J Neurol DOI 10.1007/s00415-014-7519-0
ORIGINAL COMMUNICATION
Natural history of horizontal canal benign paroxysmal positional vertigo is truly short Dae Bo Shim • Kyung Min Ko • Joon Hee Lee Hong Ju Park • Mee Hyun Song
•
Received: 30 June 2014 / Revised: 24 September 2014 / Accepted: 25 September 2014 Springer-Verlag Berlin Heidelberg 2014
Abstract The objective of the study is to characterize the natural course of positional vertigo and nystagmus in patients with horizontal canal benign paroxysmal positional vertigo (h-BPPV) and to analyze the difference in the natural course between the two variants of h-BPPV. We conducted a prospective study in 106 patients with geotropic type h-BPPV [h-BPPV (Geo)] (n = 43) and apogeotropic type h-BPPV [h-BPPV (Apo)] (n = 63) who agreed and signed the written informed consent of no treatment. All patients were asked to answer a detailed interview about the onset time of positional vertigo and to visit the hospital every 1–3 days. At every visit, they were interviewed about cessation time of positional vertigo and positional nystagmus was assessed. The mean period ± SD between the onset and remission of vertigo in the h-BPPV (Geo) was 6.7 ± 6.3 days, whereas that in the h-BPPV (Apo) was 3.7 ± 4.1 days. In addition, the mean period ± SD from the initial diagnosis to the disappearance of positional nystagmus in the h-BPPV (Geo) was 4.7 ± 3.9 days, whereas that in the h-BPPV (Apo) was 4.4 ± 5.0 days. Although the duration until natural remission of positional nystagmus did not differ between the two variants of h-BPPV, the remission of vertigo occurred faster in h-BPPV (Apo) than h-BPPV (Geo) (p \ 0.05). The natural course of h-BPPV is much shorter than that indicated in previous reports. The positional D. B. Shim K. M. Ko J. H. Lee M. H. Song (&) Department of Otorhinolaryngology, Myongji Hospital, 697-24 Hwajung-dong, Deokyang-gu, Goyang, Gyeonggi 412-270, Korea e-mail: [email protected] H. J. Park Department of Otolaryngology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
vertigo disappeared faster in the h-BPPV (Apo) compared to the h-BPPV (Geo) unlike the positional nystagmus. Keywords Benign paroxysmal positional vertigo Semicircular canal Natural course Physiopathology
Introduction Benign paroxysmal positional vertigo (BPPV) is the most common vestibular disorder. The resolution rates of BPPV following specific treatments are very high but spontaneous recovery may also occur [1]. According to the clinical practice guideline provided by the American Academy of Otolaryngology-Head and Neck Surgery (AAO-HNS), clinicians are recommended to treat posterior canal BPPV (p-BPPV) with the particle repositioning maneuver [2]. Various types of the roll maneuver have been reported to be effective in approximately 75 % of the patient for treating horizontal canal BPPV (h-BPPV), although existing data are limited [3–7]. However, observation or ‘‘watchful waiting’’ is considered a therapeutic option to manage both types of BPPV, according to the guidelines [2]. The potential benefits of observation would be that symptoms or discomforts provoked by the therapeutic maneuvers can be avoided and that medical expenses can be saved from decreased referral rates. Recent studies have reported high rates of spontaneous resolution in BPPV, although the reported rates vary widely [8–13]. Some authors have proposed that spontaneous resolution occurs faster in h-BPPV compared to that of p-BPPV, but there is no difference in the natural course between the two h-BPPV variants [14]. The variability concerning the resolution rates of BPPV in previous case– control studies may be due to the differences in the follow-
123
J Neurol
up duration. Furthermore, the follow-up interval in previous studies was longer than 4 weeks, indicating that the short-term resolution rates of BPPV are unknown [8–11, 15]. Another limitation of several recently reported longitudinal follow-up studies is that only subjective symptoms were included as outcome measures for resolution without objective data [13, 14, 16]. Therefore, we attempted to identify the natural course of the geotropic and apogeotropic type variants (h-BPPV (Geo) and h-BPPV (Apo), respectively) of h-BPPV through short-interval follow-up. Objective methods as well as subjective symptoms were used as the outcome measures for resolution. We also analyzed the difference in the natural course between the two h-BPPV variants.
