A novel muscle for electroneurography in peripheral facial palsy: occipitalis

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1 DOI /s x HEAD AND NECK A novel muscle for electroneurography in peripheral facial palsy: occipitalis Nurten Uzun Turgut Adatepe Elad Azizli Zeynep Alkan Özgür Yiğit Ayşegül Gündüz Feray Karaali-Savrun Received: 7 January 2015 / Accepted: 17 February 2015 Ó Springer-Verlag Berlin Heidelberg 2015 Abstract Electroneurography (ENoG) is one of the most objective tests in grading the damage and prediction of prognosis in peripheral facial palsy (PFP). We aimed to determine temporal changes of ENoG recorded over occipitalis muscle in acute idiopathic PFP. Consecutive 21 patients with unilateral acute idiopathic PFP and age- and sex-matched 15 healthy volunteers were included in the study. Nasal and occipital ENoG values were recorded once in the control group and the same procedure was repeated daily between the second and eight days of the disorder in the PFP group. Occipital ENoG value began to increase on the third day while nasal ENoG value was still within the normal range (27.04 vs 7.69 %, p = ). In the fourth, fifth and sixth days, occipital ENoG value was significantly high compared to nasal ENoG value (p = for each day) whereas nasal and occipital ENoG values were very similar in the seventh and eighth days (p = and p = 0.584, respectively). Our study Results were previously presented in the XXth International SFEMG and QEMG Course, XIIth QEMG Conference. 2 6 June N. Uzun (&) A. Gündüz F. Karaali-Savrun Department of Neurology, I.U. Cerrahpasa Medical Faculty, Cerrahpasa School of Medicine, Istanbul University, K.M.Pasa, Istanbul, Turkey nurtenznctf@gmail.com; nurtenzn@yahoo.com T. Adatepe Department of Electromyography Laboratory, Istanbul Training and Research Hospital, Istanbul, Turkey E. Azizli Z. Alkan Ö. Yiğit Department of Otorhinolaryngology, Istanbul Training and Research Hospital, Istanbul, Turkey presents further support for technical possibility of occipital ENoG which may reflect the degree of fiber degeneration earlier than the nasalis muscle in PFP. Keywords Nasalis muscle Occipitalis muscle Electroneurography Peripheral facial paralysis Introduction Peripheral facial palsy (PFP) is the most commonly encountered cranial neuropathy and when a thorough diagnostic work-up reveals no specific etiology, it is labeled as acute idiopathic facial nerve palsy, or Bell s palsy. The vast majority of patients in this group are generally treated with a steroid and/or antiviral regimen. Grading the damage and prediction of prognosis in PFP have a role in deciding and scheduling various treatment options since in selected cases decompression surgery may be considered as an option. There are several procedures which are traditionally known to predict prognosis [1]. Each of these tests has its own advantages and disadvantages in evaluation of facial nerve degeneration. Although none of them alone predicts prognosis definitely, electroneurography (ENoG) is one of the most objective and the most commonly used tests [2]. In predicting prognosis by ENoG, compound muscle action potentials (CMAPs) of bilateral facial nerves are recorded using the same facial muscle and the ratio of paralyzed CMAP value over the healthy side multiplied by 100 shows the percentage of facial nerve degeneration. The minimum critical value suggesting unfavorable prognosis is 90 %, above which recovery is incomplete and development of synkinesis secondary to aberrant regeneration is highly possible [3].

