Journal of Clinical Neuroscience 22 (2015) 659–663
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical Study
Hearing outcomes after loss of brainstem auditory evoked potentials during microvascular decompression Parthasarathy D. Thirumala a,b,⇑, Balaji Krishnaiah c, Miguel E. Habeych a, Jeffrey R. Balzer a, Donald J. Crammond a a b c
Department of Neurological Surgery, University of Pittsburgh Medical Centre, Suite B-400, 200 Lathrop Street, Pittsburgh, PA 15213, USA Department of Neurology, University of Pittsburgh Medical Centre, Pittsburgh, PA, USA Department of Neurology, Penn State Hershey Medical Center, Hershey, PA, USA
a r t i c l e
i n f o
Article history: Received 3 October 2014 Accepted 15 October 2014
Keywords: Brainstem auditory evoked potential Hearing loss Hemifacial spasm Microvascular decompression
a b s t r a c t The primary aim of this paper is to study the pre-operative characteristics, intra-operative changes and post-operative hearing outcomes in patients after complete loss of wave V of the brainstem auditory evoked potential. We retrospectively analyzed the brainstem auditory evoked potential data of 94 patients who underwent microvascular decompression for hemifacial spasm at our institute. Patients were divided into two groups – those with and those without loss of wave V. The differences between the two groups and outcomes were assessed using t-test and chi-squared tests. In our study 23 (24%) patients out of 94 had a complete loss of wave V, with 11 (48%) patients experiencing transient loss and 12 (52%) patients experiencing permanent loss. The incidence of hearing loss in patients with no loss of wave V was 5.7% and 26% in patients who did experience wave V loss. The incidence of hearing change in patients with no loss of wave V was 12.6% and 30.43% in patients who did experience wave V loss. Loss of wave V during the procedure or at the end of procedure significantly increases the odds of hearing loss. Hearing change is a significant under-reported clinical condition after microvascular decompression in patients who have loss of wave V. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction Hemifacial spasm (HFS) is an involuntary twitching or contraction of the facial muscles on one side of the face. The most common cause of HFS is vascular compression of the facial nerve by the anterior inferior cerebellar artery at the root exit zone. Microvascular decompression (MVD) of cranial nerve (CN) VII is an effective treatment for HFS [1]. An infrequent but significant risk of MVD is hearing loss (HL) [2]. HL occurs at a rate of 7.7–20% in HFS [3,4] caused by iatrogenic injury to CN VIII. There are multiple mechanisms that can injure CN VIII during MVD including stretching of CN VIII when retracting the cerebellum, manipulation of the compressing vessel, and direct trauma by instruments [5]. More importantly any subtle changes to hearing after MVD have been infrequently reported [4]. The use of intra-operative brainstem auditory evoked potential (BAEP) monitoring has substantially decreased the incidence of post-operative HL [6]. Studies have reported that latency and amplitude changes of wave I and wave
⇑ Corresponding author. Tel.: +1 412 648 2228; fax: +1 412 383 9899. E-mail address: [email protected] (P.D. Thirumala). http://dx.doi.org/10.1016/j.jocn.2014.10.009 0967-5868/Ó 2014 Elsevier Ltd. All rights reserved.
V of the BAEP are the most useful predictors of post-operative HL [7–9]. Complete loss of BAEP waveforms is an uncommon event during MVD, which causes significant anxiety to the surgeon and the monitoring team. However to our knowledge no study has evaluated the patients who had a loss of wave V during MVD; this could provide valuable information during the procedure in addition to its prognostic potential. The primary aim of this paper is to study the pre-operative characteristics which may increase the incidence of loss of wave V in addition to analyzing the intra-operative changes and post-operative outcomes in these patients.
2. Patients and methods 2.1. Patient selection A retrospective analysis was performed in patients who underwent MVD for HFS between January 2000 and December 2007 at the University of Pittsburgh Medical Center. We included 94 patients who had been diagnosed with HFS pre-operatively based on electromyographic testing, who had pre and post-operative hearing function documentation and those who had BAEP
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responses at baseline during surgery. We excluded patients with poor pre-operative hearing function. The study was approved by the Institutional Review Board for retrospective review of data on human subjects at the University of Pittsburgh (MOD0812039404/PRO08120394). The surgical steps during MVD for HFS have been discussed in detail in previous publications by this group [10–13]. In brief the nerve was decompressed from its cross compressing arterial loop and then the conflicting vessel was separated by means of a pledget made of soft Teflon felt fibers (DuPont, Wilmington, DE, USA) [1]. 2.2. Pre-operative auditory investigations An audiologic examination was performed in all patients before (median 1 day, range 1–16 days) and after surgery (median 7 days, range 2–16 days), consisting of an audiogram, pure tone thresholds measurement (air and bone conduction for octave frequencies 250 to 8000 Hz) and speech discrimination scores, which were considered to be the predictors of auditory function [5,6]. Pre-operative tympanometry and acoustic reflex thresholds were also obtained to detect any conduction abnormality. 2.3. Intra-operative BAEP monitoring All patients undergoing MVD had continuous intra-operative BAEP monitoring. The right or left ears were stimulated independently, using alternating rarefaction and condensation clicks with at least an 85 decibel above normal adult hearing level (dBnHL) intensity level. The BAEP responses were recorded on the side of the procedure. A stimulus rate of 17.5 Hz was used. White noise was applied to the contralateral ear at 65 dBnHL. The observation interval was 12 ms. At least 512 responses were averaged for each epoch. The recording electrodes were positioned as follows: Ch1 = vertex to left ear mastoid (Cz/A1); Ch2 = vertex to right mastoid (Cz/A2); and Ch3 = vertex to cervical C2 (Cz/Cv2). Amplifier bandpass was 100–1000 Hz for all channels. Baseline BAEP responses were obtained after anesthesia induction and patient positioning. Lateral spread response was obtained for all patients to evaluate the efficacy of decompression [11]. Physician oversight and interpretation was performed using a combined on-site and remote model utilized at the University of Pittsburgh Medical Center [14]. Consistent decreases in amplitude of greater than 50% of wave V were considered clinically significant [4,15,16]. 2.4. Analysis of neurophysiological parameters For this study, wave V was marked for analysis at the following times during surgery: (1) baseline, after intubation and positioning of the patient; (2) during dural opening; (3) at change start, when the first consistent decrease in the amplitude of wave V >50% and/ or increase in the latency of wave V >0.5 ms compared to baseline was noted, (4) when the last recordable amplitude and or latency changes before complete loss of wave V were recorded, and (5) at skin closure. We also analyzed changes as being either transient or a permanent abolition of wave V of BAEP. Transient loss of wave V is defined as loss of waveform V during MVD and subsequent reestablishment of a measurable response later during surgery. A permanent loss is defined as wave V being lost and not returning for the entire duration of the procedure. If the waveforms were lost, latency was recorded as 12 ms which is the maximum observation time and the amplitude was recorded as zero for analytical purposes. We divided patients into two groups, with Group I being patients with no loss of wave V and Group II being patients with loss of wave V during or at the end of the procedure. We also analyzed wave I and wave III of BAEP in patients during the procedure.
