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Evoked electromyography to rocuronium in orbicularis orisand gastrocnemius in facial nerve injury in rabbits

journal homepage: www.JournalofSurgicalResearch.com

Yian Xing, MD, Lianhua Chen, MD, PhD,* and Shitong Li, MD, PhD

Department of Anesthesiology, The Affiliated First People’s Hospital, Shanghai Jiaotong University, Shanghai, China

a r t i c l e i n f o

Article history:

Received 4 April 2013

Received in revised form

15 May 2013

Accepted 23 May 2013

Available online 19 June 2013

Keywords:

Sensitivity

Rocuronium

Orbicularis oris

Gastrocnemius

Evoked electromyography

Facial nerve injury

* Corresponding author. Department of Anes200080, China. Tel./fax: þ86 21 6324 0090.

E-mail address: chenlianhua1991@yahoo0022-4804/$ e see front matter ª 2013 Elsevhttp://dx.doi.org/10.1016/j.jss.2013.05.087

a b s t r a c t

Background: Muscles innervated by the facial nerve show different sensitivities to muscle

relaxants than muscles innervated by somatic nerves, especially in the presence of facial

nerve injury. We compared the evoked electromyography (EEMG) response of orbicularis

oris and gastrocnemius in with and without a non-depolarizing muscle relaxant in a rabbit

model of graded facial nerve injury.

Methods: Differences in EEMG response and inhibition by rocuroniumwere measured in the

orbicularis oris and gastrocnemius muscles 7 to 42 d after different levels of facial nerve

crush injuries in adult rabbits.

Results: Baseline EEMG of orbicularis oris was significantly smaller than those of the

gastrocnemius. Gastrocnemius was more sensitive to rocuronium than the facial muscles

(P < 0.05). Baseline EEMG and EEMG amplitude of orbicularis oris in the presence of

rocuronium was negatively correlated with the magnitude of facial nerve injury but the

sensitivity to rocuronium was not. No significant difference was found in the onset time

and the recovery time of rocuronium among gastrocnemius and normal or damaged facial

muscles.

Conclusions: Muscles innervated by somatic nerves are more sensitive to rocuronium than

those innervated by the facial nerve, but while facial nerve injury reduced EEMG responses,

the sensitivity to rocuronium is not altered. Partial neuromuscular blockade may be

a suitable technique for conducting anesthesia and surgery safely when EEMG monitoring

is needed to preserve and protect the facial nerve. Additional caution should be used if

there is a risk of preexisting facial nerve injury.

ª 2013 Elsevier Inc. All rights reserved.

1. Introduction techniques, including remifentanil infusion or high-dose

Evoked electromyography (EEMG) is commonly used during

surgery to detect the location and path of the facial nerve in

bone and tissues and thus prevent iatrogenic facial nerve

injuries [1,2]. The EEMG response depends on relatively intact

transmission of action potentials at the neuromuscular

junction, which is generally blocked by muscle relaxants

during the conduct of general anesthesia. Although some

thesiology, The Affiliated

.cn (L. Chen).ier Inc. All rights reserved

opioid or inhalational anesthesia can maintain adequate

body immovability, proper usage of muscle relaxants is still

a simple and safe strategy to maintain skeletal muscle

paralysis and facilitate mechanical ventilation, meanwhile

avoiding cardiac depression or delayed emergence from

anesthesia. On the other hand, it is important to measure

the extent of neuromuscular blockade in the most accurate

way or place in particular surgeries for the reason that

First People’s Hospital, Shanghai Jiaotong University, Shanghai,

.

j o u r n a l o f s u r g i c a l r e s e a r c h 1 8 5 ( 2 0 1 3 ) 1 9 8e2 0 5 199

train-of-four monitoring does not give the same results at

different nerves [3]. We have previously shown that partial

neuromuscular blockade to the extent of 50% inhibition of

conduction at the ulnar nerve maintains sufficient neuro-

muscular function to monitor the facial nerve safely [4]. We

also found that themechanismunderpinning this observation

was that muscles innervated by the facial nerve and somatic

nerves display different sensitivities to neuromuscular

blocking drugs [5]; these findings were consistent with other

studies [6,7].

