Abstract In this study, ten patients who exhibited severeunilateral Bell’s palsy of the House-Brackmann grade Vunderwent facial electroneurography (ENoG) on the con-tralateral, healthy side. Serial ENoG was conducted inseven consecutive sessions within 6 months at a givencurrent intensity level of stimulation. According to our re-sults, all the patients presented a rise in the maximumcompound-action potential (MCAP) amplitude on thehealthy side within 20 to 45 days from the onset of thepalsy and shortly after the onset of the recovery of the fa-cial function. This was attributed to the central contralat-eral compensatory process, which restores balanced facialfunction. Based on our data, a hypothetical model is shown,which demonstrates the clinical course of the contralateralMCAP values and reflects the plasticity effect of the cen-tral nervous system after the onset of Bell’s palsy.

Keywords Facial nerve · Facial palsies · Electroneurography · Neuroplasticity

Introduction

In the evaluation of facial nerve palsy, electroneurography(ENoG) is widely used as a quantitative method to assessthe degeneration of the facial nerve. Esslen first devel-oped ENoG in 1977 [6]. Since then, many studies havecited its prognostic value in the management of Bell’spalsy. By comparing the amplitude of the compound-ac-tion potential (CAP) of the paralyzed side to that of theopposite normal side, an estimate of the number of nervefibers that have not undergone Wallerian degeneration,expressed in percentage, could be obtained [8]. So far, theCAP absolute values of both sides, correlated separately,were not considered to be of clinical importance [11].

The neuroplastic changes induced on the contralateralside after injuries, such as the transection of the facialnerve, have been extensively studied, especially in adultrats [13]. It has already been demonstrated that patientswith complete unilateral denervation of the muscles afterfacial nerve palsy who also exhibited postfacial palsy con-tracture showed an unusually high amplitude in facial-re-flex excitability [1, 3]. This electrophysiological hyperex-citability was elicited in both facial sides, but especially inthe healthy, contralateral one. It was assumed that changesin organization at the level of the facial nucleus occurredunder a central effect. Thus, during electrophysiologicaltests such as electroneurography in facial nerve diseases,the concomitant contralateral alterations should also beassessed.

The purpose of this study was to attempt to measureand correlate the absolute values of the intact facial side inorder to follow the electrophysiologic response of thecontralateral facial nerve in cases of unilateral Bell’spalsy. Patients with severe facial palsy were selected inorder to better evaluate the role of the contralateral side.

Materials and methods

Ten patients aged 8–87 years old (mean: 48.8) suffering from uni-lateral Bell’s palsy were evaluated. All patients exhibited severe,House-Brackmann grade V facial palsy. A history was obtainedfrom each patient, and there was no previous history of facial palsyin any of these patients. A physical examination and audiologicbattery tests, including the stapedial reflex, were performed.

The surface-recording electrode was fixed just lateral to thenasal ala, with the center of the electrode placed 5 mm in the na-solabial fold [17]. The reference electrode was placed in the sameposition, but on the contralateral side. The first medial centimeterof the clavicle was chosen for the ground electrode. The area of thepatient’s skin to be placed in contact with the electrodes was pre-pared with an electrode gel swab. Conducting gel was placed onthe disk of the electrodes. The stimulus comprised monophasicsquare waves of 50 µs, delivered at a rate of 0.5/s. The amplifiergain was adjusted to 500 µV/div for both sides. The pass-band wasdetermined between 10–2,500 Hz. Impedance electrodes werechecked as being always under 5 KΩ.

The surface stimulator (Amplaid MK12) was placed over themain trunk of the facial nerve with the anode just outside of the

G. Psillas · J. Daniilidis

Facial electroneurography on the contralateral side in unilateral Bell’s palsy

Eur Arch Otorhinolaryngol (2002) 259 :339–342DOI 10.1007/s00405-002-0471-0

Received: 28 September 2001 / Accepted: 22 March 2002 / Published online: 9 May 2002

MISCELLANEOUS

G. Psillas ( ) · J. DaniilidisORL Clinic, Aristotelian University of Thessaloniki, AHEPA Hospital, 1 Stilponos Kyriakidi Str., 54006 Thessaloniki, GreeceFax: +30-31-994916

© Springer-Verlag 2002

stylomastoid foramen and the cathode in front of the ear lobe. Ineach examination, we respected these anatomical limits, obtaininga number of recordings each time, with the aim of ensuring reliablemean values.

