nature of the data that had been acquired in the previous session during patients examination and to the off-line review of the acquired electroneurographic parameters. Data analysis
Results were analyzed using the statistical package for social sciences (SPSS PC 5.0+TM, Chicago, IL, USA). The effects of the type of electrodes, side of active and reference electrodes, CMAP parameters (baseline-to-peak amplitude or peak-to-peak amplitude) on FNCS repeatability in two trials 1 month apart were assessed by an analysis of variance for repeated measures using MANOVA. Mean and standard deviation (SD) of the absolute (ms, mV) and percentage (%) variability of facial nerve distal latency, baseline-to-peak and peak-to-peak CMAP amplitude in the three assessed recording procedures were calculated by subtracting results of the second trial from those of the first trial. Comparison between mean f SD obtained for each parameter examined using the different recording methods was done using Scheffes test for multiple comparisons. P values lower than 0.05 were considered significant after Bonferronis correction.

304
Table 1. Normal values of facial motor

P Di Bella et al nerve conduction Momage SD 0.32 0.62 0.73 0.25 0.70 0.87 0.26 0.72 1.03 I IA 14 33 39 1: 32 14 35 38 Mean 3.05 2.06 2.22 3.18 2.82 3.23 3.13 1.60 2.30 studies *. Montage SD 0.23 0.67 0.75 0.21 0.68 0.93 0.23 0.73 0.98 2 IA 15 36 38 12 30 31 3.47 :;1 33 6.18 0.38 2.55 11 43 CNE recording Mean SD

Muscle Orbicularis Oculi Nasalis

Attribute DL (ms) B-PA (mV) P-PA (mV) DL (ms) B-PA (mV) P-PA (mV) DL (ms) B-PA (mV) P-PA (mV)

Mean 3.10 1.92 2.14 3.30 2.57 2.96 3.17 2.19 2.82

IA

Orbicularis oris

* Number of subjects (32, 15 men der were not significant. Montage 1: reference electrode on of the nose; IA: highest percentual CNB: concentric needle electrode; peak amplitude.

and 17 women;

ages: 16 to 74 years;

mean age 48 years).

Age and gen-

the contralateral muscle; montage 2: reference electrode on the bridge intratrial intra-individual asymmetry between the two sides of the face; DL: distal latency; B-PA: baseline-to-peak amplitude; P-PA: peak-to-

Table II. Intertrial intra-individual centage values (mean rt SD).

variability

of facial

motor

nerve

conduction

studies.

Absolute

and per-

Muscle

Attribute

Montage I (5.7Prs) ABS %

Montage I (25 pts *) ABS 70

Montage 2 (25 pts) ABS %

Surface electrode recordings Orbicularis DL (ms) 0.15*0.14 Oculi B-PA (mV) 0.32 f 0.25 P-PA(mV) 0.34kO.23 Nasalis DL (ms) 0.17rtO.13 B-PA (mV) 0.30* 0.20 P-PA (mV) 0.33 f 0.25 Orbiculruis DL (ms) 0.15*0.10 B-PA (mV) 0.36 f 0.26 Oris P-PA(mV) 0.45kO.35 CNE recording Orbicularis DL (ms) Oris P-PA (mV)

4.7.5* 15.87 f 16.16* 5.09+ 12.20 + 11.27 f 4.68* 16.18 f 17.12*

4.70 0.14*0.12 10.87 0.36 f 0.25 9.62 0.33 kO.22 3.90 0.14?0.13 8.49 0.27 kO.20 8.72 0.34 20.25 3.01 0.14~0.09 10.50 0.34 + 0.25 13.08 0.35kO.32

5.30+ 4.30 17.16? 10.30 15.CO+ 8.21 4.53+ 4.05 10.25 f 7.30 10.22 f 6.96 4.36* 2.69 15.14 f 9.75 14X%+ 10.33

0.13?0.11 0.37 f 0.21 0.37iO.27 0.16*0.09 0.30+0.19 0.34 * 0.22 0.16~0.10 0.30 f 0.23 0.35kO.29

4.21* 3.37 17.98 f 8.92 16.86+ 11.74 4.89+ 2.85 10.55 + 6.55 10.7Oi 7.01 5.25* 3.10 17.27 f 10.40 13.80+ 9.47

0.19+0.16 5.72+ 5.36 1.54 i 1.219 24.01 + 17.535

* In whom both montage 1 and montage 2 were performed. Montage 1: reference electrode on the contralateral muscle; montage 2: reference electrode on the bridge of the nose; DL: distal latency; B-PA: baseline-to-peak amplitude; P-PA: peak-to-peak amplitude; ABS: absolute value; 5: significantly different as compared with montage 1 and montage 2 (see Methods); CNE: concentric needle electrode.

