Bell palsy (BP) is an acute unilateral lower motor neuron facial paralysis. It is responsible for about 75% of cases of acute unilateral facial paralysis1 . It is one of the most common neurologic disorders of the cranial nerves. About 30% of patients have a poor outcome; however, most patients show good outcome2 .
A nerve conduction study has been commonly used to evaluate the function of the motor and sensory nerves of the human body, especially the ability of electrical conduction, and also used to predict the prognosis of nerve diseases such as Bell palsy.3
The usage of ultrasound (US) is of proven efficacy in carpal tunnel syndrome, ulnar neuropathy, and femoral neuropathy; it is capable of demonstrating structural lesions along the course of the affected nerve4 . To our knowledge, few studies have been conducted prospectively using US in BP5,6;US is a new approach for assessment of BP in comparison to known electrophysiological techniques.
This study aimed to assess the role of US in correlation with nerve conduction studies and clinical assessment in predicting the prognosis of Bell palsy.
MATERIALS AND METHODS
This is a prospective case–control study conducted on 20 patients with acute BP recruited from the outpatient clinic of the Neurology Department, Faculty of Medicine, Cairo University, between November 2014 and May 2015. The study received approval from the ethics committee of Kasr Al-Ainy Faculty of Medicine, Cairo University.
All patients were examined within a two-week period from the onset of the disease. Their ages ranged from 12 years or above to ensure their ability in making facial expressions. They had no other neurologic symptoms and were clinically free from any ear, nose, or throat diseases.
Patients with recurrent BP and secondary facial palsy causes (eg., patients with diabetes) were excluded from the study.
The healthy other side of the same 20 patients served as the control group.
After selection of the participants, the purpose of the study was adequately explained to each participant.
Informed consent was taken from all patients regarding all the steps of both the neurophysiological study and US imaging.
All patients were submitted to clinical examination using the House–Brackmann scale that categorize BP on a scale of (I-VI) and facial nerve NCs, and US were performed for the affected side at onset and followed up 1 month later, and for the normal side only at onset.
After careful facial assessment, we used the House–Brackmann (HB) grading system—which is valid to evaluate new and existing patients—as follows7: grade I; normal facial function, grade II; mild dysfunction, grade III; moderate dysfunction, grade IV is moderately severe dysfunction, grade V is severe dysfunction, and grade VI is total paralysis.
Nihon Kohden Neuropack M1 machine, JAPAN, at the Clinical Neurophysiology Unit, Faculty of medicine, Cairo University, was used for neurophysiological study.
The NCs was performed by stimulation of the facial nerve terminal branches (zygomatic, temporal, and buccal) and recording compound muscle action potentials (CMAP) from the facial muscles supplied by these branches.
Recording was performed by placing the active electrode on the ipsilateral muscle (nasalis, orbicularis oculi, or orbicularis oris), reference electrode placed on the contralateral muscle, ground electrode placed at the back of the hand, the stimulating electrode placed below the ear and anterior to the mastoid process, or directly over the stylomastoid foramen. The intensity we used was approximately 50 to 100uV. The conduction time and the amplitude of the CMAP of the three muscles were measured.
The original study included the three muscles mentioned but, in this article, we chose the nasalis muscle only for simplification and to be more precise in reviewing the results.
PHILIPS IU22 xMATRIX, California, US, L7-10 transducer, using 9-MHz linear array transducer, was used for neurosonological study by a certified neurosonographer (N.S.C.H) at the Neurosonology Unit, Neurology department, Faculty of Medicine, Cairo University.
The subject is made to lie in the supine position with the head turned to the left or right, laterally. The transducer is placed transversely at the level of common carotid artery and then moved to follow external carotid artery and its branches medially. Color Doppler was used to avoid confusion with the facial artery that lies deep to the facial nerve. The transducer at this point is perpendicular to the facial nerve that runs anterior to the styloid process, then the transducer is tilted to be parallel to the posterior ramus of the mandible to avoid the angle of the mandible, with minimal pressure exerted by the probe. The acoustic shadow of the mastoid process can be visualized posteriorly and the mandibular ramus anteriorly. The probe's orientation marker directed to the sonographer's left side is taken into consideration.8
The facial nerve is now in the longitudinal view and can be identified at the mastoid region (as it emerges from the stylomastoid foramen before it enters the parotid gland substance and divides into five terminal branches). At this level, we freeze and zoom the picture and take the three measurements (most proximal, most distal, and in between). The facial nerve diameter is then measured inside the hyperechoic neurolemmal borders.