The current intensity (mA) was increased from zero to a levelsufficient to evoke the maximum compound-action potential(MCAP). An additional 10% of current was added to ensure supra-maximal stimulation. MCAP was calculated in microvolts (µV).Patient discomfort and nonfacial artifacts were avoided.

In order to better evaluate the intrasubject amplitude variabilityof the compound-action potential, we used the same current inten-sity. This current intensity value was determined to be the onewhich elicited MCAP in the first session. Thus, this current inten-sity value remained the same for each individual patient in the ses-sions that followed.

The lack of reliability and validity in the latency measures [9]causes us to prefer the traditional amplitude parameter [6], namely,peak-to-peak or absolute amplitude. The peak-to-peak intrasubjectamplitude from the intact side was measured in µV. A statisticalmethod (Student’s t-test) was used for comparing peak-to-peak in-trasubject amplitude from one session to another.

From the onset of facial paralysis, all the patients were assessedin seven consecutive sessions within 6 months. In month 1, pa-tients were submitted to four examinations and then follow-up test-ing was carried out in the 2nd, 4th and 6th months after the onsetof palsy.

The time at which facial function recovery commenced wasnoted for each patient. Postfacial palsy synkinesis was not ob-served in any of the patients.

Treatment was identical for all the patients, including the intra-venous administration of steroids and vasodilators in various doses,depending on the age.

Data were obtained from previous control measurements in ourclinic in order to assess the amplitude variability on normal sub-jects. In this study, 25 healthy subjects, 13 women and 12 men,were examined under the same testing conditions as the group ofpatients. The subjects were recruited from the medical and techni-cal staff and from medical students in our clinic. Their ages rangedfrom 17 to 42 years (mean: 25 years). None of the test persons hadsymptoms of an acute virus infection, and none of the women werepregnant at the time of testing. Every subject was submitted toseven examinations, the first in 15 days and then after every monthup to 6 months. The tests were performed first on the right side andthen on the left. A statistical method (Student’s t-test) was used forintrasubject MCAP comparison from the seven consecutive ses-sions.

Results

According to our results (Table 1), all the patients pre-sented a rise in MCAP amplitude on the side contralateralto the affected side. The detailed measures of amplitude inrelation to the time of the onset of facial nerve paralysisare shown in Table 1.

For each patient, measures taken on the healthy sideand indicating the first rise in MCAP, which occurredwithin a maximum of 1 month from the onset of paralysis,were compared with the previous low ones for statisticalreasons. MCAP reached maximal values of between 254and 2,254 µV (mean: 1,237.4 µV) when previous low MCAP values ranged from 175 to 1,823 µV (mean:756.4 µV). The difference between these sequential mea-sures was calculated statistically (Student’s t-test) and wasfound to be highly significant (P<0.001). Amplitude mea-surements were then compared between consecutive peri-ods of 1, 2, 4 and 6 months from the onset of paralysis.These comparisons showed that the difference in MCAPmeasures between months 1 and 2 (P>0.05) and months 2and 4 (P>0.05) was not statistically significant, but be-tween months 4 and 6 a significant drop occurred(P<0.001). MCAP measures were also compared betweenthe first rise at 1 month and after 4 and 6 months, and al-though the difference at 4 months was not yet statisticallysignificant (P>0.05), at 6 months it was found to be highlysignificant (P<0.001). Finally, comparing the amplitudemeasurements shortly before the first rise and at 6 months,we concluded that the latter values are higher than the for-mer ones (0.01<P<0.05).