Materials and methods Subjects A longitudinal follow-up study was conducted on 106 patients without a trauma history or concomitant neurootologic disease who were diagnosed with h-BPPV and agreed to sign the written informed consent of no treatment from January 2011 to December 2012 at the Department of Otorhinolaryngology, Myongji Hospital. BPPV was diagnosed when characteristic nystagmus was demonstrated combined with typical symptoms of positional vertigo during the supine head roll test using video Frenzel goggle system (SLMED, Seoul, Korea). In all subjects, there were no identifiable central nervous system disorders that could explain the positional vertigo and nystagmus in neurotologic examinations including spontaneous and gaze-evoked nystagmus, smooth pursuit and saccades, limb ataxia, and balance function in addition to routine neurologic examinations. The provocation test method and the diagnostic criteria for BPPV followed the guidelines provided by the AAO-HNS [2]. The h-BPPV subtypes were determined according to the nystagmus evoked as follows: •
•
h-BPPV (Geo): horizontal direction-changing geotropic nystagmus. The affected ear is identified by the head lateral position that evokes the more intense nystagmus during the supine head roll test (e.g. right ear affected when nystagmus is stronger in the right lateral head turning position). h-BPPV (Apo): horizontal direction-changing apogeotropic nystagmus. The affected ear is identified by the head lateral position that evokes the lesser intense nystagmus during the supine head roll test (e.g. right ear affected when nystagmus is stronger in the left lateral head turning position).
123
Study design All patients were required to revisit the hospital at least every 1–3 days after the initial visit. The patients were asked about the onset time of positional vertigo before visiting our hospital through a detailed interview at the initial visit. At every visit, an interview and examination using the supine head roll test were conducted. When the positional nystagmus disappeared, patients were asked to indicate the exact time at which the positional vertigo disappeared. In addition, the conversion between the two subtypes of h-BPPV was checked using the supine head roll test at every visit. The patients were not given any specific instructions that could affect the remission of disease after the initial diagnosis. A questionnaire asking about sleep position was given to all patients at the first visit and at the time of disappearance of positional vertigo or nystagmus to identify the potential therapeutic effect of forced prolonged position. Written informed consent was obtained from all patients who were enrolled in this study after explaining the detailed pros and cons of both treatment options including receiving therapeutic maneuvers and observation with no treatment. Statistical analysis The comparison between the characteristics of the two h-BPPV subtypes was analyzed with the Mann–Whitney U test. Residual rates of positional vertigo and nystagmus were calculated with the Kaplan–Meier method, and the differences between the two subtypes of h-BPPV in remission curves were analyzed using the log-rank test. All results were considered significant when the p value was \0.05.
Results h-BPPV (Geo) was diagnosed in 43 patients (40.6 %) and h-BPPV (Apo) in 63 patients (59.4 %). The demographic data of our study is presented in Table 1. No significant difference in age or sex was observed between the two subtypes of h-BPPV. Table 2 demonstrates the natural courses of positional nystagmus and vertigo in h-BPPV and both subtypes of h-BPPV. The mean duration from the onset of positional vertigo to the initial visit to our clinic was 2.0 days for h-BPPV, and 3.0 and 1.4 days for h-BPPV (Geo) and h-BPPV (Apo), respectively. The difference of duration between the two subtypes of h-BPPV was significant (p \ 0.05). The average value from the initial diagnosis to the remission of positional nystagmus was 4.5 days, and that value from the
J Neurol Table 1 Clinical and demographic characteristics h-BPPV (Geo) (n = 43)
h-BPPV (Apo) (n = 63)
Age (years) Range
23–81
25–80
Mean ± SD
52.0 ± 13.0
55.2 ± 11.6
Male
9
14
Female
34
49
Sex (numbers)
Affected side (numbers) Right
19
43
Left
24
20
h-BPPV horizontal semicircular canal benign paroxysmal positional vertigo, h-BPPV (Geo) geotropic variant of horizontal semicircular canal benign paroxysmal positional vertigo, h-BPPV (Apo) apogeotropic variant of horizontal semicircular canal benign paroxysmal positional vertigo
onset to the disappearance of positional vertigo was 4.9 days in h-BPPV. When comparing the natural courses between positional nystagmus and vertigo after the initial diagnosis for each variant of h-BPPV, the mean period of positional vertigo was more than 1 day shorter than that of positional nystagmus in both subtypes of h-BPPV (Table 2). However, statistically significant difference was shown for h-BPPV (Apo) only in the duration of remission between the two outcome measures (p = 0.001) (Fig. 1). When analyzing the differences in the natural courses between the two subtypes of h-BPPV, no significant difference was observed between the two subtypes in the remission of positional nystagmus after the initial diagnosis (Fig. 2). However, the remission of positional vertigo after the initial diagnosis as well as after the onset of symptoms in h-BPPV (Apo) was faster than that in h-BPPV (Geo) (p \ 0.05) (Fig. 3). Of 106 patients with h-BPPV, only 7 patients (6.6 %) slept on the contralesional side after the initial diagnosis.
