Reza Hoseinabadi, Akram Pourbakht, Nasrin Yazdani, Ali Kouhi & Mohammad Kamali
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1 The effects of abnormality of cvemp and ovemp on rehabilitation outcomes in patients with idiopathic benign paroxysmal positional vertigo Reza Hoseinabadi, Akram Pourbakht, Nasrin Yazdani, Ali Kouhi & Mohammad Kamali European Archives of Oto-Rhino- Laryngology and Head & Neck ISSN DOI /s y 1 23
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3 DOI /s y OTOLOGY The effects of abnormality of cvemp and ovemp on rehabilitation outcomes in patients with idiopathic benign paroxysmal positional vertigo Reza Hoseinabadi 1 Akram Pourbakht 2 Nasrin Yazdani 3 Ali Kouhi 3 Mohammad Kamali 4 Received: 21 January 2015 / Accepted: 24 March 2015 Ó Springer-Verlag Berlin Heidelberg 2015 Abstract The presence of utricular and saccular dysfunction impairs quality of life (QoL) in patients. The aims of the present study were to examine the effect of repositioning maneuvers on QoL of patients with idiopathic benign paroxysmal positional vertigo (BPPV) and to describe the effect of cervical vestibular-evoked myogenic potential (cvemp) or ocular VEMP (ovemp) abnormalities on patient recovery after rehabilitation. Thirty idiopathic BPPV patients with/without otolith dysfunctions (n = 15, each group) were included in this clinical trial study. Otolith dysfunction was determined using ovemp and cvemp abnormalities. EcochG and caloric tests were performed to rule out other causes of secondary BPPV. The QoL in groups of patients with idiopathic BPPV was assessed using a Persian version of the dizziness handicap inventory (DHI-P) before and after treatment with Epley s maneuver. Pre-treatment results showed significant handicaps in both groups. DHI-P scores were higher in BPPV patients with otolith dysfunction (total, functional, emotional, physical score: 34.13, 11.20, 7.06, 15.86, respectively) than those in patients without otolith dysfunction & Nasrin Yazdani N_yazdani@tums.ac.ir Department of Audiology, School of Rehabilitation, Tehran University of Medical Sciences, Tehran, Iran Department of Audiology, Rehabilitation Research Centre, School of Rehabilitation Sciences, Iran University of Medical Sciences, Tehran, Iran Otorhinolaryngology Research Centre, Amir-Alam Hospital, Tehran University of Medical Sciences, Saadi Avenue, Tehran, Iran Department of Rehabilitation Management, School of Rehabilitation Sciences, Iran University of Medical Sciences, Tehran, Iran (total, functional, emotional, physical score: 25.46, 7.86, 6.13, 11.46, respectively, P \ 0.05). After treatment, DHI- P scores decreased in both groups. However, in the otolith dysfunction group, DHI-P scores (total, functional, emotional, physical score: 9.20, 3.33, 1.33, 4.53, respectively) were higher than those in patients without otolith dysfunction (total, functional, emotional, physical score: 4.13, 0.93, 1.06, 2.00, respectively). In BPPV patients with cvemp or ovemp abnormalities, QoL is more compromised in comparison with that in BPPV patients without these dysfunctions. Otolith dysfunction enhances the negative effects of BPPV on QoL. Keywords Handicap Otolith dysfunction Idiopathic BPPV Epley s maneuver Introduction Benign paroxysmal positional vertigo (BPPV) is a recurrent vestibular disorder that causes vertigo and dizziness [1, 2]. Up to 90 % of positioning nystagmus/vertigo is related to BPPV [3, 4]. The mean age of BPPV onset is 49 years and its lifetime prevalence is 2.4 % [5]. The posterior semicircular canal is most commonly affected [6]. Principal symptoms of BPPV are vertigo with a change of head position with respect to gravity [7], dizziness, postural instability, imbalance, light headedness, and nausea that may last for several hours [6, 8, 9]. BPPV may be caused by different disorders of the inner ear that dislodge small calcium particles (otoconia) from the utricular macula [7]. However, this detachment sometimes occurs without any specific cause [10]. The otoconia dislodge from a degenerative utricular macula and cause a displacement of the endolymph [11]. The degenerative process that leads to