RESULTS Normal values of FNCS are shown in table I. In all patients first examination, FNCS were normal on both the healthy and the affected side. In table II the mean it SD absolute and percentage values of intertrial intra-examiner variability of FNCS are summarized. In MANOVA no statistically significant source of variance was found when surface electrode recording trials were considered (table III).

Facial nerve conduction

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305
on facial motor nerve conducfor repeated measures using

Table III. Effects of recording procedure, test day and muscle examined tion studies (FNCS) repeatability assessed by analysis of variance MANOVA. Source ofvariafion Surface Methods Muscles Methods Surface Methods electrode x time x time x muscle recording B-PA df

F value FNCS 0.06 0.80 0.02

P value

F value

P value

F value

P-PA df

P value

time needle

; 2

NS NS NS in orbicularis NS

3.52 0.26 0.29

: 2

NS NS NS

3.44 0.24 0.31 5.79

1 2 2 2

NS NS NS < 0.01

and concentric x time

recording 0.07 2

oris muscle

DL: distal latency; B-PA: CMAP baseline-topeak amplitude; P-PA: compound muscle action potential peakto-peak amplitude; methods: montage I, montage 2, concentric needle recording (see text); muscles: orbicularis oculi, nasalis, orbiculatis oris; time: first trial, second trial; df: degree of freedom; NS: not significant.

Table ance.

IV. Summary

of the P and F values

of the attributes

examined

for intra-examiner

analysis

of vari-

Muscle Surface recording Montage 1

Attribute

Orbicularis Nasalis Orbicuhvis

oculi

oris

DL (ms) B-PA (mV) P-PA (mV) DL (ms) B-PA (mV) P-PA (mV) DL (ms) B-PA (mV) P-PA (mV) DL (ms) B-PA (mV) P-PA (mV) DL (ms) B-PA (mV) P-PA (mV) DL (ms) B-PA (mV) P-PA (mV) DL (ms) P-PA (mV)

0.67 1.40 0.93 0.07 0.89 1.44 0.78 1.49 I .87 0.52 1.18 0.69 0.11 0.79 0.84 0.36 0.64 1.95 1.72 1.13 2: reference electrode B-PA: baseline-to-peak

NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS on the bridge amplitude;

Surface recording Montage 2

Orbicularis

oculi

Nasalis Orbicularis oris

CNE recording

Orbicularis

oris

Montage I : reference electrode of the nose; CNE: concentric P-PA: peak-to-peak amplitude;

on the contralateral muscle; montage needle electrode; DL: distal latency; NS: not significant,

Surface recording FNCS did not vary significantly depending on the test day (tables III, IV). FNCS variability was not significantly influenced by recording site (OOr vs OOc vs nasalis muscle). In 25 patients in whom both surface electrode recording montages were used, FNCS repeatability did not significantly differ when the reference electrode was on the bridge of the nose or on the contralateral homony-