The proportion of the patients who slept on the contralesional side were 7.0 % (3/43 patients) and 6.3 % (4/63 patients) in h-BPPV (Geo) and h-BPPV (Apo), respectively, which did not differ statistically between the two subtypes. Conversion between the two subtypes of h-BPPV was identified in 21 patients (19.8 %). Conversion from h-BPPV (Apo) to h-BPPV (Geo) was observed in 16 patients (25.4 %), whereas the conversion from h-BPPV (Geo) to h-BPPV (Apo) was seen in 5 patients (11.6 %).
Discussion This study demonstrated that the natural course of h-BPPV was very short regarding the objective findings (positional nystagmus) as well as in the subjective symptoms (positional vertigo) using a longitudinal study design. In the present study, the average and median values of duration from the initial onset to the remission of positional vertigo in patients with h-BPPV (Apo) were 3.7 and 2.0, respectively, whereas those in patients with h-BPPV (Geo) were 6.7 and 4.0, respectively. These results are very interesting findings, considering that the mean duration of h-BPPV (Apo) and h-BPPV (Geo) without treatment were previously reported as 16 and 13 days, respectively [13, 16]. A variety of studies have referred to high resolution rates without specific therapeutic maneuver in patients with BPPV and a longitudinal study by Sekine et al. [14] reported that the natural history of h-BPPV was shorter than that of p-BPPV although the exact mean duration of positional vertigo was not presented [13, 16]. However, the previous studies had some limitations in that they had long follow-up intervals usually of more than 2 weeks and that the outcome measures were dependent on the patients’ subjective memory about the time at which their symptoms disappeared. Therefore, to overcome these limitations, the present study was designed to include direct examination
Table 2 The natural courses of positional nystagmus and vertigo in h-BPPV and two subtypes of h-BPPV h-BPPV (n = 106)
Onseta (days)
h-BPPV (Geo) (n = 43)
h-BPPV (Apo) (n = 63)
Mean ± SD
Median
Mean ± SD
Median
Mean ± SD
Median
2.0 ± 3.2
1.0
3.0 ± 3.9
1.0
1.4 ± 2.4
0.0
p value
0.008
Duration of remission (days) Positional nystagmus
4.5 ± 4.5
3.0
4.7 ± 3.9
3.0
4.4 ± 5.0
3.0
0.358
Positional symptom
2.9 ± 3.5
2.0
3.7 ± 4.1
2.0
2.3 ± 2.9
1.0
0.032
Total symptomb
4.9 ± 5.3
3.0
6.7 ± 6.3
4.0
3.7 ± 4.1
2.0
0.008
a
Onset means duration of the symptom until visiting the clinic
b
Total symptom means the duration from the onset until remission of positional symptom
c
Statistical analysis: the comparison between the characteristics of the two subtypes of horizontal canal benign paroxysmal positional vertigo and the p values were computed using the Mann–Whitney U test
123
J Neurol
Fig. 1 Comparison between positional nystagmus and symptoms in the two subtypes of horizontal canal benign paroxysmal positional vertigo (h-BPPV). a No difference was observed between positional nystagmus and vertigo in patients with geotropic type of h-BPPV
(p = 0.228). b A significant difference was observed between positional nystagmus and vertigo in patients with apogeotropic type of h-BPPV (p = 0.001)
Fig. 2 Comparison between the subtypes of horizontal canal benign paroxysmal positional vertigo in the remission from the initial diagnosis to the disappearance of positional nystagmus. a No significant difference was observed between the two subtypes
analyzed by Mann–Whitney U test. b Kaplan–Meier curve with a log-rank test also shows no difference between the two subtypes (p = 0.671)
Fig. 3 Comparison between the subtypes of horizontal canal benign paroxysmal positional vertigo in the remission from the initial diagnosis to the remission of positional vertigo. A significant difference was observed between the two subtypes in the time
courses of vertigo remission a after the initial diagnosis (p = 0.032) and b after the onset of symptoms (p = 0.003) using Kaplan–Meier curve with a log-rank test
123
J Neurol
about the objective nystagmus as well as subjective symptoms with a short follow-up interval. The theoretical hypothesis for the short natural course of h-BPPV could be different for each subtype. In h-BPPV (Geo), the short natural course of h-BPPV (Geo) has been reported to be related to the anatomical position of the horizontal semicircular canal (HC). As the anterior cupular end of the HC is anatomically elevated about 20 degrees from the horizontal plane [17], otoconia within the posterior arm of the HC can theoretically be repositioned back into the utricle possibly by head movements of daily life (e.g. walking) without specific therapeutic maneuvers [13, 14]. The faster symptom remission in h-BPPV (Apo) compared to that in h-BPPV (Geo) suggests that the utricular type of cupulolithiasis may be the predominant pathology underlying h-BPPV (Apo) rather than either the canal type of cupulolithiasis or the presence of free-floating