The normal facial nerve has a relatively hyperechoic neurolemma compared with the surrounding masseter muscle (which lies below and anterior to the nerve) and exhibits a linear mono-fascicular appearance. By contrast, the abnormal facial nerve is often swollen (Fig. 1).5 , 9
The three diameters were taken 3 times, and the mean was calculated to be used in the statistical analysis.
Data were statistically described in terms of mean ± standard deviation (SD), median and range, or frequencies (number of cases) and percentages when appropriate. Comparison between diseased side and control side was performed using Wilcoxon signed-rank test for paired (matched) samples. Correlation between various variables was performed using Pearson moment correlation equation for linear relation in normally distributed variables and Spearman rank correlation equation for non–normal variables/nonlinear monotonic relation. A multivariate analysis model was used to test for the significant independent predictors of the prognosis. The ROC curve was constructed with the area under the curve analysis performed to detect the best cutoff value of NCs and US for detection of a good prognosis. P values less than 0.05 was considered statistically significant. All statistical calculations were performed using computer program SPSS (Statistical Package for the Social Science; SPSS Inc, Chicago, IL) release 15 for Microsoft Windows (2006).
Table 1 showed the participants' demographic, clinical, neurophysiological, and neurosonological results of the affected side at onset and follow-up.
There was significant lower amplitude of the CMAP recorded from the nasalis muscle only in the affected side (P = 0.003); however, there was no significant difference in latency between the affected and healthy sides. As regards the facial US (proximal, midway, and distal segments), there were highly significant differences between the mean of the affected side (proximal segment = 1.2 ± 0.4 mm, mid segment = 1.0 ± 0.4 mm, and distal segment = 0.9 ± 0.3 mm) and the healthy side (P value < 0.001) (Table 2).
HB Grading Score
The difference between the HB grading score at the onset of the disease and follow-up after one month from onset showed a highly significant value (P value < 0.001) (Table 2).
The comparison of the amplitude of nasalis-CMAP of the affected side at onset and follow-up showed significant difference (P value < 0.05). The latency showed no significant difference between the affected side at onset and follow-up (Table 2).
The comparative data of facial US diameters (proximal, midway, and distal segments) between the affected sides at onset and follow-up showed significant statistical difference (P value < 0.05) (Table 2).
There were significant positive correlations between the clinical HB grades at follow-up with onset HB (Table 3).
There is no significant correlation between the US diameter of any of the three segments and the percentage of degeneration at the onset of the disease, whereas at follow-up, the mid-segment diameter showed significant positive correlation with the percentage of degeneration (p value < 0.05, r = 0.47).
Predictability of Prognosis
The area under the curve analysis was performed to detect the best cutoff value of NCs for prediction of good outcome (clinical grade at follow-up ≤ 3) using the nerve conduction study. It showed that latencies and amplitudes of CMAP recorded from the nasalis muscle only at the onset of polyscan predicts good outcome (Table 4) (Fig. 2).
Initial US cannot predict the prognosis. This was measured using the mean of the three segments of US as in Table 4. The patients' data were divided into two groups; one with those having clinical grade at follow-up 1,2, or 3 and the other one with those having clinical grade at follow-up four or more using ROC curve.
This study was mainly concerned with BP outcome and the investigation that gives an impression on its prognosis in one-month duration, which may have a great implication on management, especially rehabilitation and early surgical interference. The one-month review period was chosen to ensure good patients' contact and compliance during the follow-up.
In our study, there was a significant positive correlation between onset and follow-up HB grading; this means that the cases with mild clinical manifestations had improvement chances better than those who manifested severely. Previous studies also concluded that the most important factor in the prognosis of Bell palsy is the clinical severity of the patient's initial condition. Generally, patients whose paralysis is less severe tend to recover more completely.10 , 11
In the current study, we tested the ability of initial US to predict the outcome and it was unable to help in prediction, whereas the amplitude of the CMAP recorded from the nasalis muscle was able to predict the outcome.