4 dislodgement of otoconia in BPPV patients is not yet fully understood. The role of the utricle has been widely accepted given its close proximity to the ampulla of the posterior canal [12]. Although it has been found that otoconia could come from degenerated saccular macula too [13]. So, degenerated utricular and saccular structures could lead to a higher possibility of BPPV, its resistance to treatment and recurrence. Canalith repositioning maneuvers are the most commonly used procedures for the treatment of BPPV and in % of cases lead to cessation of nystagmus and [9, 14, 15] vertigo. These maneuvers treat BPPV by moving otoconia particles from the semicircular canal to the vestibule, where they dissolve. The effectiveness of Epley s maneuver in the treatment of BPPV patients has been demonstrated [16] and this maneuver is the most successful, particularly indicated in the treatment of posterior canal BPPV [7]. However, one study showed that twothirds of patients had residual dizziness after successful repositioning [17] and this may be due to otoconia remaining in the semicircular canal. The number of maneuvers needed to abolish positioning nystagmus is 1 3 (mean of 1.5). Although there are some cases that have required ten or more maneuvers [18]. Delay in treatment or no treatment of BPPV increases the possibility of cupululithiasis, duration of dizziness and hydrops. A decrease in disease duration increases quality of life (QoL) [19]. So the prompt diagnosis and treatment of BPPV significantly improves QoL of patients [9]. These findings highlight the importance of appropriate diagnosis and treatment of BPPV. Patients with otolith disorders may have dizziness persisting for more than 1 year [20] which significantly limits their lifestyle [21]. Recently, with new tests of otolith function, we can find abnormalities in the otolith structures and assess the impact on patients QoL [14]. The cervical VEMP response originates from the saccule [22]. ovemp is another new test for the assessment of the vestibular system with myogenic potentials. In this test, activation of extraocular muscles in response to sound is measured. Recent studies have shown that ovemp, which occurs in response to AC sounds and recorded by infraorbital electrodes, is originated from the utricle and superior vestibular nerve [23 25]. It has also shown that abnormalities in utricular function and ovemp abnormalities are correlated [26]. Dysfunction of otolith organs affects QoL of patients and findings of VEMP (cervical and ocular) provide indications for these dysfunctions. Vestibular disorders have detrimental effects on the daily activities of patients [27]. BPPV as one of the most common vestibular disorders causing disability and handicap has important effects on physical and social functioning [2, 15, 16, 28]. Being aware of the negative effects of different vestibular disorders on the QoL of patients is an important part of vestibular rehabilitation. The dizziness handicap inventory (DHI) is the first self-assessment inventory to evaluate the degree of disability associated with any cause of dizziness and the efficacy of vestibular rehabilitation. This questionnaire was developed in 1990 by Jacobson and Newman [29] and in this study, a Persian translated and validated DHI (DHI-P) [30] was used. It can be completed before and after treatment so that the problems that each patient experiences can be assessed. The purposes of the present study were; (1) to examine the effect of repositioning maneuvers on the QoL of idiopathic BPPV patients, and (2) to describe the effect of cvemp and ovemp abnormalities on the recovery of idiopathic BPPV patients. Materials and methods Subjects This clinical trial study was conducted on 30 BPPV patients aged 22 to 59 years old, with vertigo and nystagmus (torsional upbeating geotropic nystagmus) as assessed by the Dix Hallpike test. All patients had unilateral posterior canal BPPV and patients with anterior or horizontal canal BPPV were excluded from this study. BPPV and VEMP abnormalities were in the same side. Patients were divided into two groups based on the absence of otolith problems (group 1) or the presence of these problems (group 2). Patients in both groups were age matched. The number of patients in each group was determined with sample size formula. Meniere s disease, endolymphatic hydrops, labyrinthitis, vestibular neuritis, cervical problems, trauma history, migraine, otologic or nonotologic surgery (surgeries involving drilling and also maxillofacial and dental surgery including placement of dental implants in 1 year before BPPV), sudden SNHL, conductive hearing loss, prolonged bed rest and patient refusal to participate in the study were exclusion criteria. We also excluded patients who were [60 years old. This study was approved by the ethics committee of the Tehran University of Medical Sciences. The time interval between onset of BPPV and treatment of these patients was less than 2 weeks. It prevented from including of patients with chronic disease in our study. Protocol Common otologic and neurologic tests (depending on the physician decision) were done to rule out central nervous system problems. History taking and physical exam, tympanometry and audiometry, tiptrode EcochG with gold