otoconia in the anterior arm of the HC, which is in contrast to the previous reports [5, 6, 18]. If the otoconia is firmly attached to the canal side of the cupula or is freely floating in the anterior arm of the HC in h-BPPV (Apo) as in previous reports, symptom duration should theoretically be longer than h-BPPV (Geo) because the otoconia needs to pass through the posterior arm and the isthmic portion of the HC in order to return to the utricle. However, in the case of the utricular type of cupulolithiasis where the otoconia are attached to the utricular side of the cupula, the pathway to the utricle is very short, which could lead to prompt spontaneous remission of symptoms. Therefore, the short natural course of h-BPPV (Apo) may be explained by the location of the otoconia, which is presumed to be the utricular side of cupula in most cases. Another finding to support the higher incidence of utricular side cupulolithiasis in h-BPPV (Apo) is the low conversion rate (25.4 %) from h-BPPV (Apo) to h-BPPV (Geo) in the course of spontaneous resolution. In a previous study, we have already suggested similar results that the utricular type of cupulolithiais in h-BPPV (Apo) is more common compared to the other two types [19]. In addition to these anatomical factors, spontaneous dissolution of otoconia could be another factor to explain for the short natural course of BPPV as reported previously in several studies [13, 20–22]. Although no significant difference was observed in the remission period of positional nystagmus between the two subtypes, the atypical cases (8/63 patients) of h-BPPV (Apo) demonstrated very long duration of nystagmus of up to 31 days as shown in Fig. 2. Most of these patients showed conversion from h-BPPV (Apo) to h-BPPV (Geo) during the natural course except for two cases. It is postulated that a longer period was needed in these atypical cases for the otoconia to return from the anterior arm of the HC to the utricle, or to return to the utricle after dislodging from the canal side of the cupula. There are numerous
previous studies reporting that cure rate of h-BPPV (Apo) is far lower than that of p-BPPV or h-BPPV (Geo) in contrast to the results of this study [6, 23, 24]. The discrepancy of results among different studies may be associated with the limitation of accurate lateralization methods in the diagnosis of h-BPPV. We checked the sleep position to identify the potential therapeutic effect of forced prolonged position and only seven (6.6 %) out of 106 patients were found to sleep on the contralesional side. The sleep position toward the contralesional side was observed in 7.0 % (3/43 patients) and 6.3 % (4/63 patients) in the h-BPPV (Geo) and h-BPPV (Apo), respectively. Many authors have reported that patients with BPPV have a tendency to sleep with their head to the contralesional side, which may affect the treatment outcome [25, 26]. However, this tendency was observed in only a small proportion of patients in our study, suggesting that the sleep position did not seem to have a significant effect on our results. In this study, only the positional vertigo showed statistically significant difference, while no significant difference was found for the duration of positional nystagmus between the two subtypes of h-BPPV. According to a study about physiomathematical models of BPPV, a greater number of otoconia are required to induce positional vertigo in cupulolithiasis compared to canalolithiasis; 490 otoconia for cupulolithiasis and 62 for canalithiasis [21]. This result indicates that repositioning of fewer otoconia can relieve positional vertigo in cupulolithiasis compared to canalithiasis theoretically, assuming that the same number of otoconia is detached from utricle and also returned to the utricle spontaneously. There are some limitations of this study. First, our results may have potential biases due to the effect of the short interval follow-up on the natural course of h-BPPV. Frequent examination with the positional test can lead to rapid remission of positional nystagmus by the potential therapeutic effect of the diagnostic roll maneuver. Emotional support by frequent consultation with a doctor may have also influenced symptom duration. However, we believe that these effects are probably minimal as no objective evidence to support the therapeutic effects of frequent diagnostic positional test and interview in patients with BPPV has been reported. Another limitation is the difference in onset duration between the two subtypes of h-BPPV. Such a difference was caused by the clinical features of h-BPPV (Apo) exhibiting short latency and long duration of positional nystagmus leading to more severe symptoms than h-BPPV (Geo) caused by minimal movements. To overcome this limitation, the remission time of positional nystagmus as well as symptoms after the initial diagnosis were compared in this study.