In clinical practice, a proportion of patients may already

have a degree of facial nerve injury before surgery, due to

trauma, inflammation, or infiltration by tumors. The ampli-

tude of EEMG responses is reduced in patients whose facial

nerve function are impaired before surgery compared with

those whose facial nerve functions are normal [8]. To avoid

iatrogenic injury in patients with preexisting or unrecognized

impairment of facial nerve function, EEMGmonitoring should

be conducted with extra caution. Moreover, different degrees

and time courses of facial nerve injuries may cause various

EEMG responses, which become the background for the usage

of EEMG monitoring for intraoperative facial nerve functional

evaluation and prediction for outcomes. Our previous in vitro

study found that the amplitude of contraction of orbicularis

oris was more sensitive to inhibition by the non-depolarizing

muscle relaxant rocuronium if the innervating facial nerve

was injured [5]. However, the relationships between EEMG

responses, the sensitivity to muscle relaxants, and the extent

of facial nerve injury have not been reported.

Therefore, we used an in vivo rabbit model of graded facial

nerve injury [9] to compare the inhibitory effects and inhibi-

tory time of rocuronium on EEMG recordings taken from the

orbicularis oris (represents facial nerve innervated muscles)

and gastrocnemius muscles (represents somatic nerve

innervated muscles). We aimed to draw inferences about the

best means of balancing the need for EEMG monitoring and

muscle relaxation during general anesthesia for patients with

preexisting facial nerve injury, where somatic neuromuscular

function is generally monitored with a peripheral nerve

stimulator.

2. Materials and methods

2.1. Animal model and experimental protocol

The study was approved by the Ethics Committee of Shanghai

Jiaotong University (Shanghai, China). Seventy-two New

Zealand rabbits (Experimental Animal Centre of the School of

Medicine, Shanghai Jiaotong University, Shanghai, China) of

both genders, weighing 2e2.5 kg, were fasted but allowed to

have free access to water for 12 to 18 h prior to surgery. The

first procedure consisted of a left facial nerve injury, induced

by using the crush axotomymodel by means of vessel clamps

[9]. Briefly, the rabbits were anesthetized by an intramuscular

injection of ketamine 40 mg/kg and diazepam 5 mg/kg. A

2.0e2.5 cm curvilinear incisionwasmade just below the lower

eyelid. The superficial facialmuscleswere divided sharply and

the buccal branch of the facial nerve was exposed. A crush

was made at the middle point of the buccal branch of the left

facial nerve. A standard crush using the same batch of vessel

clamps was performed for a defined amount of time causing

one of the graded injuries according to the Sunderland

method [10], in which crushing for 30 s results in a grade I

injury, 60 s a grade II injury, and 120 s a grade III injury. Finally,

the wound was closed using 4-0 skin sutures (Ethicon; John-

son & Johnson Medical (China) Ltd, Shanghai, China). Success

was assessed on the basis of damage to facial nerve functions

on the left side, which includes ipsilateral impairment of the

blink reflex, altered orientation of the vibrissae, and mouth

drooping after recovery from anesthesia. After surgery, all

rabbits were allowed free access to water and food for 7e42 d

prior to the second procedure. At the end of all experiments,

animals were euthanized by overdose anesthetics. Tissue

samples from the same segments of the injured facial nerves

were obtained from each rabbit to check the integrity of the

facial nerve by pathologic examination using the modified

trichrome staining technique under light microscopy (oil

immersion objective at �400 magnification). The structurally

intact contralateral facial nerve was used as a control for

comparison.

All rabbits were randomly divided into three groups con-

taining 24 rabbits each, according to the designated degree of

injury: groups DI (grade I injury) to DIII (grade III). Subse-

quently, each group was divided into four subgroups con-

taining six rabbits each, in which the EEMG monitoring was

performed 7, 14, 28, and 42 d after the facial nerve injury. In

addition, six rabbits underwent sham surgery with the left

facial nerve exposed without crushing.