Based on the above data, a hypothetical model show-ing the clinical course of the contralateral MCAP values isillustrated in Fig.1. In the first 2 weeks after the onset offacial paralysis, MCAP values remain invariable. Then, inthe subsequent 3rd or 4th weeks, MCAP values abruptlyrise to a plateau threshold. This plateau remains constantfor approximately 13 weeks, beginning in the 3rd weekand lasting until the 4th month. After that period, MCAP

340

Patient Age, sex, Current Day 10 Week 2 Week 3 Month 1 Month 2 Month 4 Month 6side of paralysis intensity

(mA)

1 59 years, F, R 22 725 823 1,400 1,450 1,427 1,489 9702 30 years, M, R 30 178 176 175 254 376 423 1973 87 years, F, R 28 267 278 529 860 890 857 6784 8 years, F, L 34 1,840 1,823 2,254 2,531 2,497 2,596 1,9565 70 years, M, L 52 902 627 1,058 1,370 1,313 784 7506 46 years, F, L 38 850 879 1,117 1,590 1,647 1,638 1,2807 66 years, M, R 40 863 860 863 1,078 1,256 1,278 9218 42 years, M, R 46 734 788 750 1,040 1,450 1,567 8329 15 years, M, L 26 1,000 1,095 1,333 1,372 1,578 1,505 1,213

10 65 years, F, L 43 1,810 1,803 1,980 1,989 1,950 1,965 1,750

Table 1 Electroneurographic values (in µV) of MCAP amplitudefrom the contralateral normal side in patients with unilateral facialpalsyand carried out in seven consecutive sessions. The personal

data of the patients, the side of facial nerve paralysis and the current intensity applied in milliamperes (mA) are also shown.(M male, F female, R right, L left)

values drop to a level that is nevertheless still higher thanthe values before the plateau.

Table 2 shows the time at which facial function recov-ery commenced on the side contralateral to the affectedside, combined with the first rise in MCAP in relation tothe onset of facial paralysis. All patients experienced re-covery within 18 days of the onset of paralysis. On thecontralateral side, the first rise in MCAP occurred 20 to45 days after the onset (mean: 26.4 days). The first rise inMCAP always took place after the first clinical signs ofrecovery with a delay of 3 to 27 days.

In the control group, no intrasubject variations in am-plitude were recorded after seven consecutive ENoGrecordings taken from all healthy subjects (P>0.05) onboth sides.

Discussion

ENoG is widely applied as an objective tool for evaluat-ing facial nerve function and measuring facial nerve ac-tivity. During calculations applied to extract the percent-age of degenerated facial motorneurons, the contralateralintact electrophysiologic response was always overlooked.This was inevitable since ENoG was devised to evaluatethe relative neural degeneration of the two sides as a per-centage value. In this way, progressive facial nerve de-generation is followed on several occasions with ENoGrecordings based on the more clinically practical percent-age values.

In this study, we assessed the contralateral electrophys-iological facial course in relation to the side affected withBell’s palsy. According to our results, in serial ENoGmeasurements in all our patients with complete facialBell’s paralysis, the amplitude of the MCAP on the con-tralateral healthy side was increased at a given intensitylevel of stimulation shortly after the onset of the recoveryof the facial function. This means that as long as facialparalysis clinically persisted, the amplitude of the MCAPdid not alter. Once facial function returned, the MCAPsubsequently presented a rapid rise in amplitude.

The mechanism explaining this rise in MCAP ampli-tude is not fully understood. Potentials of larger amplitudeare successfully obtained with increased intensity stimula-tion of the exposed facial nerve or with greater proximityto the facial-nerve generator site [2, 10, 15]. It is assumedthat increased amplitude reflects a state of improved stim-ulation of the facial nerve in which more neural axons andtheir innervated muscle fibers become activated. For ex-ample, in experiments carried out on normal cats, a largeramplitude of evoked antidromic potentials is obtained byincreased stimulus intensity following bipolar stimulationof the exposed nerve trunk at the stylomastoid foramen[15]. In dogs [10], as the stimulus intensity applied to theperipheral facial branches was increased, the amplitude ofthe nerve response also increased. In humans [2], follow-ing electrical stimulation of the marginalis mandibulae,facial nerve-evoked antidromic potentials were recordedon the proximal portion, raised as a function of stimulusintensity. Moreover, the identification of the generator siteof the facial nerve after either electrical stimulation [15]or magnetic stimulation [12, 16] is achieved by elicitingthe largest amplitude by means of recording electrodesover a specific position on the scalp.