2.5. Post-operative auditory testing and HL criteria Both pure tone thresholds measurement and speech discrimination scores were re-tested after surgery (median 7 days, range 2–16 days). To avoid misinterpretation of audiometric findings, otoscopy and tympanometry was also performed to detect middle ear dysfunction, which may be due to fluid entering the mastoid air cells and or bone dust deposition during craniotomy. An air–bone conduction gap identified in the speech range of frequencies determined post-operative conductive HL status [17]. We compared both pre and post-operative pure tone thresholds measurement and speech discrimination scores, and classified post-operative HL using the American Academy of Otolaryngology–Head and Neck Surgery criteria [4,18]. Using the post-operative audiogram data and speech discrimination scores patient hearing was divided into three categories, being Category A = no hearing change, Category B = hearing change HC) including altered but useful hearing or serviceable hearing loss, and Category C = non-serviceable hearing loss, that is, HL not amenable to hearing aids (Table 1). 2.6. Statistical analysis Statistical analyses were performed using the Statistical Package for the Social Sciences version 20 (SPSS, Chicago, IL, USA). Continuous variables were presented as mean ± standard deviation and categorical variables as frequency (%). The differences in demographic and operative characteristics were compared between the two groups and outcomes were assessed using t-tests and chi-squared tests. p < 0.05 was considered statistically significant. Univariate logistic regression analysis was done to evaluate the effect of loss of wave V of BAEP responses during the procedure and at the end of the procedure on post-operative HL.
Table 1 Demographics and comparison of clinical characteristics between Group I (no wave V loss) and Group II (transient or permanent wave V loss) Variable
Group I
Group II
Patients, n
71
23
p value
Sex Male Female
22 (30%) 49 (70%)
11 (47.82%) 12 (52.17%)
0.14
Side Left Right
38 (53.52%) 33 (46.47%)
16 (69.56%) 7 (30.43%)
0.176
Botulinum toxin treatment Used by patient Multiple injections
47 (66.19%) 38 (53.52%)
17 (73.91%) 17 (73.91%)
0.01 0.02
Pre-operative symptom Decreased corneal reflex Tinnitus Decreased hearing Tonus Platysma involvement
17 (23.94%) 4 (5.64%) 8 (11.26%) 40 (56.33%) 33 (46.47%)
5 (21.70%) 0 2 (8.69%) 16 (69.56%) 9 (39.13%)
0.50 0.96 0.404 0.50 0.15
Offending vessel AICA PICA VA Unnamed artery Vein Perforator Average time to maximum change, hour:min:s
35 (49.29%) 30 (42.25%) 17 (23.94%) 9 (12.6%) 0 (42.25%) 9 (12.6%) 01:13:10
10 (43.47%) 10 (43.47%) 4 (5.63%) 4 (5.63%) 11 (47.8%) 2 (8.69%) 01:02:08
0.77 0.50 0.31 0.04 0.50 0.92 0.61
Total duration of surgery, hour:min:s
01:51:53
01:55:06
0.48
AICA = anterior inferior cerebellar artery, min = minutes, PICA = posterior inferior cerebellar artery, VA = vertebral artery. Bold indicates a statistically significant result.
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3. Results
3.3. Neurophysiological analysis
3.1. Demographics
In the present study 23 out of 94 (24%) patients had complete loss of wave V, of whom 11 (48%) patients had transient loss and 12 (52%) had permanent loss. Of the patients with transient loss of wave V all 11 had significant latency increases which did not improve to baseline values at the end of surgery (measured at the time of skin closure). Five patients with transient wave V loss had significant decreases in amplitude that did not return to baseline at the end of surgery. The remaining four patients had insignificant decreases in amplitude at the end of surgery compared to baseline. Two patients with transient wave V loss had a decrease in amplitude during surgery but their amplitude recovered back to baseline. All patients in Group II with HL had a significant decrease in wave V amplitude, but never recovered to normal baseline values. Of the 23 Group II patients, six had measureable latency and amplitude of wave III despite wave V loss. Among them, four (67%) patients had no HL and three out of these four had transient loss of wave V. Three patients had total loss of wave I along with wave III and V. All three patients did not have any improvement in BAEP waveforms at the end of the procedure. Two of the patients who lost all waveforms had HL and the other had normal hearing.