2.2. Recording of EEMG responses

At the designed point in the protocol for each group of rabbits,

animals were anesthetized by an intravenous injection of

pentobarbital 25 mg/kg, followed by an infusion at 10e15 mg/

kg/h to maintain anesthesia. Rabbits were then placed supine

on the operating table and mechanically ventilated (respira-

tion frequency 40 breaths/min, tidal volume 12 mL/kg, inspir-

ation:expiration ratio 1:2) by an animal respirator (model

DHX-150; Chengdu Instrument Plant, China). Bilateral orbicu-

laris oris muscles innervated by the buccal branches of the

facial nerve and the right gastrocnemiusmuscle innervated by

the tibial nerve were exposed. The EEMG was recorded sim-

ultaneously for the three muscles with a bioelectric signals

processing system (model SMUP-PC; Jide experimental ins-

trument factory, Shanghai, China). Briefly, a recording pin

electrode was inserted into each muscle and connected to the

system. The nerves were stimulated with a single supra-

maximal train of rectangular pulses (4 V, duration 0.2ms). The

pulse was repeated four times at 2.0 Hz at 2-s intervals and the

mean EEMG amplitude of the corresponding muscle was

calculated. The muscle relaxant rocuronium (Organon Com-

pany, Oss, The Netherlands) was then administered intrave-

nously at a dose of 0.18 mg/kg (2 � ED90 in rabbits [11]) to each

animal after stable EEMG recordings had been obtained for at

least 30 min. Both baseline EEMG and EEMG responses at 1, 10,

15, 20, 25, 30, and 35 min after rocuronium injection, respec-

tively, were recorded for each group of muscles.

Changes in EEMG amplitude in each muscle group were

expressed as the absolute value and the proportion of

j o u r n a l o f s u r g i c a l r e s e a r c h 1 8 5 ( 2 0 1 3 ) 1 9 8e2 0 5200

inhibition expressed as a percentage (EEMG%). The onset time

and the recovery time of rocuronium were also recorded. The

time at which maximal EEMG inhibition was observed was

defined as the onset time; the time at which EEMG recovered

to 95% of the baseline measurement was defined as the

recovery time. The time that EEMG% recovered from the 75%e

25% of the maximum extent of inhibition was expressed as

TEEMG75e25%. A time-effect curve was obtained by setting the

EEMG or EEMG% as the ordinate and the time elapsed from

injection of rocuroniumas the abscissa for eachmuscle group.

2.3. Data analysis

All data are presented as the mean � standard deviation and

were analyzed using the SPSS 17.0 statistical software package

(SPSS Inc, Chicago, IL). The paired t test was used to compare

between the each injured facial nerve and the normal control

groups, respectively. The intra-group and the inter-group

mean values were analyzed by randomized block analysis of

the variance,whereas the differences between any two groups

were identified by the Student-Newman-Keul test and Dun-

nett’s T3 test for heterogeneity of variance. Correlation anal-

ysis of the EEMG in response to rocuroniumwith the extent of

facial nerve injury was undertaken using Spearman’s test. A P

value < 0.05 was considered to be a statistically significant

difference.

3. Results

3.1. Histopathologic examination of injured facial nerve

Group DI was found to have approximately normal morpho-

logical appearance, with an integrated perineurium and

axonal continuity and well-distributed aligned myelin

sheaths in cross section, with a small amount of demyelin-

ation at all time points. Group DII exhibited patchy loss of

myelin sheaths with intact nerve bundles at 7 d; swollen

axons, thickened perineurium, and obvious demyelination at

14e28 d; and thinning perineurium, fewer Schwann cells and

fibroblasts, but some remyelination at 42 d after injury. In

group DIII, at 7 d the nerve bundle was intact but the intima

had disintegrated with substantial thinning of the myelin

sheath and blistered and vacuolar degenerative axons; by 14 d

the myelin sheath had almost completely disaggregated with

almost as severe as axonal disaggregation resulting in barely

recognizable nerve bundles; and at 28e42 d post-injury there

was a certain amount of irreversible neuronal degeneration

accompanied by different extents of remyelination and axon

regeneration (Fig. 1). These findings are in accordancewith the

characteristics of grade I to grade III nerve injury described by

Sunderland [10].