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mous muscle. CMAP amplitude measurement reproducibility was not significantly influenced when measuring it baseline-to-peak or peak-to-peak. When ANOVA was computed to determine whether in CNE recordings DL and CMAP peak-to-peak amplitude vary depending on the test day, nerve conduction measurements proved reliable and comparable in time (table IV). Repeatability of OOr muscle CMAP peak-to-peak amplitude measurements was significantly worse in CNE recordings than in surface recordings, both in montage 1 and in montage 2 (table II). DL reproducibility was not significantly influenced by CNE or surface electrode recording (tables II, IV). In all montages DL repeatability was significantly better than CMAP repeatability. In surface recordings, automated cursor placement was more accurate on nasalis muscle than on OOr or OOc muscles, because a more frequent clear-cut negative onset of nasalis CMAP allowed for more reliable latency and amplitude measurements. More than 70% of OOc CMAP and about 60% of OOr CMAP required manual marker replacement, while nasalis CMAP measurements were correct in about 70% of trials. Electromyographic examination performed 1 month after onset of facial palsy showed signs of axonotmesis on the side affected by the paralysis that were severe in 14 patients, moderate in ten others, and mild in 11. Setting the normal value of intertrial intra-individual variability DL and CMAP amplitude at mean + 2 SD, we assessed the sensitivity to axonotmesis of these two electroneurographic parameters when using the different montages. In both montage 1 and montage 2 and in OOr CNE recordings, DL showed significant variations in all patients with severe ongoing axonotmesis and in three patients with moderate axonotmesis without there being differences in sensitivity between the three montages and the muscles examined (in montages 1 and 2). In both montage 1 and montage 2, CMAP amplitude, measured peak-to-peak and baseline-to-negative peak, showed significant intertrial variations in all patients with severe or moderate axonotmesis, without any differences between the two montages. In patients with moderate axonotmesis, OOr muscle CMAP had the most frequent significant variation (ten of ten patients), while OOc and nasalis CMAP proved to be significantly different between the first and second examination in seven of ten patients. In OOr muscle CNE recordings, CMAP showed significant variations in all patients with severe axonotmesis and in five patients with moderate axonotmesis. Although evaluation of the prognostic value was not the purpose of this study, we assessed that of facial EMG and direct facial motor studies performed within 48 h of onset of facial palsy. These studies did not correlate with the evolution of facial neuropathy. DISCUSSION The main findings of our study were that: - normal FNCS are reliable when performed by a single examiner over time; - intertrial CMAP amplitude variability is nevertheless high; - this variability curtails the sensitivity of FNCS in detecting mild axonotmesis; - the various surface electrode recording methods assessed in our study have similar repeatability. In our study FNCS proved to be reproducible, but their normal variability when carried out on different days by the same examiner, was rather high, above all for the M wave of the facial muscles. Kelleher et al (1990) and Hughes et al

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(1981), although using methods different from ours and from those recommended by standard electroneurographic reference tests, also found that FNCS were reproducible. To our knowledge, our study establishesfor the first time the normal range of the M wave variability, both for DL and for amplitude. FCNS variability appears to be similar to that found in upper and lower limb electroneurographic studies (Trojaborg, 1964; McQuillen and Gorin, 1969; Bergmans, 1971; Bjorkqvist et al, 1977; Oh, 1984; Alexander and Stigler, 1989; Bleasel and Tuck, 1991; Chaudry et al, 1991, 1994; Claus et al, 1993; Valensi et al, 1993). Likewise, the range of variability for the DL is also significantly lower than for the M wave amplitude. In our study, as in previous ones, the M wave amplitude proved to be more sensitive than DL for revealing the presence and the entity of facial nerve axonotmesis (Kimura, 1989; Karnes, 1993; van Dijk et al, 1995). Since this factor determines the prognosis, the M wave amplitude becomes the most important ENG parameter in clinical practice. However, as shown by our study in casesof mild axonotmesis, the extent of intertrial variability limits the sensitivity of the M wave amplitude. In fact the variation of the M wave amplitude provoked by mild axon loss falls within the range of normal intertrial variability. Therefore, as with other muscles of the body, the EMG of facial muscles is still to be considered as the electrophysiological test which is the most sensitive to the presence of axonotmesis. ENG, on the contrary, although being specific and able to allow for detection of those patients whose axonotmesis is significant for the prognosis, is, however, insufficient to allow for a thorough diagnosis. This should be borne in mind when clinical examination is integrated with EMG-ENG and when electrophysiological tests are used in controlled clinical studies in order to stratify patients, to assess evolution of the diseaseover a period of time, and as an end point. The definition of ranges of intertrial variability is therefore important in both clinical practice and research. To reduce this variability, our study also evaluated various procedures by comparing different montages and recording techniques in different muscles. Despite the great number of variations that we introduced, none of the methods using surface electrode recording was able to improve FNCS reproducibility. As with recordings from the limbs, facial ENG carried out with concentric needle electrode recording, which is still recommended by some authors (DeLisa et al, 1987), proved to be lessreliable than surface electrode recording. Measurement of the M wave of the nasalis muscle was easier and more rapid. If for reasons of time or patient tolerance a greater number of facial muscles cannot be examined, we suggest that facial nerve ENG be performed using surface electrode recording for nasalis muscle during daily routine examinations and in any controlled therapeutic trials. The range of FNCS intertrial variability calculated for ones own laboratory or found in literature should, however, always be borne in mind. We did not find any prognostic value in performing direct facial motor studies within 48 h of onset of facial palsy; the prognostic value of blink reflex and of direct motor nerve evoked responseamplitude 7-10 days after onset of facial paralysis has been discussedelsewhere (Kimura, 1989; Neau et al, 1992; Gilchrist, 1!)93). ACKNOWLEDGMENTS
The authors thank L Filipponi the English. for her skillful technical assistance andF Baker for scrutinizing

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