In this study we analyzed the BAEP data of 94 patients and compared the pre-operative characteristics, intra-operative changes and post-operative outcomes between Group I (n = 71) and Group II (n = 23) patients. 3.2. Pre-operative characteristics and intra-operative findings In our study 64 (70.42%) out of 94 patients had received botulinum toxin treatment prior to surgery with 54 (58.51%) patients having received multiple botulinum injections prior to MVD. A majority (70.7%) of patients had multiple compressing vessels. Compression was caused mainly by the anterior inferior cerebellar artery, posterior inferior cerebellar artery, vertebral artery, and some bridging veins in both groups. Mean time taken for surgery was 02:00 hours in Group I and 01:55 hours for Group II. Average time taken for maximum change in Group I was 01:13 hours and 01:02 hours for Group II. There was no statistically significant difference between two groups when comparing demographics such as age, sex, side of operation, pre-operative symptoms and operative characteristics like duration of surgery and time to maximum change (Table 2). Patients in Group II had a significantly higher usage of pre-operative botulinum toxin injection for HFS treatment (p = 0.01) than those in Group I.
3.4. Hearing analysis The incidence of HL in patients with transient (two out of 11) and permanent loss (four out of 12) of wave V was 18% and 33%, respectively. The incidence of HC in patients with transient (three out of 11) and permanent (four out of 12) loss of wave V was 27% and 33%, respectively (Fig. 1). In Category A we had 58 Group I patients and 10 Group II patients (six had transient and four had permanent wave V loss). In Category B we had nine Group I patients and seven Group II patients (three had transient and four had permanent loss of wave V). In category C we had four Group I patients and six Group II patients (two had transient and four had permanent loss of wave V). There was a significantly higher incidence of HC and HL in Group II patients (p = 0.05) (Table 3). Regression analysis shows that patients who have a loss of wave V during the procedure and experience persistent loss of wave V are more than seven times more likely to have HL as compared to patients who did not experience a loss of wave V (Table 4).
Table 2 Correlation of wave V latency at various stages of surgery between Group I (no wave V loss) and Group II (transient or permanent wave V loss) Time point
Wave V latency, ms
Baseline (after induction) Dural opening Change start Change maximum last recorded On skin closure
Group I (n = 71)
Group II (n = 23)
p value
6.49 ± 0.38 6.71 ± 0.47 7.10 ± 0.47 8.05 ± 1.24 7.23 ± 0.87
6.52 ± 0.28 6.57 ± 0.32 7.06 ± 0.40 8.01 ± 0.62 10.03 ± 2.18
0.46 0.10 0.84 0.29 >0.001
Data are presented as mean ± standard deviation. Bold indicates a statistically significant result.
23 Paents with loss of wave V 12 paents with permanent loss
4( 17%) paents had HC
4(17%) had HL
11 paents with trasient loss 4 paents had no HL
2 paents had returned back to baseline amplitude both the paents had no HL
4 paents had Insignificant changes in amplitude on skin that did not return to baseline 1 paent had no HL, 2 had HC, 1 had HL
5 paents had significant decrease in amplitude and not returned to baseline
3 had no HL, I had HC, 1 had HL
Fig. 1. Hearing change and hearing loss pattern in patients with loss of wave V during microvascular decompression. HC = hearing change, HL = hearing loss.
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Table 3 Correlation of wave V amplitude at various stages of surgery between Group I (no wave V loss) and Group II (transient or permanent wave V loss) Time point
Wave V latency (ms)
Baseline (after induction) Dural opening Change start Change maximum last recorded On skin closure
Group I (n = 71)
Group II (n = 23)
p value
0.35 ± 0.11 0.35 ± 0.16 0.33 ± 0.11 0.21 ± 0.08 0.29 ± 0.11
0.32 ± 0.12 0.31± 0.19 0.33 ± 0.14 0.21 ± 0.10 0.08 ± 0.10
0.79 0.72 0.79 0.47 0.49
Data are presented as mean ± standard deviation.
Table 4 Results of regression analysis for loss of response of wave V and the risk of hearing loss Loss of wave V
During procedure At the end of procedure
Odds ratio
7.444 6.667
95% confidence interval Lower limit
Upper limit
1.694 1.509
32.175 29.448
4. Discussion Our results indicate that loss of wave V significantly increases the incidence of HL and HC, which to our knowledge has not been previously reported. The number of patients (24%) who experience a loss of wave V during MVD and suffer subsequent HL is similar to previously published results. Grundy et al. [8] demonstrated hearing was preserved if waveforms were intact or if only transient loss was encountered, but if waveform V was permanently abolished hearing was invariably lost. Similarly Allen et al. [19] showed that no hearing impairment (all five cases) was seen in patients with transient wave loss, but two out of three patients who had permanent wave V loss had HL. Raudzen and Shetter [7] reported that intra-operative BAEP were unchanged throughout surgery in 34 patients (74%) and these individuals had no post-operative hearing deficit. Four patients had loss of all BAEP waveforms and this correlated to deafness or HL. In a study performed by Polo et al. [6] there was a 33% rate of HL when wave V was abolished permanently. Our results indicate increased HC in patients who had a loss of wave V during MVD. Transient stretching of a cranial or peripheral nerve can result in temporal dispersion with or without conduction block resulting in drop in amplitude of the response. The generator of wave V, the inferior colliculus, is several synapses more distal along the auditory pathway. Therefore a change in wave V is a cumulative desynchronization of BAEP responses over one or two synapses that decreases the overall strength, that is, each synapse has an additional threshold for synaptic integration of multiple afferents. In some cases the potential generated at the cochlea and travelling in the auditory nerve is severely dispersed leading to a recording of wave III but a loss of wave V, as observed in our study. Improvement in the amplitude after complete loss, as seen in BAEP during MVD, can occur without permanent injury to the nerve [20]. In acute conditions where pressure of high magnitude has been directly applied to a nerve trunk, the resulting disturbances in nerve function are based mainly upon the effect of myelin damage. The redistribution of tissue from compressed to non-compressed levels of the nerve is associated with invagination of the myelin sheaths at the nodes of Ranvier [21,22]. The resulting myelin damage is associated with partial or complete local conduction block and it is usually reversible. Based on nerve stretch studies a permanent loss of wave V of BAEP could be caused by complete infarction