3.2. EEMG changes observed

According to the preliminary results, the sample size should

extend to at least five animals for each subgroup. Our study

fulfilled the prescribed power. The baseline EEMG of facial

nerve-innervated orbicularis oris was significantly smaller

than those of the tibial nerve-innervated gastrocnemius. The

baseline EEMG recordings of grade II- and III-injured facial

nerve-innervated orbicularis oris were significantly smaller

than normal controls at all time points; those of grade I-

injured muscles were not significantly different from controls

(Fig. 2AeD). In the presence of rocuronium the EEMG ampli-

tude in all muscle groups was significantly reduced

(Fig. 2AeD), although the maximum extent of inhibition

(maximum EEMG%) in the gastrocnemius was significantly

greater than that of the orbicularis oris innervated by either

normal or any grade of damaged facial nerve (Fig. 3AeD).

There was no significant difference in the onset or recovery

times among themuscle groups innervated by the tibial nerve

and intact or any grade of damaged facial nerves at any

recovery time. The TEEMG75-25%of muscles innervated by the

tibial nerve was shorter than muscles innervated by facial

nerves, but there was no significant difference found between

normal or damaged facial nerve (Table).

At 7 d after nerve crush, no significant difference was

found between EEMG amplitude values after rocuronium in

orbicularis oris innervated by DIeDIII-injured facial nerves

(Fig. 2A). At 14 d post-injury and at 15 min after rocuronium

administration, the EEMG amplitude values of group DIII were

significantly smaller than those of group DI; by 30 and 35 min

after administration, these had become significantly smaller

than those of DI and DII (Fig. 2B). By 28 d post-injury, the EEMG

amplitude values of group DIII were significantly smaller than

those of group DI 15 min after rocuronium administration

(Fig. 2C). By 42 d, the EEMG amplitudes recorded in group DIII

were significantly smaller than those of groups DI and DII 20,

25, and 30 min after rocuronium (Fig. 2D). However, no

significant differences were found in EEMG% between the

normal and all grades of facial nerve injury after rocuronium

administration at each time course (Fig. 2AeD). The EEMG% of

gastrocnemius was significantly greater than the normal and

denervated orbicularis oris 1e20 min after rocuronium

administration (Fig. 3AeD). None of the baseline EEMG values

or EEMG responses after rocuronium administration, or the

onset or recovery times of rocuronium, was significantly

different between the injured and contralateral facial nerve-

innervated orbicularis oris in the sham operated group.

At any given time, the baseline EEMG and amplitude of

EEMG of injured facial nerve-innervated orbicularis oris in the

presence of rocuronium was negatively correlated with the

grades of facial nerve injury (Figs. 4 and 5), while EEMG% in

with rocuronium was not correlated with the grades of facial

nerve injury. At the same grades of injury, the baseline EEMG

and EEMG amplitude of injured facial nerve-innervated orbi-

cularis oris in the presence of rocuronium was not signifi-

cantly correlated with recovery time (P > 0.05).

4. Discussion

This study was an evolution of our previous research, which

showed that the EEMG of the facial nerve was detectable and

recordable even when complete neuromuscular blockade of

the limb was established. This suggests that there is a distinct

difference in sensitivity to non-depolarizing muscle relaxants

between muscles innervated by the facial nerve and those

innervated by the ulnar nerve [4]. Further animal research in

Fig. 1 e Histopathologic examination of normal and injured facial nerve by modified trichrome staining under an oil

immersion objective (3400 magnification). (A), (B), (C), and (D): Sunderland grade I injured facial nerve after 7, 14, 28, and

42 d. Little injury is evident with intact perineurium and axonal continuity between the neuron and muscle evident; (E), (F),

(G), and (H): grade II injured facial nerve after 7, 14, 28, and 42 d: some demyelination can be observed; (I), (J), (K), and (L):

grade III injured facial nerve after 7, 14, 28, and 42 d: axonal regeneration is impaired by intrafunicular fibrosis, which

obstructs or diverts them from their proper paths. (Color version of figure is available online.)