123
J Neurol
Based on the results of the present study, watchful waiting might be an important therapeutic option in the treatment of h-BPPV. However, considering that central lesions can also lead to positional vertigo or nystagmus commonly of the apogeotropic type, clinicians should rule out the central causes of positional vertigo and nystagmus before recommending observational therapy to patients [27, 28].
Conclusion The natural course of h-BPPV is much shorter than that reported in previous studies. Although no significant difference in nystagmus remission was observed between the two subtypes of h-BPPV, the natural course of h-BPPV (Apo) was shorter than that of h-BPPV (Geo) regarding the resolution of subjective symptoms. This information may provide clues about the pathophysiology of h-BPPV and also be used clinically by healthcare professionals treating patients who are unwilling to receive the repositioning maneuver for h-BPPV. Acknowledgments The authors thank Dr. Myung-Whan Suh at Seoul National University College of Medicine, for critical review of this manuscript. Conflicts of interest
None.
Ethical standard This study was approved by the Institutional Review Board of Myongji Hospital and informed consent was obtained from all patients. The study has been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki.
References 1. Lee SH, Kim JS (2010) Benign paroxysmal positional vertigo. J Clin Neurol 6:51–63 2. Bhattacharyya N, Baugh RF, Orvidas L, Barrs D, Bronston LJ, Cass S, Chalian AA, Desmond AL, Earll JM, Fife TD, Fuller DC, Judge JO, Mann NR, Rosenfeld RM, Schuring LT, Steiner RW, Whitney SL, Haidari J, American Academy of O-H, Neck Surgery F (2008) Clinical practice guideline: benign paroxysmal positional vertigo. Otolaryngol Head Neck Surg 139:S47–S81 3. Lempert T, Tiel-Wilck K (1996) A positional maneuver for treatment of horizontal-canal benign positional vertigo. Laryngoscope 106:476–478 4. Fife TD (1998) Recognition and management of horizontal canal benign positional vertigo. Am J Otol 19:345–351 5. Nuti D, Agus G, Barbieri MT, Passali D (1998) The management of horizontal-canal paroxysmal positional vertigo. Acta Otolaryngol 118:455–460 6. Casani AP, Vannucci G, Fattori B, Berrettini S (2002) The treatment of horizontal canal positional vertigo: our experience in 66 cases. Laryngoscope 112:172–178 7. Tirelli G, Russolo M (2004) 360-Degree canalith repositioning procedure for the horizontal canal. Otolaryngol Head Neck Surg 131:740–746
123
8. Blakley BW (1994) A randomized, controlled assessment of the canalith repositioning maneuver. Otolaryngol Head Neck Surg 110:391–396 9. Lynn S, Pool A, Rose D, Brey R, Suman V (1995) Randomized trial of the canalith repositioning procedure. Otolaryngol Head Neck Surg 113:712–720 10. Asawavichianginda S, Isipradit P, Snidvongs K, Supiyaphun P (2000) Canalith repositioning for benign paroxysmal positional vertigo: a randomized, controlled trial. Ear Nose Throat J 79(732–734):736–737 11. Froehling DA, Bowen JM, Mohr DN, Brey RH, Beatty CW, Wollan PC, Silverstein MD (2000) The canalith repositioning procedure for the treatment of benign paroxysmal positional vertigo: a randomized controlled trial. Mayo Clin Proc 75:695–700 12. Yimtae K, Srirompotong S, Srirompotong S, Sae-Seaw P (2003) A randomized trial of the canalith repositioning procedure. Laryngoscope 113:828–832 13. Imai T, Ito M, Takeda N, Uno A, Matsunaga T, Sekine K, Kubo T (2005) Natural course of the remission of vertigo in patients with benign paroxysmal positional vertigo. Neurology 64:920–921 14. Sekine K, Imai T, Sato G, Ito M, Takeda N (2006) Natural history of benign paroxysmal positional vertigo and efficacy of Epley and Lempert maneuvers. Otolaryngol Head Neck Surg 135:529–533 15. Woodworth BA, Gillespie MB, Lambert PR (2004) The canalith repositioning procedure for benign positional vertigo: a metaanalysis. Laryngoscope 114:1143–1146 16. Imai T, Takeda N, Ito M, Inohara H (2011) Natural course of positional vertigo in patients with apogeotropic variant of horizontal canal benign paroxysmal positional vertigo. Auris Nasus Larynx 38:2–5 