The electrophysiological finding of the rise in MCAPamplitude shortly after the onset of the recovery of thenerve may be attributed to the central compensatoryprocess, which is developed following unilateral Bell’spalsy. The central plasticity effect could be expressed asan increased input to the damaged nerve, resulting in thisrise in MCAP amplitude in order to achieve balanced fa-cial function. The central plasticity phenomenon has al-ready been noted after the occurrence of facial nerve in-sult. Central mechanisms, followed by facial nerve tran-section and reconstruction, caused contralateral mo-

341

Fig.1 Hypothetical model showing the clinical course of the con-tralateral MCAP values (in microvolts). In the first 2 weeks afterthe onset of facial paralysis, MCAP values remain invariable.Then, within the subsequent 3rd or 4th weeks, MCAP valuesabruptly rise to a plateau threshold. This plateau remains constantfor approximately 13 weeks, beginning in the 3rd week and lastinguntil the 4th month. After that period, MCAP values fall to a levelthat is nevertheless still higher than the value before the plateau

Table 2 First signs of recovery, first rise in MCAP and the differ-ence between the two, in days, of all patients after the onset of thefacial paralysis

Patient First signs First rise Differenceof recovery in MCAP

1 17 20 32 13 34 213 13 32 194 16 21 55 14 20 66 8 22 147 14 28 148 18 45 279 18 21 3

10 8 21 13

torneurons to sprout axons to cross the midline and rein-nervate the denervated muscle [7]. It was shown that fa-cial muscle denervation was able to induce a contralateralcompensatory process, called the cross-reinnervation phe-nomenon, in patients operated on for the removal ofacoustic neuroma who had had a seventh-twelfth-nerveanastomosis [18]. This was expressed by increasing am-plitude values after electrical stimulation was given on thenormal side. Contralateral motor cortex changes, as a re-sult of the cortical reorganization that follows peripheralfacial nerve transection, were also described in adult rats[13, 14, 19].

A similar central compensatory process involving thecontralateral healthy side is also described for the vestibu-lar system, although this constitutes a polysynaptic andmore complicated sensory tract. It has been demonstratedin hemilabyrinthectomized frogs [4, 5] that, after behav-ioral compensation, the increased amplitude of excitatorypostsynaptic potentials was elicited by the stimulation ofthe contralateral vestibular nerve. In cats after unilaterallabyrinthectomy, the resting activity of the contralateralcentral vestibular neurons in the compensated state, de-spite being reduced towards more normal levels, remainedelevated in relation to the normal levels [20].

According to the hypothetical plateau (Fig.1), the cen-tral plasticity process lasts for approximately 13 weeks,beginning in the 3rd week and lasting until the 4th month.The compensatory process does not seem to occur after 4 months. This time possibly corresponds to that of thehealthy side, when the reinnervation, by means of the out-growth of axons and/or collateral sprouting, is developed.On the affected side, CAP amplitude starts to improvewithin a maximum period of 4 months from when theminimal CAP response was elicited [17]. Although MCAPmeasures do drop on the healthy side 4 months after theonset of Bell’s paralysis, the values are still significantlyhigher compared to those before the central plasticityprocess arises. It is possible that total electrophysiologicalfacial recovery will not have been achieved by the time 6 months have passed.

We electrophysiologically demonstrated the contribu-tion of the contralateral side during the clinical course ofuncomplicated unilateral Bell’s palsy. This study supportsthat this phenomenon is the result of the plasticity of thecentral nervous system and occurs in cases of completerecovery, in the same way as the cross-reinnervation phe-nomenon described when the stimulus is being given onthe normal side [18]. The assessment of absolute MCAPvalues could provide supplementary information aboutthe clinical course of not only idiopathic etiologies, suchas that of Bell’s palsy, but also those of other facial nervedisorders, such as trauma, herpes zoster oticus infection,etc.