j o u r n a l o f s u r g i c a l r e s e a r c h 1 8 5 ( 2 0 1 3 ) 1 9 8e2 0 5 201

a rat model of facial nerve injury found that inhibition of the

electrical stimulation-evoked muscular tension amplitude

(MTA), which reflected the muscle’s contractile force, by

Fig. 2 e Evoked electromyography amplitude values of the norm

and after a 23 ED90 dose of rocuronium (*P< 0.05, DIII versus DI

versus orbicularis oris, ◎P< 0.05, normal orbicularis oris versus D

is available online.)

rocuronium was greater in gastrocnemius than orbicularis

oris, confirming that muscles innervated by somatic nerves

are more sensitive to neuromuscular blockade than those

al, injured side orbicularis oris, and gastrocnemius before

and DII; 6P< 0.05, DI versus DIII, yP< 0.05, gastrocnemius

II- and DIII-injured orbicularis oris). (Color version of figure

Fig. 3 e Evokedelectromyographyamplitude inhibitionof thenormal, injuredorbicularis oris andgastrocnemiusbefore andafter

the 23 ED90 dose of rocuronium (yP< 0.05, gastrocnemius versus orbicularis oris). (Color version of figure is available online.)

j o u r n a l o f s u r g i c a l r e s e a r c h 1 8 5 ( 2 0 1 3 ) 1 9 8e2 0 5202

innervated by facial nerve [5]. However, no significant differ-

ence in the proportion of MTA inhibition in the muscle

innervated by normal or injured facial nerve was seen even

though the absolute MTA values in muscle innervated by

injured nerve were significantly smaller than uninjured

controls at any dose of rocuroniumeindicating that the

sensitivity to muscle relaxants was not influenced by nerve

injury [5]. In the original protocol of that research, we had

planned to record MTA and EEMG as outcome measures for

neuromuscular conduction, but EEMG proved impracticable

because of strong artefacts from laboratory equipment. We

designed this protocol using the same method of EEMG

monitoring in a rabbit model of facial nerve injury of different

severity and chronicity to mimic the clinical situation more

closely. Clinically, the ulnar nerve innervated adductor polli-

cis is usually used for the monitoring for muscle relaxation in

anesthetic management, which represents the extent of

skeletal muscle neuromuscular blockade. Both orbicularis

muscle and orbicularis oris are usually used for intraoperative

facial nerve EEMG monitoring, which reflects the extent of

facial nerve neuromuscular blockade. Considering that the

isolation and monitoring of orbicularis muscle and adductor

pollicis is hardly in practice in rabbits, we choose the orbicu-

laris oris (represents facial nerve innervated muscles) and

gastrocnemius (represents somatic nerve innervatedmuscles)

to simulate the clinical situation.

The findings of this study show that the EEMG inhibition of

gastrocnemius by rocuronium was greater than that of orbi-

cularis oris, which was in accordance with our previous study

and several others [12]. The results of this study that facial

nerve injuries (grade II and III) reduced EEMG amplitude in

orbicularis oris comparedwith controls, but that no difference

was found in the EEMG% in response to rocuronium also

support the previous findings in vitro and other models [13,14].

However, in this study we found a relationship between the

extent of facial nerve injury and the magnitude of the reduc-

tion in EEMG baseline and amplitude in the presence of

rocuronium: EEMG amplitude was lower the more severe the

nerve injury. However, there was no difference in the EEMG%

in response to rocuronium between injured and uninjured

groups, indicating that nerve injury influences the ability of

a muscle to contract but not the sensitivity of its neuromus-

cular junction to muscle relaxants.