17. Della Santina CC, Potyagaylo V, Migliaccio AA, Minor LB, Carey JP (2005) Orientation of human semicircular canals measured by three-dimensional multiplanar CT reconstruction. J Assoc Res Otolaryngol 6:191–206 18. Baloh RW, Jacobson K, Honrubia V (1993) Horizontal semicircular canal variant of benign positional vertigo. Neurology 43:2542–2549 19. Shim DB, Kim JH, Park KC, Song MH, Park HJ (2012) Correlation between the head-lying side during sleep and the affected side by benign paroxysmal positional vertigo involving the posterior or horizontal semicircular canal. Laryngoscope 122:873–876 20. Zucca G, Valli S, Valli P, Perin P, Mira E (1998) Why do benign paroxysmal positional vertigo episodes recover spontaneously? J Vestib Res 8:325–329 21. House MG, Honrubia V (2003) Theoretical models for the mechanisms of benign paroxysmal positional vertigo. Audiol Neurootol 8:91–99 22. Thalmann R, Ignatova E, Kachar B, Ornitz DM, Thalmann I (2001) Development and maintenance of otoconia: biochemical considerations. Ann N Y Acad Sci 942:162–178 23. White JA, Coale KD, Catalano PJ, Oas JG (2005) Diagnosis and management of lateral semicircular canal benign paroxysmal positional vertigo. Otolaryngol Head Neck Surg 133:278–284 24. Kim JH, Jung EJ, Song CE, Song MH, Park KC, Ko KM, Shim DB (2013) Risk factors for treatment failure in benign paroxysmal positional vertigo. Korean J Otorhinolaryngol-Head Neck Surg 56:74–78 25. Shigeno K, Ogita H, Funabiki K (2012) Benign paroxysmal positional vertigo and head position during sleep. J Vestib Res 22:197–203 26. Li S, Tian L, Han Z, Wang J (2013) Impact of postmaneuver sleep position on recurrence of benign paroxysmal positional
J Neurol vertigo. PLoS ONE 8(12):e83566. doi:10.1371/journal.pone. 0083566 27. Shoman N, Longridge N (2007) Cerebellar vermis lesions and tumours of the fourth ventricle in patients with positional and positioning vertigo and nystagmus. J Laryngol Otol 121:166–169
28. Shim DB, Song CE, Baek SJ, Song MH (2012) A case of isolated cerebellar hemorrhage presenting as vestibular neuritis combined with contralateral benign paroxysmal positional vertigo. Otolaryngol Head Neck Surg 146:865–867
123
ORIGINAL COMMUNICATION
Natural history of horizontal canal benign paroxysmal positional vertigo is truly short Dae Bo Shim • Kyung Min Ko • Joon Hee Lee Hong Ju Park • Mee Hyun Song
•
Received: 30 June 2014 / Revised: 24 September 2014 / Accepted: 25 September 2014 Springer-Verlag Berlin Heidelberg 2014
Abstract The objective of the study is to characterize the natural course of positional vertigo and nystagmus in patients with horizontal canal benign paroxysmal positional vertigo (h-BPPV) and to analyze the difference in the natural course between the two variants of h-BPPV. We conducted a prospective study in 106 patients with geotropic type h-BPPV [h-BPPV (Geo)] (n = 43) and apogeotropic type h-BPPV [h-BPPV (Apo)] (n = 63) who agreed and signed the written informed consent of no treatment. All patients were asked to answer a detailed interview about the onset time of positional vertigo and to visit the hospital every 1–3 days. At every visit, they were interviewed about cessation time of positional vertigo and positional nystagmus was assessed. The mean period ± SD between the onset and remission of vertigo in the h-BPPV (Geo) was 6.7 ± 6.3 days, whereas that in the h-BPPV (Apo) was 3.7 ± 4.1 days. In addition, the mean period ± SD from the initial diagnosis to the disappearance of positional nystagmus in the h-BPPV (Geo) was 4.7 ± 3.9 days, whereas that in the h-BPPV (Apo) was 4.4 ± 5.0 days. Although the duration until natural remission of positional nystagmus did not differ between the two variants of h-BPPV, the remission of vertigo occurred faster in h-BPPV (Apo) than h-BPPV (Geo) (p \ 0.05). The natural course of h-BPPV is much shorter than that indicated in previous reports. The positional D. B. Shim K. M. Ko J. H. Lee M. H. Song (&) Department of Otorhinolaryngology, Myongji Hospital, 697-24 Hwajung-dong, Deokyang-gu, Goyang, Gyeonggi 412-270, Korea e-mail: [email protected] H. J. Park Department of Otolaryngology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