5 electrodes (to rule out endolymphatic hydrops), caloric test (to rule out vestibular neuritis), VEMP and ovemp were performed. All patients completed the DHI-P before treatment and 1 month after successful treatment. BPPV patients based on inclusion and exclusion criteria and the absence or presence of otolith dysfunction were placed in group 1 or 2. cvemps cvemp testing was conducted in a sitting position with the patient s head turned to opposite side of the stimulus. EMG activity was recorded by superficial electrodes in the middle of the sternocleidomastoid (SCM), a reference electrode on the upper third section of the sternum, and a ground electrode in the middle of the forehead. The feedback method was used for SCM contraction. Using an ICS Charter, 95 db nhl 500 Hz tone bursts were presented through headphones, and the EMG signal was amplified and bandpass filtered ( Hz). The analysis window was 100 ms wide and responses to 150 stimuli were averaged. The amplitude of the first positive negative peak (P13 N23) was recorded. ovemps ovemp testing was conducted in a sitting position with the patient looking upward at the center of a small target that was 100 cm from the patient s eyes. The visual angle was about 30 as this angle has been shown to produce the best response in comparison to other eye positions [31]. An active electrode was placed on the face approximately 1 cm below the inferior eyelid of the eye contralateral to the acoustic stimulus. The reference electrode was placed about 1 cm below the active electrode on the chin and the ground electrode on the forehead. Using an ICS Charter, 95 db nhl 500 Hz tone bursts were presented through headphones, and the EMG signal was amplified and bandpass filtered ( Hz). The analysis window was 100 ms wide and responses to 200 stimuli were averaged. The initial negative positive biphasic waveform comprised peaks N1 and P1. We analyzed the peak-to-peak amplitude of N1 and P1 at the maximal intensity of stimulation. Otolith dysfunction in our patients was defined as the lack of unilateral responses in cvemp or ovemp. BPPV and cvemp/ovemp abnormalities were in the same side. DHI The DHI questionnaire, which was developed by Jacobson and Newman (1990) [29] and translated and standardized for the Persian language by Jafarzade et al. [30] was used to assess the harmful effects of dizziness on QoL of patients. Cronbach s alpha for DHI-P was 0.79, 0.82, 0.83, and 0.9 for total, emotional, physical, and functional subscales, respectively [30]. For reliability, the intraclass correlation coefficient was 0.96 for total score, and 0.92, 0.92, and 0.96 for emotional, physical, and functional subscales, respectively [30]. Considering good reliability and internal consistency, it was suggested that DHI-P can be used for evaluating the dizziness effects on QoL in the Persian population. It evaluates the dizziness associated with the incapacities and handicap. Patients were asked to complete the DHI-P consisting of 25 questions, and a total score (0 100 points) was obtained by sum of ordinal scale responses. Higher scores on the DHI-P indicated a more severe handicap. The 25 items were divided into three subscales: functional, emotional, and physical aspects of dizziness and unsteadiness. There are nine questions within each of the functional and emotional subscales, with each question having a maximum score of 4 for each item. Within the physical subscale, there are seven questions with a maximum score of 4 for each. The range of possible scores was points. Scores up to 30 represented a mild handicap, scores between 31 and 60 represented a moderate handicap, and scores of more than 60 represented a severe handicap. The smallest detectable change in DHI- P score was 19 points [30]. Intervention Treatment of patients was done using Epley s maneuver. One week after treatment they were assessed with a Dix Hallpike test. If no nystagmus and vertigo were present, successful treatment was considered. If symptoms were persistent, Epley s maneuver was repeated. Statistical analysis For statistical analysis, SPSS 19.0 software was used. The values (DHI-P total score and subscales) for the both groups were compared with an independent sample t test and Mann Whitney U test (based on normal or abnormal distribution of data) and a P value of \0.05 indicated statistical significance. To compare the DHI-P scores before and after treatment in each group, a paired t test and a two-related sample test (based on normal or abnormal distribution of data) were used. Results Thirty patients fulfilled the inclusion criteria and were evaluated and treated in this study. Ages ranged from 22 to 59 years. The mean age of patients in the group without otolith dysfunction was (±7.39) and (±9.70)