Our finding that there was no difference in the onset and

recovery times of rocuronium in normal or injured facial nerve

groups is at odds with some other reports [15,16]. Recovery

index (RI) is an indicator of the rate of skeletal muscle recov-

eryeessentially, the difference between the time to recovery to

25% and time to recovery to 75% of the baseline value, but as

maximum inhibition did not reach 75% in orbicularis oris we

could not calculate RI. We defined the TEEMG75e25% as an

outcome measure of neuromuscular recovery and found that

the gastrocnemius takes less time to recover than the orbicu-

laris oris at our chosen dose of rocuronium. The choice of drug

mighthaveplayedapart, asdifferences in facial andperipheral

neuromuscular blockade have been shown to vary with

different relaxants and doses [17]. Beside, the choice of

different muscles, different monitoring methods or factors

thatmight influence themetabolismand absorption ofmuscle

relaxants such as blood flow, oxygen consumption and work

output may also be the reasons included [18,19]. Finally, we

would argue that EEMG amplitude is amore clinically relevant

outcomemeasure than onset and recovery times.

Explanations for the observed differences in sensitivity

to rocuronium between the facial- and somatic nerve-

innervated muscle groups might be differences in the

density of acetylcholine receptors (AChR) at motor end-plates

or a different affinity of AChRs to muscle relaxants [5], while

Table e Onset time, recovery time and TEEMG75%e25% of normal orbicularis, Sunderland IeIII injured orbicularis andgastrocnemius under 2 3 ED90 of rocuronium.

Muscles Injured degree Recoverytime (day)

Onset time (sec) Recoverytime (min)

TEEMG75e25% (min)

Gastrocnemius 18.14 � 4.34 37.72 � 9.20 7.05 � 0.99*

Normal side orbicularis oris 21.75 � 4.51 36.87 � 9.20 9.29 � 0.83

Injured side orbicularis oris I 7 18.75 � 3.05 39.91 � 10.45 9.42 � 0.68

14 21.74 � 2.08 36.48 � 9.59 9.38 � 0.66

28 20.77 � 3.10 38.37 � 8.16 9.64 � 0.87

42 18.33 � 4.66 39.49 � 11.00 9.21 � 0.54

II 7 21.03 � 1.66 30.72 � 4.51 9.20 � 0.80

14 21.84 � 2.67 38.90 � 4.28 9.36 � 0.47

28 22.38 � 3.74 36.19 � 9.90 9.42 � 0.64

42 18.13 � 4.84 42.66 � 10.22 9.25 � 0.59

III 7 18.15 � 3.30 31.24 � 7.19 9.38 � 0.71

14 19.43 � 6.34 40.79 � 7.21 9.37 � 0.79

28 21.47 � 1.22 33.35 � 10.95 9.16 � 0.91

42 19.83 � 5.36 44.56 � 10.23 9.41 � 0.66

* P < 0.05, gastrocnemius versus normal and injured side orbicularis oris.

j o u r n a l o f s u r g i c a l r e s e a r c h 1 8 5 ( 2 0 1 3 ) 1 9 8e2 0 5 203

the differences in the contractile responses between muscles

innervated by intact and injured facial nerve might have

arisen from a relatively lower AChR density at end-plates. The

lack of variability in the sensitivity to rocuronium might be

due to a proportionally similar occupation of the residual

AChRs in the injured neuromuscular junction to those in the

normal neuromuscular junction, resulting in a proportionally

similar inhibition of contraction. Another explanation is that

an injury dependent reduction in end-plate AChR density is

matched by the proportional occupation of the residual AChRs

by muscle relaxants. The 50% inhibitory concentration (IC50)

of non-depolarizing muscle relaxants at neuromuscular

nicotinic AChRs is much higher in denervated skeletal

muscles, a finding that might be due to altered proportions of

ε- and g-AChR subtypes [20].

Fig. 4 e The correlation analysis of the baseline EEMG of DI-III in

0.05), at 14 d (r [ L0.787, P < 0.01); at 28 d (r [ L0.611, P < 0.

available online.)

Unexpectedly, the EEMG responses in nerve injury were

not affected by the chronicity of the injury, which is not

consistent with our clinical experience and other reports [21].

Histopathological findings were consistent with our expecta-

tions of graded severity of injury and with the original

description by Sunderland [10], but the relatively normal

appearance of grade I injuries might account for the lack of

variance in EEMG responses when compared with controls.