vertigo disappeared faster in the h-BPPV (Apo) compared to the h-BPPV (Geo) unlike the positional nystagmus. Keywords Benign paroxysmal positional vertigo Semicircular canal Natural course Physiopathology
Introduction Benign paroxysmal positional vertigo (BPPV) is the most common vestibular disorder. The resolution rates of BPPV following specific treatments are very high but spontaneous recovery may also occur [1]. According to the clinical practice guideline provided by the American Academy of Otolaryngology-Head and Neck Surgery (AAO-HNS), clinicians are recommended to treat posterior canal BPPV (p-BPPV) with the particle repositioning maneuver [2]. Various types of the roll maneuver have been reported to be effective in approximately 75 % of the patient for treating horizontal canal BPPV (h-BPPV), although existing data are limited [3–7]. However, observation or ‘‘watchful waiting’’ is considered a therapeutic option to manage both types of BPPV, according to the guidelines [2]. The potential benefits of observation would be that symptoms or discomforts provoked by the therapeutic maneuvers can be avoided and that medical expenses can be saved from decreased referral rates. Recent studies have reported high rates of spontaneous resolution in BPPV, although the reported rates vary widely [8–13]. Some authors have proposed that spontaneous resolution occurs faster in h-BPPV compared to that of p-BPPV, but there is no difference in the natural course between the two h-BPPV variants [14]. The variability concerning the resolution rates of BPPV in previous case– control studies may be due to the differences in the follow-
123
J Neurol
up duration. Furthermore, the follow-up interval in previous studies was longer than 4 weeks, indicating that the short-term resolution rates of BPPV are unknown [8–11, 15]. Another limitation of several recently reported longitudinal follow-up studies is that only subjective symptoms were included as outcome measures for resolution without objective data [13, 14, 16]. Therefore, we attempted to identify the natural course of the geotropic and apogeotropic type variants (h-BPPV (Geo) and h-BPPV (Apo), respectively) of h-BPPV through short-interval follow-up. Objective methods as well as subjective symptoms were used as the outcome measures for resolution. We also analyzed the difference in the natural course between the two h-BPPV variants.
Materials and methods Subjects A longitudinal follow-up study was conducted on 106 patients without a trauma history or concomitant neurootologic disease who were diagnosed with h-BPPV and agreed to sign the written informed consent of no treatment from January 2011 to December 2012 at the Department of Otorhinolaryngology, Myongji Hospital. BPPV was diagnosed when characteristic nystagmus was demonstrated combined with typical symptoms of positional vertigo during the supine head roll test using video Frenzel goggle system (SLMED, Seoul, Korea). In all subjects, there were no identifiable central nervous system disorders that could explain the positional vertigo and nystagmus in neurotologic examinations including spontaneous and gaze-evoked nystagmus, smooth pursuit and saccades, limb ataxia, and balance function in addition to routine neurologic examinations. The provocation test method and the diagnostic criteria for BPPV followed the guidelines provided by the AAO-HNS [2]. The h-BPPV subtypes were determined according to the nystagmus evoked as follows: •
•
h-BPPV (Geo): horizontal direction-changing geotropic nystagmus. The affected ear is identified by the head lateral position that evokes the more intense nystagmus during the supine head roll test (e.g. right ear affected when nystagmus is stronger in the right lateral head turning position). h-BPPV (Apo): horizontal direction-changing apogeotropic nystagmus. The affected ear is identified by the head lateral position that evokes the lesser intense nystagmus during the supine head roll test (e.g. right ear affected when nystagmus is stronger in the left lateral head turning position).