2 Nasalis muscle is known as the most appropriate muscle for ENoG. Although other facial mimic muscles have also been suggested, CMAPs recorded over nasalis muscle were found to more correctly predict prognosis [4]. However, nasal ENoG is not able to predict the prognosis until the end of the first week [5]. Occipitalis muscle forms the posterior part of the occipito-frontal muscle which is innervated by posterior auricular branch of facial nerve after its exit from the stylomastoid foramen [6]. It extends between occipital protuberance and mastoid process and aponeurosis. Since occipital branch is shorter than the zygomatic branch, we hypothesized that occipital ENoG may reflect the prognosis earlier than nasal ENoG in PFP. Therefore, we aimed to determine the changes of morphology, latency and amplitude of CMAP recorded over occipitalis muscle and role of ENoG recorded over occipitalis muscle in predicting prognosis in acute idiopathic PFP. Patients and method Patients This is prospective electrophysiological study which included consecutive 21 patients with unilateral acute idiopathic PFP (47.6 % male; mean age, 39.8 ± 13.9 years) and age- and sex-matched 15 healthy volunteers (46.7 % male; mean age, 34.7 ± 9.0 years) between September 2011 and December Detailed clinical evaluation specific to facial nerve functions using House Brackmann scale (HBS) [7] and electrophysiological investigations were performed once in the control group and same procedures were repeated daily between the second and eight days of the disorder in the PFP group. Subjects with craniofacial anomaly, previous history of PFP, and history of any systemic or neurological diseases were excluded. All participants gave informed consent. This study was approved by the Institutional Review Board. Electrophysiological examinations All investigations were performed under similar conditions in a quiet room while patients were in supine position (Neurosoft Micro 2 channels, Russia) by the same senior neurologist experienced in electrophysiology (TA). Ipsilateral nasal and occipital CMAPs were recorded simultaneously. The recordings over nasalis muscles were made in accordance with previously published reports [8]. Briefly, the active and reference electrodes were placed on the bilateral nasolabial grooves close to the ala nasi, and the ground electrode on the forehead. For occipital ENoG, active recording electrode was placed over the midpoint on the imaginary line between external auditory meatus pore and external occipital protuberence (inion) while reference electrode was located 3 cm rostral to this point on the vertical line. Ground electrode was placed on mastoid process. Figure 1 demonstrates recording technique of ENoG over the two muscles. A single square wave electrical stimulus of 0.2 ms duration was applied percutaneously by bipolar superficial electrodes. Increasing intensity of the stimulus, 110 % of the intensity inducing the maximum response amplitude was considered as the supramaximal intensity. The filter settings were 3 khz high cut and 3 Hz low cut. Analysis time was adjusted as 1 2 ms/div and amplitude sensitivity was 1 2 mv. Statistical analysis Onset latency (ms) and peak to peak amplitudes (mv) of CMAP responses were measured and the maximum response over each muscle was included in the analysis. Ratio of the remaining intact motor axons on the affected side in the patient group was calculated using the following formula: Ratio of the remaining intact motor axons CMAP of paralyzed side ¼ CMAP of healthy side 100 ENoG value is defined as follows: Ratio of the degenerated nerve fibers = Ratio of the remaining intact motor axons [9]. Data analyses were performed using the SPSS 11.5 software statistical package. Mean values of CMAP amplitudes and latencies were calculated for right-sided and left-sided responses over each muscle in healthy subjects and for responses over healthy sides in patient group. Mean differences of rightsided and left-sided nasal CMAP as well as occipital CMAP were calculated. Occipital and nasal ENoG values at each investigation day (2, 3, 4, 5, 6, 7 and 8) in PFP group were compared with the respective ENoG values of healthy subjects using the Student t test since the data distributed homogenously. Occipital and nasal ENoG values at each investigation day were also compared with each other within the patient group using the Student t test. p value \0.05 was set to be significant. Results The clinical facial nerve function at first presentation was HB grade II in seven patients, grade III in nine patients and IV in five patients.

3 Fig. 1 a Electrode positioning of facial motor response recording over nasalis muscle. b Electrode positioning of facial motor response recording over occipitalis muscle. (Electrodes: black active, red reference and yellow ground) We obtained consistent responses over occipitalis muscle similar to nasalis. There were no artifacts and stimulation was not painful for any of the participants. Response morphologies of nasalis and occipitalis CMAPs were similar to each other in healthy subjects, specifically consistent biphasic waveform shape. Mean amplitudes of right- and left-sided nasalis CMAPs were 3.16 and 3.17 mv, respectively. The mean difference between the two sides was 3.6 %. Mean amplitudes of occipitalis CMAPs were also similar, 3.97 and 3.99 mv, respectively. Mean difference between the two sides was minimal: 4.8 % in healthy subjects. Healthy sides of patient group also showed consistent responses with pattern and morphology similar to healthy subjects. On the second day of PFP showed that mean nasal and occipital ENoG values in patients were similar to those in healthy subjects (p = and p = 0.382, respectively). On the third day, ENoG values began to increase: 7.69 % for nasal response and % for occipital response. After the third day, both nasal and occipital ENoG values were significantly high compared to healthy subjects (p = for each investigation day). Occipital ENoG values were significantly greater compared to nasal ENoG values in the third, fourth, fifth and sixth days (p = , Fig. 2) whereas nasal and occipital ENoG values were very similar in the seventh and eighth days (p = and p = 0.584, respectively). Figures 3 and 4 demonstrates more evident and earlier reduction of CMAP amplitude recorded over occipital muscle in representative examples of PFP subjects. Discussion Our study supports that occipital ENoG is technically possible and reliable to use in PFP. It may even reflect fiber degeneration earlier than the recording over nasalis muscle. The technique described in our study is reproducible and easy to perform, and stimulation anterior to external acoustic pore is painless. There are several reasons for using occipitalis muscle. First, branch of facial nerve innervating this muscle is the shortest one among the branches to the facial muscles [6]. Second, isolated localization of occipitalis muscle [6] compared to crowded alignment of other facial nerve innervated muscles decreases the possibility of spread of CMAP response from neighboring muscles. Other reasons can be listed as follows: (i) remote distance of stimulation site to the muscle decreases the possibility of stimulation artifact, (ii) the larger surface area of occipitalis muscle and its tendon facilitates the placement of electrodes, decreases the risk of misplacement of electrodes, (iii) the tendon is stabilized in the bony calvarium, therefore it does not move decreasing the risk of artifacts and providing responses with smooth morphology. Relatively larger surface area of occipitalis muscle compared to the nasalis muscle may result in much higher CMAP amplitudes over the former one. However, we did not observe such a high difference. CMAPs recorded over occipitalis muscle were well-shaped with very similar amplitudes to nasal CMAPs in our study population. ENoG values for previously established sites are considered as normal till 20 % as this degree of difference between the two sides may normally occur due to asymmetries or errors in electrode placement [10]. Neurophysiological investigations are required in PFP for several reasons: determination of underlying pathological process, localization of the lesion, or prediction of prognosis. In the very first few days, electrically evoked BR or transpetrosal facial nerve conduction studies provide reliable information regarding the localization of lesion and prediction of prognosis. ENoG is considered as the most convenient method, mostly valuable in the tenth day of the disease on average in determining the ratio of axon loss and