As our results show, in Bell’s palsy the MCAP ampli-tude is increased on the healthy side. Up until now, the re-sulting MCAP percentage in facial electroneurographywas based on the healthy side, which had the role of thecontrol side. This results in misleading conclusions, be-

cause the compensatory alterations of the contralateralhealthy side has not been taken into account in MCAPpercentage calculations thus far. In ENoG measurements,absolute MCAP values should be thoroughly evaluated onboth sides in order to obtain objective and reliable results.

References

1.Bratzlavsky M, Eecken HV (1977) Altered synaptic organiza-tion in facial nucleus following facial nerve regeneration: anelectrophysiological study in man. Ann Neurol 2: 71–73

2.Colletti V, Fiorino FG, Policante Z, Bruni L (1996) New per-spectives in intraoperative facial nerve monitoring with an-tidromic potentials. Am J Otol 17: 755–762

3.Cossu G, Valls-Solé J, Valldeoriola F, Munoz E, Benitez P,Aguilar F (1999) Reflex excitability of facial motoneurons atonset of muscle reinnervation after facial nerve palsy. MuscleNerve 22: 614–620

4.Dieringer N, Precht W (1979) Mechanisms of compensationfor vestibular deficits in the frog. I. Modification of the excita-tory commissural system. Exp Brain Res 36: 311–328

5.Dieringer N, Precht W (1979) Mechanisms of compensationfor vestibular deficits in the frog. II. Modification of inhibitorypathways. Exp Brain Res 36: 329–341

6.Esslen E (1977) Electrodiagnosis of facial palsy. In: Miehlke A(ed) Surgery of the facial nerve. Saunders, Philadelphia, pp 45–51

7.Fernandez E, Pallini R, Marchese E, Lauretti L, Bozzini V,Sbriccoli A (1992) Reconstruction of peripheral nerves: thephenomenon of bilateral reinnervation of muscles originally in-nervated by unilateral motorneurons. Neurosurgery 30: 364–369

8.Fisch U (1980) Maximal nerve excitability testing vs elec-troneurography. Arch Otolaryngol 106: 352–357

9.Halvorson DJ, Coker NJ, Wang-Bennett LT (1993) Histologiccorrelation of the degenerating facial nerve with electroneurog-raphy. Laryngoscope 103: 178–184

10.Hanson DG, Honrubia V (1985) Evoked responses from pe-ripheral stimulation of the facial nerve. Am J Otolaryngol 6:98–102

11.Kartush JM, Lilly DJ, Kemink JL (1985) Facial electroneurog-raphy: clinical and experimental investigations. OtolaryngolHead Neck Surg 93: 516–523

12.Kartush JM, Bouchard KR, Graham MD, Linstrom CL (1989)Magnetic stimulation of the facial nerve. Am J Otol 10: 14–19

13.Landgrebe M, Laskawi R, Wolff JR (2000) Transient changesin cortical distribution of S100 proteins during reorganizationof somatotopy in the primary motor cortex induced by facialnerve transection in adult rats. Eur J Neurosci 12: 3729–3740

14.Laskawi R, Landgrebe M, Wolff JR (1996) Electron micro-scopical evidence of synaptic reorganization in the contralat-eral motor cortex of adult rats following facial nerve lesion.ORL 58: 266–270

15.Metson R (1988) Facial nerve evoked potentials in the cat. Oto-laryngol Head Neck Surg 98: 130–137

16.Metson R, Rebeiz E, West C, Thornton A (1991) Magneticstimulation of the facial nerve. Laryngoscope 101: 25–30

17.Thomander L, Stålberg E (1981) Electroneurography in theprognostication of Bell’s palsy. Acta Otolaryngol 92: 221–237

18.Soudant J, Lamas G, Vitte E, Tankere F, Willer JC (1999)Evaluation of the facial nerve palsies: are the grading systemsreliable? Face 6: 175–185

19.Wolff JR, Laskawi R, Spatz WB, Missler M (1995) Structuraldynamics of synapses and synaptic components. Behav BrainRes 66: 13–20

20.Yagi T, Markham CH (1984) Neural correlates of compensa-tion after hemilabyrinthectomy. Exp Neurol 84: 98–108

342