According to Weber, if the nerve had only been stretched and

not seriously bruised or torn, then there might be complete

return of function within 6 weeks, but with a more severe

stretch and some bruising the nerve could still recover in

about 3 months [22]. We chose a 42 day time period to match

Weber’s stretch injury, but if the crush injury were more

severe (grade II-III) recovery could be expected to be less

jured muscles at each post-injury time course. At 7 d (P >01); at 42 d (r [ L0.59, P < 0.05). (Color version of figure is

Fig. 5 e The correlation analysis of the EEMG of DI-III injuredmuscles at maximum inhibition at each post-injury time point.

At 7 d (P > 0.05); at 14 d (r [ L0.472, P < 0.05); at 28 d (r [ L0.611, P < 0.01); at 42 d (P > 0.05). (Color version of figure is

available online.)

j o u r n a l o f s u r g i c a l r e s e a r c h 1 8 5 ( 2 0 1 3 ) 1 9 8e2 0 5204

complete and take longer. In a pigmodel of facial nerve repair,

grafts that were undertaken 21 days after injury to coincide

with the peak of neuronal cell-body metabolic activity were

found to be no more likely to succeed [23]. Other studies have

reported a mismatch between the physiological and the

pathological characteristics of recovery; for example, the

symptoms of facial nerve paresis could resolve within

6 months while the restoration of a normal EEMG response

might take up to 18 months [2,24]. Moreover, it has been re-

ported that other parameters for EEMG monitoring, such as

proximal stimulation threshold and proximal-to-distal

response amplitude ratio, are more suitable for predicting

long-term facial nerve dysfunction than amplitude values [3]

Therefore, conclusions cannot be drawn about time-related

EEMG changes and the effect of muscle relaxants after facial

nerve injury until studies that include longer observation and

monitoring periods are conducted or alterative detection

techniques are available.

In summary, the somatic neuromuscular junction appears

to be more sensitive to muscle relaxants than the neuro-

muscular junction in the face, supporting the hypothesis that

the partial neuromuscular blockade of the somatic muscles is

a suitable strategy for muscle relaxant use in surgery

requiring EEMG monitoring. The extent of pre-existing facial

nerve injury influences themagnitude of the EEMG responses,

but not the sensitivity tomuscle relaxants. In clinical practice,

extra caution should be paid when muscle relaxants are used

during surgery requiring EEMG monitoring and there is

a possibility that facial nerve function is already impaired. The

results of the study could help to get a point at which a balance

between somatic nerve innervatedmuscle relaxation required

when a patient is under general anesthesia and facial nerve

innervated muscle response required for facial nerve

monitoring could be maintained, including the normal and

different degrees of pre-surgical injured facial nerves.

Acknowledgment

This study is supported by the National Natural Science

Foundation of China, grant number 81271075. The authors

declare no conflict of interest.

r e f e r e n c e s

[1] Goldbrunner RH, Schlake HP, Milewski C, Tonn JC, Helms J,Roosen K. Quantitative parameters of intraoperativeelectromyography predict facial nerve outcomes for vestibularschwannoma surgery. Neurosurgery 2000;46:1140. discussion1146.

[2] Meier JD, Wenig BL, Manders EC, Nenonene EK. Continuousintraoperative facial nerve monitoring in predictingpostoperative injury during parotidectomy. Laryngoscope2006;116:1569.

[3] Dhonneur G, Kirov K, Motamed C, et al. Post-tetanic count atadductor pollicis is a better indicator of early diaphragmaticrecovery than train-of-four count at corrugator supercilii. Br JAnaesth 2007;99:376.

[4] Cai YR, Xu J, Chen LH, Chi FL. Electromyographic monitoringof facial nerve under different levels of neuromuscularblockade during middle ear microsurgery. Chin Med J 2009;122:311.

[5] ZhouRY, Xu J, Chi FL, Chen LH, Li ST. Differences in sensitivityto rocuronium among orbicularis oris muscles innervated bynormal or damaged facial nerves and gastrocnemius muscle

j o u r n a l o f s u r g i c a l r e s e a r c h 1 8 5 ( 2 0 1 3 ) 1 9 8e2 0 5 205

innervated by somatic nerve in rats: combinedmorphologicaland functional analyses. Laryngoscope 2012;122:1831.