of the peripheral nerve, and transient loss might be due to ischemia which improved after the end of the surgery. Changes in the amplitude and latency of BAEP secondary to stretching clearly seem to affect post-operative hearing outcomes, including both HL and HC. Wave I of BAEP originates from the auditory nerve, an area that is not vulnerable during surgery. Three of our patients displayed a loss of wave I. This may be attributed to manipulation of the labyrinthine artery and/or anterior inferior cerebellar artery during surgery, leading to reversible ischemia or infarction of the cochlea [5]. We had patients who had no hearing dysfunction despite loss of wave V on BAEP. Similar findings were reported by Broggi et al. [23] who suggested that the abolition of wave V with preservation of wave I may be associated with good post-operative hearing function. It is possible these patients had a neuropraxic injury of CN VIII which improved after the end of the surgical procedure. Furthermore, in our study, use of pre-operative botulinum toxin was associated with loss of wave V during MVD. Botulinum toxin treatment is a common, transient treatment for HFS as its effects are at the level of the neuromuscular junction. In our patients the exact etiopathogenesis of the loss of wave V and its association with increased use of botulinum toxin is unclear. Previous studies which analyzed changes in the latency changes of wave V identified prolongation in latency of 1.5 ms, 1.0 ms and 0.5 ms as alarms to warn the surgeon of impending injury to CN VIII [8,16,24]. However Friedman et al. [9] have suggested that simple prolongations of wave I, III and V latencies do not correlate with post-operative hearing deficits. Loiselle and Nuwer [25] commented that overreliance upon arbitrary warning criteria invites inaccuracy, which leads to increased patient risk. Hence the currently recommended alarm criteria [26,27] need to be robustly evaluated before being widely accepted as a standard to warn the surgeon of an impending loss of waveform. Although our study was limited because of its retrospective nature and lack of long-term follow-up audiograms, we highlight a very important clinical change in hearing function with loss of wave V during MVD. 5. Conclusion Loss of wave V during MVD significantly increases the odds of HL. HC is a significant under-reported condition after MVD in patients who have loss of wave V. Pre-operative use of botulinum toxin injection was significantly higher in patients with loss of wave V during MVD. More than half of patients with no HL despite wave V loss during MVD had transient loss of wave V. Alarm criteria need to be developed to predict and prevent the loss of wave V during MVD. Conflicts of Interest/Disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication. References [1] Jannetta PJ, Abbasy M, Maroon JC, et al. Etiology and definitive microsurgical treatment of hemifacial spasm. Operative techniques and results in 47 patients. J Neurosurg 1977;47:321–8. [2] Little JR, Lesser RP, Lueders H, et al. Brain stem auditory evoked potentials in posterior circulation surgery. Neurosurgery 1983;12:496–502. [3] Rizvi SS, Goyal RN, Calder HB. Hearing preservation in microvascular decompression for trigeminal neuralgia. Laryngoscope 1999;109:591–4. [4] Shah A, Nikonow T, Thirumala P, et al. Hearing outcomes following microvascular decompression for hemifacial spasm. Clin Neurol Neurosurg 2012;114:673–7. [5] Sindou MP. Microvascular decompression for primary hemifacial spasm. Importance of intraoperative neurophysiological monitoring. Acta Neurochir (Wien) 2005;147:1019–26 [discussion 1026].
P.D. Thirumala et al. / Journal of Clinical Neuroscience 22 (2015) 659–663 [6] Polo G, Fischer C, Sindou MP, et al. Brainstem auditory evoked potential monitoring during microvascular decompression for hemifacial spasm: intraoperative brainstem auditory evoked potential changes and warning values to prevent hearing loss–prospective study in a consecutive series of 84 patients. Neurosurgery 2004;54:97–104 [discussion 104–6]. [7] Raudzens PA, Shetter AG. Intraoperative monitoring of brain-stem auditory evoked potentials. J Neurosurg 1982;57:341–8. [8] Grundy BL, Jannetta PJ, Procopio PT, et al. Intraoperative monitoring of brainstem auditory evoked potentials. J Neurosurg 1982;57:674–81. [9] Friedman WA, Kaplan BJ, Gravenstein D, et al. Intraoperative brain-stem auditory evoked potentials during posterior fossa microvascular decompression. J Neurosurg 1985;62:552–7. [10] Thirumala PD, Ilangovan P, Habeych M, et al. Analysis of interpeak latencies of brainstem auditory evoked potential waveforms during microvascular decompression of cranial nerve VII for hemifacial spasm. Neurosurg Focus 2013;34:E6. [11] Thirumala PD, Shah AC, Nikonow TN, et al. Microvascular decompression for hemifacial spasm: evaluating outcome prognosticators including the value of intraoperative lateral spread response monitoring and clinical characteristics in 293 patients. J Clin Neurophysiol 2011;28:56–66. [12] Wang X, Thirumala PD, Shah A, et al. Microvascular decompression for hemifacial spasm: focus on late reoperation. Neurosurg Rev 2013;36:637–43 [discussion 643–4]. [13] Wang X, Thirumala PD, Shah A, et al. The role of vein in microvascular decompression for hemifacial spasm: a clinical analysis of 15 cases. Neurol Res 2013;35:389–94. [14] Thirumala PD, Kassasm AB, Habeych M, et al. Somatosensory evoked potential monitoring during endoscopic endonasal approach to skull base surgery: analysis of observed changes. Neurosurgery 2011;69:ons64–76 [discussion ons76]. [15] Ramnarayan R, Mackenzie I. Brain-stem auditory evoked responses during microvascular decompression for trigeminal neuralgia: predicting postoperative hearing loss. Neurol India 2006;54:250–4.