This is contradictory to the study conducted by Lo et al.,5 which showed that US is better than NCs in detecting the prognosis of BP after 3 months from onset. Normal US on the affected side had a 100% positive predictive value, whereas NCs showed a value of 72% to 80%. Abnormal facial nerve US had a negative predictive value of 77% if House–Brackmann scale was Grade II or worse, which was again higher than that of the nerve conduction studies (25% to 35%). The main difference between this study and the study by Lo is the timing of follow-up.
Tawfik et al. (2015)6 showed a low sensitivity (75%) and specificity (70%) of facial nerve US, suggesting that facial nerve US may have a limited role in prognosis.
Inflammation of the facial nerve evidenced by lymphocytic infiltrates and edema has been established as a pathogenic mechanism of Bell palsy.12 The edema leads to nerve entrapment and consequent ischemia because of the blockage of the vasa nervorum. Despite the known pathogenesis, the cause of inflammation, segmental location of entrapment, and management of the disease remains controversial.13
Operative findings and contrast-enhanced MRI have demonstrated that nerve swelling and enhancement occur at/or proximal to the facial canal rather than distally.14 , 15 , 16 But as US does not have the ability to examine the nerve within its anatomic site of entrapment, the current study localized the facial nerve swelling at the mastoid region, which goes in accordance with that reported by Lo et al.5 The significant reduction of facial nerve diameter at follow-up may reflect part of the pathogenesis of Bell palsy, which improves after a period of adequate therapy.5 , 2
Lack of correlation between the HB clinical grading, NCs percentage of degeneration, and US diameter at the onset of BP is an interesting point. Facial nerve fibers are a rapid conducting one17 and prove to be highly sensitive to minor injury.18 The minimal increased diameter of the facial nerve, which could be contributed to edema, increased blood flow, or any other pathologic causes may lead to thinning of the myelin sheath around the nerve and so, decreasing the conduction through it, which then results in increased degeneration in a manner that does not match with diameter change. After treatment, this thinning of the myelin sheath becomes less, and conduction regains its function in relation to the entire nerve diameter. At follow-up; the percentage of degeneration became correlated to the US diameter of the mid-segment and added valuable information about the severity and the outcome of BP because the extent of the nerve damage can determine the extent of its outcome.1 The study by Prakash and Raymond19 showed a strong positive correlation between facial nerve percentage of degeneration and the clinical outcome of Bell palsy at one and even after 2 months from onset. However, the increase in US diameter could not specify the nature of nerve fiber degeneration (demyelination/axonal) compared with NCs.20
It was noted that the diameter on the diseased side of some patients falls in the upper limit of normal diameters or equal to the mean normal diameter. This applies to the mid and the distal facial diameters. Those patients were mostly with mild clinical symptoms. According to the House–Brackmann (HB) grading system, at onset, 10% of cases, and at follow-up, 70% of the patients, were with mild to moderate affection. This reflects the poor prognostic utility of US
In our study, the zooming technique during measurement of the facial nerve diameter was performed for all cases, for both affected and control sides, at onset and follow-up to overcome its effect. The affection of the zoom function on the results of facial nerve diameter needs to be assessed, however, it would be difficult to re-assess all cases before and after zooming. This will be a good idea for the next research. Also, assessment of facial nerve vascularity is missing in our study.
In the current study, the correlation for clinical improvement was based on data obtained from the nasalis muscle only. Although the original study included the three muscles (o.oculi, o.oris, and nasalis), in this article, we chose the nasalis muscle only for simplification and to be more precise in reviewing the results because our main aim was to study the role of US in correlation with nerve conduction studies and clinical assessment in predicting the prognosis of Bell palsy.
Other limitations that were detected during the study include the following: small sample size, one half of the patients refused to do electromyogram and electromyographic examination because they were afraid of needle insertion, and follow-up after a one-month duration only.