[6] Ibebunjo C, Srikant CB, Donati F. Morphological correlates ofthe differential responses of muscles to vecuronium. Br JAnaesth 1999;83:284.

[7] Ibebunjo C, Hall LW. Muscle fibre diameter and sensitivity toneuromuscular blocking drugs. Br J Anaesth 1993;71:732.

[8] Aimoni C, Lombardi L, Gastaldo E, Stacchini M, Pastore A.Preoperative and postoperative electroneurographic facialnerve monitoring in patients with parotid tumors. ArchOtolaryngol Head Neck Surg 2003;129:940.

[9] Cai Z, Yu G, Ma D, Tan J, Yang Z, Zhang X. Experimentalstudies on traumatic facial nerve injury. J Laryngol Otol 1998;112:243.

[10] Sunderland S. A classification of peripheral nerve injuriesproducing loss of function. Brain 1951;74:491.

[11] Gyermek L, Lee C, ChoYM,NguyenN, Tsai SK. Neuromuscularpharmacology of taac3, a new nondepolarizing musclerelaxant with rapid onset and ultrashortultra-short durationof action. Anesth Analg 2002;94:879.

[12] Hemmerling T, Schmidt J, Hanusa C, Wolf T, Schmitt H.Simultaneous determination of neuromuscular block at thelarynx, diaphragm, adductor pollicis, orbicularis oculi, andcorrugator supercilii muscles. Br J Anaesth 2000;85:856.

[13] Donati F, Meistelman C, Plaud B. Vecuronium neuromuscularblockade at the adductor muscles of the larynx and adductorpollicis. Anesthesiology 1991;74:833.

[14] Hemmerling T, Donati F. Neuromuscular blockade at thelarynx, the diaphragm and the corrugator supercilii muscle:a review. Can J Anaesth 2003;58:779.

[15] Osawa T. Different recovery of the train-of-four ratio fromrocuronium-induced neuromuscular blockade in thediaphragm and the tibialis anterior muscle in rat. J Anesth2008;22:236.

[16] Michalek-Sauberer A, Gilly H, Steinbereithner K, Vizi ES.Effects of vecuronium and rocuronium in antagonisticlaryngeal muscles and the anterior tibial muscle in the cat.Acta Anaesthesiol Scand 2000;44:503.

[17] Rimaniol JM, Dhonneur G, Sperry L, Duvaldestin P. Acomparison of the neuromuscular blocking effects ofatracurium, mivacurium, and vecuronium on the adductorpollicis and the orbicularis oculi muscle in humans. AnesthAnalg 1996;83:808.

[18] Pansard JL, Chauvin M, Lebrault C, Gauneau P, Duvaldestin P.Effect of an intubating dose of succinylcholine andatracurium on the diaphragm and the adductor pollicismuscle in humans. Anesthesiology 1987;67:326.

[19] Robertson CH Jr, Pagel MA, Johnson RL Jr. The distribution ofblood flow, oxygen consumption, and work output amongthe respiratory muscles during unobstructedhyperventilation. J Clin Invest 1977;59:43.

[20] Wang H, Yang B, Xu YF, Yan T, Li ST. Different magnitude ofresistance to nondepolarizing muscle relaxants in thedenervated mouse skeletal muscle. Acta Pharmacol Sin 2010;31:399.

[21] Weber, RA, Dellon AL. Nerve lacerations: repair of acuteinjuries, Hand Surgery 1st ed. Philadelphia: LippincottWilliams & Wilkins. Available at: http://www.msdlatinamerica.com/ebooks/HandSurgery/sid620432.html;2004.

[22] Barrs DM. Facial nerve trauma: optimal timing for repair.Laryngoscope 1991;101:835.

[23] Eaton DA, Hirsch BE, Mansour OI. Recovery of facial nervefunction after repair or grafting: our experience with 24patients. Am J Otolaryngol 2007;28:37.

[24] Isaacson B, Kileny PR, El-Kashlan HK. Prediction of long-termfacial nerve outcomes with intraoperative nerve monitoring.Otol Neurotol 2005;26:270.