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[16] Hatayama T, Moller AR. Correlation between latency and amplitude of peak V in the brainstem auditory evoked potentials: intraoperative recordings in microvascular decompression operations. Acta Neurochir (Wien) 1998;140:681–7. [17] Committee on Hearing and Equilibrium guidelines for the evaluation of hearing preservation in acoustic neuroma (vestibular schwannoma). American Academy of Otolaryngology-Head and Neck Surgery Foundation, INC. Otolaryngol Head Neck Surg 1995;113:179–80. [18] Committee on Hearing and Equilibrium guidelines for the evaluation of results of treatment of conductive hearing loss. American Academy of Otolaryngology-Head and Neck Surgery Ffoundation, Inc., Otolaryngol Head Neck Surg 1995;113:186–87. [19] Allen A, Starr A, Nudleman K. Assessment of sensory function in the operating room utilizing cerebral evoked potentials: a study of fifty-six surgically anesthetized patients. Clin Neurosurg 1981;28:457–81. [20] Wall EJ, Massie JB, Kwan MK, et al. Experimental stretch neuropathy. Changes in nerve conduction under tension. J Bone Joint Surg Br 1992;74:126–9. [21] Ochoa J, Fowler TJ, Gilliatt RW. Anatomical changes in peripheral nerves compressed by a pneumatic tourniquet. J Anat 1972;113:433–55. [22] Fowler CJ, Gilliatt RW. Conduction velocity and conduction block after experimental ischaemic nerve injury. J Neurol Sci 1981;52:221–38. [23] Broggi G, Scaioli V, Brock S, et al. Neurophysiological monitoring of cranial nerves during posterior fossa surgery. Acta Neurochir Suppl 1995;64:35–9. [24] Radtke RA, Erwin CW, Wilkins RH. Intraoperative brainstem auditory evoked potentials: significant decrease in postoperative morbidity. Neurology 1989;39:187–91. [25] Loiselle DL, Nuwer MR. When should we warn the surgeon? Diagnosis-based warning criteria for BAEP monitoring. Neurology 2005;65:1522–3. [26] Martin WH, Stecker MM. ASNM position statement: intraoperative monitoring of auditory evoked potentials. J Clin Monit Comput 2008;22:75–85. [27] American Clinical Neurophysiology Society. Guideline 11 C: recommended standards for intraoperative monitoring of auditory evoked potentials. 2009. Available from: http://www.acns.org/pdf/guidelines/Guideline-11C.pdf.
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical Study
Hearing outcomes after loss of brainstem auditory evoked potentials during microvascular decompression Parthasarathy D. Thirumala a,b,⇑, Balaji Krishnaiah c, Miguel E. Habeych a, Jeffrey R. Balzer a, Donald J. Crammond a a b c
Department of Neurological Surgery, University of Pittsburgh Medical Centre, Suite B-400, 200 Lathrop Street, Pittsburgh, PA 15213, USA Department of Neurology, University of Pittsburgh Medical Centre, Pittsburgh, PA, USA Department of Neurology, Penn State Hershey Medical Center, Hershey, PA, USA
a r t i c l e
i n f o
Article history: Received 3 October 2014 Accepted 15 October 2014
Keywords: Brainstem auditory evoked potential Hearing loss Hemifacial spasm Microvascular decompression
a b s t r a c t The primary aim of this paper is to study the pre-operative characteristics, intra-operative changes and post-operative hearing outcomes in patients after complete loss of wave V of the brainstem auditory evoked potential. We retrospectively analyzed the brainstem auditory evoked potential data of 94 patients who underwent microvascular decompression for hemifacial spasm at our institute. Patients were divided into two groups – those with and those without loss of wave V. The differences between the two groups and outcomes were assessed using t-test and chi-squared tests. In our study 23 (24%) patients out of 94 had a complete loss of wave V, with 11 (48%) patients experiencing transient loss and 12 (52%) patients experiencing permanent loss. The incidence of hearing loss in patients with no loss of wave V was 5.7% and 26% in patients who did experience wave V loss. The incidence of hearing change in patients with no loss of wave V was 12.6% and 30.43% in patients who did experience wave V loss. Loss of wave V during the procedure or at the end of procedure significantly increases the odds of hearing loss. Hearing change is a significant under-reported clinical condition after microvascular decompression in patients who have loss of wave V. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction Hemifacial spasm (HFS) is an involuntary twitching or contraction of the facial muscles on one side of the face. The most common cause of HFS is vascular compression of the facial nerve by the anterior inferior cerebellar artery at the root exit zone. Microvascular decompression (MVD) of cranial nerve (CN) VII is an effective treatment for HFS [1]. An infrequent but significant risk of MVD is hearing loss (HL) [2]. HL occurs at a rate of 7.7–20% in HFS [3,4] caused by iatrogenic injury to CN VIII. There are multiple mechanisms that can injure CN VIII during MVD including stretching of CN VIII when retracting the cerebellum, manipulation of the compressing vessel, and direct trauma by instruments [5]. More importantly any subtle changes to hearing after MVD have been infrequently reported [4]. The use of intra-operative brainstem auditory evoked potential (BAEP) monitoring has substantially decreased the incidence of post-operative HL [6]. Studies have reported that latency and amplitude changes of wave I and wave
⇑ Corresponding author. Tel.: +1 412 648 2228; fax: +1 412 383 9899. E-mail address: [email protected] (P.D. Thirumala). http://dx.doi.org/10.1016/j.jocn.2014.10.009 0967-5868/Ó 2014 Elsevier Ltd. All rights reserved.
V of the BAEP are the most useful predictors of post-operative HL [7–9]. Complete loss of BAEP waveforms is an uncommon event during MVD, which causes significant anxiety to the surgeon and the monitoring team. However to our knowledge no study has evaluated the patients who had a loss of wave V during MVD; this could provide valuable information during the procedure in addition to its prognostic potential. The primary aim of this paper is to study the pre-operative characteristics which may increase the incidence of loss of wave V in addition to analyzing the intra-operative changes and post-operative outcomes in these patients.