6 in the group with otolith dysfunction. In group 1, there were six males and nine females and in group 2, there were eight males and seven females. In group 1, eight patients had right-sided BPPV and seven had left-sided BPPV. In group 2, six patients had right-sided BPPV and nine had left-sided BPPV. Twenty-six patients were treated with a single Epley s maneuver, three patients received two maneuvers, and one patient needed three maneuvers. In BPPV patients with otolith dysfunction (n = 15), ten patients had saccular dysfunction and five patients had utricular dysfunction. None of our patients in this group had both of saccular and utricular dysfunction. The total score before treatment in the saccular dysfunction group was (±5.94) and (±8.78) in the utricular dysfunction group. In groups 1 and 2, mean total DHI scores before treatment were (±10.23) and (±7.65), respectively. This difference was statistically significant (P = 0.02). Total DHI-P scores and subscale scores before and after treatment in the group without otolith dysfunction are shown in Table 1. The results show that DHI-P scores after treatment decreased. Total DHI-P scores and subscale scores before and after treatment in the group with otolith dysfunction are shown in Table 2. The results show that DHI-P scores after treatment decreased. The difference between results before and after treatment in this group was more than the group without otolith dysfunction. In group 1, 11 patients (73 %) and in group 2, 13 patients (86 %) showed an improvement of more than 19 points on the DHI-P. Table 1 Total DHI-P and subscale scores before and after treatment in the group without otolith dysfunction Results Before treatment [mean (±SD)] After treatment [mean (±SD)] P value Total score (±10.23) 4.13 (±5.26) \0.001 Functional score 7.86 (±3.58) 0.93 (±1.66) \0.001 Emotional score 6.13 (±5.82) 1.06 (±2.71) \0.001 Physical score (±3.66) 2.00 (±1.69) \0.001 Table 2 Total DHI scores and subscale scores before and after treatment in the group with otolith dysfunction Results Before treatment [mean (±SD)] After treatment [mean (±SD)] P value Total score (±7.65) 9.20 (±8.16) \0.001 Functional score (±3.83) 3.33 (±3.08) \0.001 Emotional score 7.06 (±2.91) 1.33 (±2.22) \0.001 Physical score (±4.98) 4.53 (±3.50) \0.001 The average scores of functional, emotional, and physical subscales, after treatment for both groups are shown in Table 3. If the distribution of data was normal, T test was used (total and physical subscales) and when the distribution was not normal, Mann Whitney U test was used (functional and emotional subscales). Comparison of reduction rates of DHI-P scores in both groups is shown in Table 4. Discussion In the present study we examined the effect of repositioning maneuvers on the QoL of idiopathic BPPV patients and described the effect of cvemp or ovemp abnormalities on patient recovery after rehabilitation. Pre-treatment assessment of patients using the DHI-P showed that dizziness and vertigo resulting from BPPV negatively affected QoL of patients in all dimensions of daily life. Moreover, BPPV patients with otolith dysfunction showed greater handicaps. In both groups, the most compromised subscale was physical, followed by the functional and emotional subscales. The physical subscale assesses the relation between the onset and worsening of dizziness and eye, head, and body movements of patients [32]. These functions are more compromised in BPPV patients. So this leads to higher scores in the physical subscale in these patients. The findings of other studies validate our results [15, 32 34]. The difference between DHI-P scores before and after treatment was statistically significant in both groups of patients. This finding that DHI-P subscale scores decrease after treatment is supported in the literature [15]. Most BPPV patients, even with otolith dysfunction, showed an improvement of greater than 19 points. The smallest detectable change in DHI-P scores was 19. This change is not due to measurement errors and shows genuine changes in patient status. Therefore, if the change in total score was more than 19, this change was considered significant and demonstrates effective treatment [30]. Because of more definite improvements in BPPV after rehabilitation with canalith repositioning maneuvers, this finding is feasible. This may be a point of difference for BPPV compared to other vestibular disorders. Post-treatment results showed that in the otolith dysfunction group in comparison to the group without otolith dysfunction, all of the DHI-P subscales were higher and this difference was statistically significant in the physical and functional subscales. This shows the negative effects of otolith dysfunction on the QoL of BPPV patients. Higher physical subscale scores in patients with otolith dysfunction may be due to otoconia remaining in the semicircular canal as a result of continued detachment of otoconia from