Baseline HB clinical grade is the most important predictor of BP outcome. Initial NCs of nasalis muscles are superior to the measurement of facial nerve diameter by US in predicting the outcome prognosis. Further research is recommended to show the value of facial nerve US in predicting prognosis.
1. Peitersen E. Bell's palsy; the spontaneous course of 2,500 peripheral facial nerve
palsies of different etiologies. Acta Otolaryngol Suppl 2002;549:4–30.
2. Sullivan FM, Swan IR, Donnan PT, et al. Early treatment with prednisolone or acyclovir in Bell's palsy. N Engl J Med 2007;357:1598–1607.
3. Hayder KH, Musa MM, Ajeena IM, Mahmood AA. Role of Neurophysiology in predicting poor outcome in Bell's palsy. Kufa Med J 2009;12:84–90.
4. Beekman R, Schoemaker MC, vander JP. Diagnostic value of high-resolution sonography in ulnar neuropathy at the elbow. Neurology 2004;62:767–773.
5. Lo YL, Fook-Chong S, Leoh TH, et al. High-resolution ultrasound
in the evaluation and prognosis
of Bell's palsy. Eur J Neurol 2010;17:885–889.
6. Tawfik EA, Walker FO, Cartwright MS. A pilot study of diagnostic neuromuscular ultrasound
in Bell's palsy. J Neuroimaging 2015;25:564–570.
7. Vrabec JT, Backous DD, Djalilian HR, et al. Facial nerve
grading system. Otolaryngol Head Neck Surg 2009;140:445–450.
8. Tawfik EA. Sonographic characteristics of the facial nerve
in healthy volunteers. Muscle Nerve 2015;52:767–771.
9. Tawfik EA, Walker FO, Cartwright MS. Neuromuscular ultrasound
of cranial nerves. J Clin Neurol 2015;11:109–121.
10. Aoyagi M. Accuracy of the prognostic diagnosis in acute peripheral facial palsy. Nihon Jibiinkoka Gakkai Kaiho 2005;108:1–7.
11. Yeo SW, Lee DH, Jun BC, Chang KH, Park YS. Analysis of prognostic factors in Bell's palsy and Ramsay Hunt syndrome. Auris Nasus Larynx 2007;34:159–164.
12. Liston SL, Kleid MS. Histopathology of Bell's palsy. Laryngoscope 1989;99:23–26.
13. Vianna M, Adams M, Schachern P, Lazarini PR, Paparella MM, Cureoglu S. Differences in the diameter of facial nerve
and facial canal in Bell's palsy—a 3-dimensional temporal bone study. Otol Neurotol 2014;35:514–518.
14. Fisch U, Esslen E. Total intratemporal exposure of the facial nerve
. Pathologic findings in Bell's palsy. Arch Otolaryngol 1972;95:335–341.
15. Sartoretti-Schefer S, Kollias S, Wichmann W, Valavanis A. T2-weighted three-dimensional fast spin-echo MR in inflammatory peripheral facial nerve
palsy. Am J Neuroradiol 1998;19:491–495.
16. Kim IS, Shin SH, Kim J, Lee WS, Lee HK. Correlation between MRI and operative findings in Bell's palsy and Ramsay Hunt syndrome. Yonsei Med J 2007;48:963–968.
17. Thurner KH, Egg G, Spoendlin H, Schrott FA. A quantitative study of nerve fiber in the human facial nerve
. Eur Arch Otorhinolaryngol 1993;250:161–167.
18. Fujimura Y, Yokoyama K, Araki S, Murata K. Changes in the distribution of nerve conduction velocities in diabetics. Tohoku J Exp Med 1996;178:177–185.
19. Prakash KM, Raymond AA. The use of nerve conduction studies in determining the short-term outcome of Bell's palsy. Med J Malaysia 2003;58:69–78.
20. Beekman R, Visser LH. Sonography in the diagnosis of carpal tunnel syndrome: a critical review of the literature. Muscle Nerve 2003;27:26–33.
Keywords:© 2018 by the American Clinical Neurophysiology Society
Bell palsy; Facial nerve; Ultrasound; Nerve conduction study; Prognosis; House–Brackmann scale