2. Patients and methods 2.1. Patient selection A retrospective analysis was performed in patients who underwent MVD for HFS between January 2000 and December 2007 at the University of Pittsburgh Medical Center. We included 94 patients who had been diagnosed with HFS pre-operatively based on electromyographic testing, who had pre and post-operative hearing function documentation and those who had BAEP
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responses at baseline during surgery. We excluded patients with poor pre-operative hearing function. The study was approved by the Institutional Review Board for retrospective review of data on human subjects at the University of Pittsburgh (MOD0812039404/PRO08120394). The surgical steps during MVD for HFS have been discussed in detail in previous publications by this group [10–13]. In brief the nerve was decompressed from its cross compressing arterial loop and then the conflicting vessel was separated by means of a pledget made of soft Teflon felt fibers (DuPont, Wilmington, DE, USA) [1]. 2.2. Pre-operative auditory investigations An audiologic examination was performed in all patients before (median 1 day, range 1–16 days) and after surgery (median 7 days, range 2–16 days), consisting of an audiogram, pure tone thresholds measurement (air and bone conduction for octave frequencies 250 to 8000 Hz) and speech discrimination scores, which were considered to be the predictors of auditory function [5,6]. Pre-operative tympanometry and acoustic reflex thresholds were also obtained to detect any conduction abnormality. 2.3. Intra-operative BAEP monitoring All patients undergoing MVD had continuous intra-operative BAEP monitoring. The right or left ears were stimulated independently, using alternating rarefaction and condensation clicks with at least an 85 decibel above normal adult hearing level (dBnHL) intensity level. The BAEP responses were recorded on the side of the procedure. A stimulus rate of 17.5 Hz was used. White noise was applied to the contralateral ear at 65 dBnHL. The observation interval was 12 ms. At least 512 responses were averaged for each epoch. The recording electrodes were positioned as follows: Ch1 = vertex to left ear mastoid (Cz/A1); Ch2 = vertex to right mastoid (Cz/A2); and Ch3 = vertex to cervical C2 (Cz/Cv2). Amplifier bandpass was 100–1000 Hz for all channels. Baseline BAEP responses were obtained after anesthesia induction and patient positioning. Lateral spread response was obtained for all patients to evaluate the efficacy of decompression [11]. Physician oversight and interpretation was performed using a combined on-site and remote model utilized at the University of Pittsburgh Medical Center [14]. Consistent decreases in amplitude of greater than 50% of wave V were considered clinically significant [4,15,16]. 2.4. Analysis of neurophysiological parameters For this study, wave V was marked for analysis at the following times during surgery: (1) baseline, after intubation and positioning of the patient; (2) during dural opening; (3) at change start, when the first consistent decrease in the amplitude of wave V >50% and/ or increase in the latency of wave V >0.5 ms compared to baseline was noted, (4) when the last recordable amplitude and or latency changes before complete loss of wave V were recorded, and (5) at skin closure. We also analyzed changes as being either transient or a permanent abolition of wave V of BAEP. Transient loss of wave V is defined as loss of waveform V during MVD and subsequent reestablishment of a measurable response later during surgery. A permanent loss is defined as wave V being lost and not returning for the entire duration of the procedure. If the waveforms were lost, latency was recorded as 12 ms which is the maximum observation time and the amplitude was recorded as zero for analytical purposes. We divided patients into two groups, with Group I being patients with no loss of wave V and Group II being patients with loss of wave V during or at the end of the procedure. We also analyzed wave I and wave III of BAEP in patients during the procedure.
2.5. Post-operative auditory testing and HL criteria Both pure tone thresholds measurement and speech discrimination scores were re-tested after surgery (median 7 days, range 2–16 days). To avoid misinterpretation of audiometric findings, otoscopy and tympanometry was also performed to detect middle ear dysfunction, which may be due to fluid entering the mastoid air cells and or bone dust deposition during craniotomy. An air–bone conduction gap identified in the speech range of frequencies determined post-operative conductive HL status [17]. We compared both pre and post-operative pure tone thresholds measurement and speech discrimination scores, and classified post-operative HL using the American Academy of Otolaryngology–Head and Neck Surgery criteria [4,18]. Using the post-operative audiogram data and speech discrimination scores patient hearing was divided into three categories, being Category A = no hearing change, Category B = hearing change HC) including altered but useful hearing or serviceable hearing loss, and Category C = non-serviceable hearing loss, that is, HL not amenable to hearing aids (Table 1). 2.6. Statistical analysis Statistical analyses were performed using the Statistical Package for the Social Sciences version 20 (SPSS, Chicago, IL, USA). Continuous variables were presented as mean ± standard deviation and categorical variables as frequency (%). The differences in demographic and operative characteristics were compared between the two groups and outcomes were assessed using t-tests and chi-squared tests. p < 0.05 was considered statistically significant. Univariate logistic regression analysis was done to evaluate the effect of loss of wave V of BAEP responses during the procedure and at the end of the procedure on post-operative HL.