7 Table 3 DHI-P scores after treatment in group 1 and 2 Group Total [mean (±SD)] Functional [mean (±SD)] Emotional [mean (±SD)] Physical [mean (±SD)] Without otolith dysfunction 4.13 (±5.26) 0.93 (±1.66) 1.06 (±2.71) 2.00 (±1.69) With otolith dysfunction 9.20 (±8.16) 3.33 (±3.08) 1.33 (±2.22) 4.53 (±3.50) P value 0.05 \ Table 4 Comparison of reduction rates of DHI-P scores in both groups Group Reduction rate Without otolith dysfunction (±5.93) With otolith dysfunction (±4.58) P value 0.06 otoliths. Continued detachment of otoconia leads to more residual dizziness in the absence of severe nystagmus. It demonstrates the need for follow-up assessment in patients with these dysfunctions and ensuring patients are aware of the possibility of disease recurrence. Other studies have shown that otolith dysfunction alone has negative effects on the balance of patients which limits their lifestyle [21, 35]. Our study showed that otolith dysfunctions in combination with BPPV enhance the negative effects on QOL of patients. The emotional subscale decreased after treatment and this finding is similar to previous studies on other vestibular disorders [15, 36]. The emotional subscale is related to the psychological aspects of dizziness [32], such as how subjects feel about the opinions of others and issues such as depression [37]. However, the emotional subscale scores were the lowest and that may be due to our early intervention. Paiva and Kuhn [37] showed that psychological symptoms were associated with dizziness. Our findings show that duration of a vestibular disorder may be related to negative effects on the emotional condition of patients. In our study, early intervention lowered the duration of disease symptoms in patients. Reduction rate of more than 19 is considered to be significant in DHI-P. This shows real changes in individual patients and is not due to measurement errors and is indicative of the change in patient s status [30]. This degree of improvement is related to the first score of any patient and shows the recovery degree of them. Our results showed that reduction rate in group 2 was more than group 1 but this difference was not statistically significant. Decrease of DHI-P scores after treatment shows the effectiveness of Epley s maneuver in the treatment of BPPV. The effectiveness of Epley s maneuver has also been shown in the literature [15, 38]. The results of this study also showed that although the difference between DHI-P scores before and after treatment in the group with otolith dysfunction was greater, DHI-P scores in this group after treatment were greater than the other group. This means greater handicaps in BPPV patients with otolith dysfunction were found even after treatment with Epley s maneuver. So it is possible that the degree of recovery could be related to other vestibular disorders that any patient has (in our study, this was otolith dysfunction). Therefore, we cannot rely solely on repositioning maneuvers in the treatment process of patients especially patients with other dysfunctions. In BPPV patients with otolith dysfunction (n = 15), 10 patients had saccular dysfunction and 5 patients had utricular dysfunction. It has shown that BPPV is associated to utricular and saccular dysfunction and possibly is due to utricular or saccular degeneration [12, 13]. In our study, the number of patients with saccular dysfunction was more than those with utricular dysfunction. Although this shows the role of saccule in BPPV, it should not be misinterpreted as the predominant role of saccule in BPPV in comparison to utricle. We did not have any patient with combined utricular and saccular dysfunction. These patients may show more handicaps. Future study is needed regarding these patient s handicaps. Other topics for future studies should include the long-term effects and potential positive impact of vestibular rehabilitation exercises on the QOL of patients with otolith dysfunction. Conclusion Otolith dysfunction negatively affects QOL of BPPV patients even after treatment. The presence of residual dizziness after treatment shows that rehabilitation exercises in addition to CRT may be needed for such patients. Acknowledgments The authors thank the patients for participation. This article was obtained from part of Ph.D. thesis entitled The effect of vestibular rehabilitation on BPPV recurrence and degeneration of otolithic organs in idiopathic BPPV patients sponsored by Tehran University of medical sciences, school of rehabilitation, audiology department, year The authors declare no conflict of interest re- Conflict of interest lated to this study.
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