4 Fig. 2 Graphical representation of temporal change of occipital and nasal ENoG values Fig. 3 Motor response recorded over occipitalis (upper two traces) and nasalis (lower two traces) muscles in a female PFP subject on second (a) and third (b) investigation days (1 and 3 traces represent the paralyzed side) predicting the prognosis [1]. It was also reported to be the most useful method in selection of cases for decompression surgery in idiopathic PFP [11, 12]. The most commonly used muscle for ENoG is nasalis, however, ENoG was obtained consistently over other muscles like over orbicularis oculi, frontalis, orbicularis oris, mentalis and even stylohyoid and posterior digastricus muscle complex muscles [13 16]. Temporal change of ENoG was also similar in these muscles [13]. Prediction of prognosis is designated according to the ENoG value, 90 % of which indicates a significant risk for permanent damage to the facial nerve with incomplete recovery [17, 18]. A study predicted irreversible damage with 77.8 % specificity and 71.4 % sensitivity when ENoG values were higher than 85 % [19]. Tojima and colleagues reported early prediction of prognosis in the sixth and seventh days using ENoG and certain other techniques [20]. Reduction of amplitude by 35 % within 2 days or loss of CMAP in the fourth or fifth day examinations suggested total degeneration and unfavorable prognosis. At least two serial investigations should be done in PFP. First, ENoG investigation is recommended to be performed in the third day of the disease and second examination should follow within 1 3 days [21]. Thomander and colleagues [22]

5 Fig. 4 More evident reduction of motor response amplitude recorded over occipitalis muscle (upper two traces) compared to nasalis muscle (lower two traces) in a male PFP subject on fourth (a) and sixth (b) investigation days. (1 and 3 traces represent the paralyzed side) succeeded to predict prognosis in the fourth day of the disease in 70 % of patients using automatically signal analysis method. Our study showed statistical significance between the ENoG values of different facial muscles from the third to sixth day which disappeared in the seventh and eighth day investigation. Therefore, we may claim that nasal and occipital ENoG investigations revealed similar ratios of axon loss in the end which is considered as reasonable time to perform nasal ENoG. Assuming the nasal ENoG investigation as the gold standardized method of predicting axonal loss within the given period, we report that occipital ENoG determines and predicts the real value of axon loss at an earlier time which is probably related to the shorter distance from the facial nerve to the muscle since daily progression of axon loss is inversely proportional to the distance between lesion site and muscle. There are some limitations of the study. The number of the patient population is relatively small. Widespread use of this simple method may lead to reports with larger populations. A second limitation of the study is sole inclusion of subjects with incomplete facial paralysis. ENoG is primarily used in cases of complete PFP. Study of the characteristics of the occipital ENoG in cases of complete PFP is required. In summary, occipital ENoG may reflect nerve fiber degeneration earlier than the nasal ENoG. The method is easy to perform. Therefore, we recommend recordings over occipitalis muscles in addition to nasalis recordings in cases of PFP. Authors thank Pasa Basar for excellent techni- Acknowledgments cal assistance. Conflict of interest References None. 1. Valls-Solé J (2007) Electrodiagnostic studies of the facial nerve in peripheral facial palsy and hemifacial spasm. Muscle Nerve 36: Sittel C, Stennert E (2001) Prognostic value of electromyography in acute peripheral facial nerve palsy. Otol Neurotol 22: Esslen E (1973) Electrodiagnosis of facial palsy. In: Miehlke A (ed) Surgery of the facial nerve. W. B. Saunders, Philadelphia, pp Smith IM, Murray JA, Prescott RJ, Barr-Hamilton R (1988) Facial electroneurography. Standardization of electrode position. Arch Otolaryngol Head Neck Surg 114: Tojima H, Aoyagi M, Inamura H, Koike Y (1994) Clinical advantages of electroneurography in patients with Bell s palsy

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