Table 1 Demographics and comparison of clinical characteristics between Group I (no wave V loss) and Group II (transient or permanent wave V loss) Variable
Group I
Group II
Patients, n
71
23
p value
Sex Male Female
22 (30%) 49 (70%)
11 (47.82%) 12 (52.17%)
0.14
Side Left Right
38 (53.52%) 33 (46.47%)
16 (69.56%) 7 (30.43%)
0.176
Botulinum toxin treatment Used by patient Multiple injections
47 (66.19%) 38 (53.52%)
17 (73.91%) 17 (73.91%)
0.01 0.02
Pre-operative symptom Decreased corneal reflex Tinnitus Decreased hearing Tonus Platysma involvement
17 (23.94%) 4 (5.64%) 8 (11.26%) 40 (56.33%) 33 (46.47%)
5 (21.70%) 0 2 (8.69%) 16 (69.56%) 9 (39.13%)
0.50 0.96 0.404 0.50 0.15
Offending vessel AICA PICA VA Unnamed artery Vein Perforator Average time to maximum change, hour:min:s
35 (49.29%) 30 (42.25%) 17 (23.94%) 9 (12.6%) 0 (42.25%) 9 (12.6%) 01:13:10
10 (43.47%) 10 (43.47%) 4 (5.63%) 4 (5.63%) 11 (47.8%) 2 (8.69%) 01:02:08
0.77 0.50 0.31 0.04 0.50 0.92 0.61
Total duration of surgery, hour:min:s
01:51:53
01:55:06
0.48
AICA = anterior inferior cerebellar artery, min = minutes, PICA = posterior inferior cerebellar artery, VA = vertebral artery. Bold indicates a statistically significant result.
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3. Results
3.3. Neurophysiological analysis
3.1. Demographics
In the present study 23 out of 94 (24%) patients had complete loss of wave V, of whom 11 (48%) patients had transient loss and 12 (52%) had permanent loss. Of the patients with transient loss of wave V all 11 had significant latency increases which did not improve to baseline values at the end of surgery (measured at the time of skin closure). Five patients with transient wave V loss had significant decreases in amplitude that did not return to baseline at the end of surgery. The remaining four patients had insignificant decreases in amplitude at the end of surgery compared to baseline. Two patients with transient wave V loss had a decrease in amplitude during surgery but their amplitude recovered back to baseline. All patients in Group II with HL had a significant decrease in wave V amplitude, but never recovered to normal baseline values. Of the 23 Group II patients, six had measureable latency and amplitude of wave III despite wave V loss. Among them, four (67%) patients had no HL and three out of these four had transient loss of wave V. Three patients had total loss of wave I along with wave III and V. All three patients did not have any improvement in BAEP waveforms at the end of the procedure. Two of the patients who lost all waveforms had HL and the other had normal hearing.
In this study we analyzed the BAEP data of 94 patients and compared the pre-operative characteristics, intra-operative changes and post-operative outcomes between Group I (n = 71) and Group II (n = 23) patients. 3.2. Pre-operative characteristics and intra-operative findings In our study 64 (70.42%) out of 94 patients had received botulinum toxin treatment prior to surgery with 54 (58.51%) patients having received multiple botulinum injections prior to MVD. A majority (70.7%) of patients had multiple compressing vessels. Compression was caused mainly by the anterior inferior cerebellar artery, posterior inferior cerebellar artery, vertebral artery, and some bridging veins in both groups. Mean time taken for surgery was 02:00 hours in Group I and 01:55 hours for Group II. Average time taken for maximum change in Group I was 01:13 hours and 01:02 hours for Group II. There was no statistically significant difference between two groups when comparing demographics such as age, sex, side of operation, pre-operative symptoms and operative characteristics like duration of surgery and time to maximum change (Table 2). Patients in Group II had a significantly higher usage of pre-operative botulinum toxin injection for HFS treatment (p = 0.01) than those in Group I.
3.4. Hearing analysis The incidence of HL in patients with transient (two out of 11) and permanent loss (four out of 12) of wave V was 18% and 33%, respectively. The incidence of HC in patients with transient (three out of 11) and permanent (four out of 12) loss of wave V was 27% and 33%, respectively (Fig. 1). In Category A we had 58 Group I patients and 10 Group II patients (six had transient and four had permanent wave V loss). In Category B we had nine Group I patients and seven Group II patients (three had transient and four had permanent loss of wave V). In category C we had four Group I patients and six Group II patients (two had transient and four had permanent loss of wave V). There was a significantly higher incidence of HC and HL in Group II patients (p = 0.05) (Table 3). Regression analysis shows that patients who have a loss of wave V during the procedure and experience persistent loss of wave V are more than seven times more likely to have HL as compared to patients who did not experience a loss of wave V (Table 4).
Table 2 Correlation of wave V latency at various stages of surgery between Group I (no wave V loss) and Group II (transient or permanent wave V loss) Time point
Wave V latency, ms
Baseline (after induction) Dural opening Change start Change maximum last recorded On skin closure
Group I (n = 71)
Group II (n = 23)
p value
6.49 ± 0.38 6.71 ± 0.47 7.10 ± 0.47 8.05 ± 1.24 7.23 ± 0.87
6.52 ± 0.28 6.57 ± 0.32 7.06 ± 0.40 8.01 ± 0.62 10.03 ± 2.18
0.46 0.10 0.84 0.29 >0.001
Data are presented as mean ± standard deviation. Bold indicates a statistically significant result.
23 Paents with loss of wave V 12 paents with permanent loss
4( 17%) paents had HC
4(17%) had HL
11 paents with trasient loss 4 paents had no HL
2 paents had returned back to baseline amplitude both the paents had no HL
4 paents had Insignificant changes in amplitude on skin that did not return to baseline 1 paent had no HL, 2 had HC, 1 had HL
5 paents had significant decrease in amplitude and not returned to baseline
3 had no HL, I had HC, 1 had HL
Fig. 1. Hearing change and hearing loss pattern in patients with loss of wave V during microvascular decompression. HC = hearing change, HL = hearing loss.
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Table 3 Correlation of wave V amplitude at various stages of surgery between Group I (no wave V loss) and Group II (transient or permanent wave V loss) Time point
Wave V latency (ms)
Baseline (after induction) Dural opening Change start Change maximum last recorded On skin closure
Group I (n = 71)
Group II (n = 23)
p value
0.35 ± 0.11 0.35 ± 0.16 0.33 ± 0.11 0.21 ± 0.08 0.29 ± 0.11
0.32 ± 0.12 0.31± 0.19 0.33 ± 0.14 0.21 ± 0.10 0.08 ± 0.10
0.79 0.72 0.79 0.47 0.49
Data are presented as mean ± standard deviation.
Table 4 Results of regression analysis for loss of response of wave V and the risk of hearing loss Loss of wave V
During procedure At the end of procedure
Odds ratio
7.444 6.667
95% confidence interval Lower limit
Upper limit
1.694 1.509
32.175 29.448
4. Discussion Our results indicate that loss of wave V significantly increases the incidence of HL and HC, which to our knowledge has not been previously reported. The number of patients (24%) who experience a loss of wave V during MVD and suffer subsequent HL is similar to previously published results. Grundy et al. [8] demonstrated hearing was preserved if waveforms were intact or if only transient loss was encountered, but if waveform V was permanently abolished hearing was invariably lost. Similarly Allen et al. [19] showed that no hearing impairment (all five cases) was seen in patients with transient wave loss, but two out of three patients who had permanent wave V loss had HL. Raudzen and Shetter [7] reported that intra-operative BAEP were unchanged throughout surgery in 34 patients (74%) and these individuals had no post-operative hearing deficit. Four patients had loss of all BAEP waveforms and this correlated to deafness or HL. In a study performed by Polo et al. [6] there was a 33% rate of HL when wave V was abolished permanently. Our results indicate increased HC in patients who had a loss of wave V during MVD. Transient stretching of a cranial or peripheral nerve can result in temporal dispersion with or without conduction block resulting in drop in amplitude of the response. The generator of wave V, the inferior colliculus, is several synapses more distal along the auditory pathway. Therefore a change in wave V is a cumulative desynchronization of BAEP responses over one or two synapses that decreases the overall strength, that is, each synapse has an additional threshold for synaptic integration of multiple afferents. In some cases the potential generated at the cochlea and travelling in the auditory nerve is severely dispersed leading to a recording of wave III but a loss of wave V, as observed in our study. Improvement in the amplitude after complete loss, as seen in BAEP during MVD, can occur without permanent injury to the nerve [20]. In acute conditions where pressure of high magnitude has been directly applied to a nerve trunk, the resulting disturbances in nerve function are based mainly upon the effect of myelin damage. The redistribution of tissue from compressed to non-compressed levels of the nerve is associated with invagination of the myelin sheaths at the nodes of Ranvier [21,22]. The resulting myelin damage is associated with partial or complete local conduction block and it is usually reversible. Based on nerve stretch studies a permanent loss of wave V of BAEP could be caused by complete infarction
of the peripheral nerve, and transient loss might be due to ischemia which improved after the end of the surgery. Changes in the amplitude and latency of BAEP secondary to stretching clearly seem to affect post-operative hearing outcomes, including both HL and HC. Wave I of BAEP originates from the auditory nerve, an area that is not vulnerable during surgery. Three of our patients displayed a loss of wave I. This may be attributed to manipulation of the labyrinthine artery and/or anterior inferior cerebellar artery during surgery, leading to reversible ischemia or infarction of the cochlea [5]. We had patients who had no hearing dysfunction despite loss of wave V on BAEP. Similar findings were reported by Broggi et al. [23] who suggested that the abolition of wave V with preservation of wave I may be associated with good post-operative hearing function. It is possible these patients had a neuropraxic injury of CN VIII which improved after the end of the surgical procedure. Furthermore, in our study, use of pre-operative botulinum toxin was associated with loss of wave V during MVD. Botulinum toxin treatment is a common, transient treatment for HFS as its effects are at the level of the neuromuscular junction. In our patients the exact etiopathogenesis of the loss of wave V and its association with increased use of botulinum toxin is unclear. Previous studies which analyzed changes in the latency changes of wave V identified prolongation in latency of 1.5 ms, 1.0 ms and 0.5 ms as alarms to warn the surgeon of impending injury to CN VIII [8,16,24]. However Friedman et al. [9] have suggested that simple prolongations of wave I, III and V latencies do not correlate with post-operative hearing deficits. Loiselle and Nuwer [25] commented that overreliance upon arbitrary warning criteria invites inaccuracy, which leads to increased patient risk. Hence the currently recommended alarm criteria [26,27] need to be robustly evaluated before being widely accepted as a standard to warn the surgeon of an impending loss of waveform. Although our study was limited because of its retrospective nature and lack of long-term follow-up audiograms, we highlight a very important clinical change in hearing function with loss of wave V during MVD. 5. Conclusion Loss of wave V during MVD significantly increases the odds of HL. HC is a significant under-reported condition after MVD in patients who have loss of wave V. Pre-operative use of botulinum toxin injection was significantly higher in patients with loss of wave V during MVD. More than half of patients with no HL despite wave V loss during MVD had transient loss of wave V. Alarm criteria need to be developed to predict and prevent the loss of wave V during MVD. Conflicts of Interest/Disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication. References [1] Jannetta PJ, Abbasy M, Maroon JC, et al. Etiology and definitive microsurgical treatment of hemifacial spasm. Operative techniques and results in 47 patients. J Neurosurg 1977;47:321–8. [2] Little JR, Lesser RP, Lueders H, et al. Brain stem auditory evoked potentials in posterior circulation surgery. Neurosurgery 1983;12:496–502. [3] Rizvi SS, Goyal RN, Calder HB. Hearing preservation in microvascular decompression for trigeminal neuralgia. Laryngoscope 1999;109:591–4. [4] Shah A, Nikonow T, Thirumala P, et al. Hearing outcomes following microvascular decompression for hemifacial spasm. Clin Neurol Neurosurg 2012;114:673–7. [5] Sindou MP. Microvascular decompression for primary hemifacial spasm. Importance of intraoperative neurophysiological monitoring. Acta Neurochir (Wien) 2005;147:1019–26 [discussion 1026].
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