123
Study design All patients were required to revisit the hospital at least every 1–3 days after the initial visit. The patients were asked about the onset time of positional vertigo before visiting our hospital through a detailed interview at the initial visit. At every visit, an interview and examination using the supine head roll test were conducted. When the positional nystagmus disappeared, patients were asked to indicate the exact time at which the positional vertigo disappeared. In addition, the conversion between the two subtypes of h-BPPV was checked using the supine head roll test at every visit. The patients were not given any specific instructions that could affect the remission of disease after the initial diagnosis. A questionnaire asking about sleep position was given to all patients at the first visit and at the time of disappearance of positional vertigo or nystagmus to identify the potential therapeutic effect of forced prolonged position. Written informed consent was obtained from all patients who were enrolled in this study after explaining the detailed pros and cons of both treatment options including receiving therapeutic maneuvers and observation with no treatment. Statistical analysis The comparison between the characteristics of the two h-BPPV subtypes was analyzed with the Mann–Whitney U test. Residual rates of positional vertigo and nystagmus were calculated with the Kaplan–Meier method, and the differences between the two subtypes of h-BPPV in remission curves were analyzed using the log-rank test. All results were considered significant when the p value was \0.05.
Results h-BPPV (Geo) was diagnosed in 43 patients (40.6 %) and h-BPPV (Apo) in 63 patients (59.4 %). The demographic data of our study is presented in Table 1. No significant difference in age or sex was observed between the two subtypes of h-BPPV. Table 2 demonstrates the natural courses of positional nystagmus and vertigo in h-BPPV and both subtypes of h-BPPV. The mean duration from the onset of positional vertigo to the initial visit to our clinic was 2.0 days for h-BPPV, and 3.0 and 1.4 days for h-BPPV (Geo) and h-BPPV (Apo), respectively. The difference of duration between the two subtypes of h-BPPV was significant (p \ 0.05). The average value from the initial diagnosis to the remission of positional nystagmus was 4.5 days, and that value from the
J Neurol Table 1 Clinical and demographic characteristics h-BPPV (Geo) (n = 43)
h-BPPV (Apo) (n = 63)
Age (years) Range
23–81
25–80
Mean ± SD
52.0 ± 13.0
55.2 ± 11.6
Male
9
14
Female
34
49
Sex (numbers)
Affected side (numbers) Right
19
43
Left
24
20
h-BPPV horizontal semicircular canal benign paroxysmal positional vertigo, h-BPPV (Geo) geotropic variant of horizontal semicircular canal benign paroxysmal positional vertigo, h-BPPV (Apo) apogeotropic variant of horizontal semicircular canal benign paroxysmal positional vertigo
onset to the disappearance of positional vertigo was 4.9 days in h-BPPV. When comparing the natural courses between positional nystagmus and vertigo after the initial diagnosis for each variant of h-BPPV, the mean period of positional vertigo was more than 1 day shorter than that of positional nystagmus in both subtypes of h-BPPV (Table 2). However, statistically significant difference was shown for h-BPPV (Apo) only in the duration of remission between the two outcome measures (p = 0.001) (Fig. 1). When analyzing the differences in the natural courses between the two subtypes of h-BPPV, no significant difference was observed between the two subtypes in the remission of positional nystagmus after the initial diagnosis (Fig. 2). However, the remission of positional vertigo after the initial diagnosis as well as after the onset of symptoms in h-BPPV (Apo) was faster than that in h-BPPV (Geo) (p \ 0.05) (Fig. 3). Of 106 patients with h-BPPV, only 7 patients (6.6 %) slept on the contralesional side after the initial diagnosis.
The proportion of the patients who slept on the contralesional side were 7.0 % (3/43 patients) and 6.3 % (4/63 patients) in h-BPPV (Geo) and h-BPPV (Apo), respectively, which did not differ statistically between the two subtypes. Conversion between the two subtypes of h-BPPV was identified in 21 patients (19.8 %). Conversion from h-BPPV (Apo) to h-BPPV (Geo) was observed in 16 patients (25.4 %), whereas the conversion from h-BPPV (Geo) to h-BPPV (Apo) was seen in 5 patients (11.6 %).
Discussion This study demonstrated that the natural course of h-BPPV was very short regarding the objective findings (positional nystagmus) as well as in the subjective symptoms (positional vertigo) using a longitudinal study design. In the present study, the average and median values of duration from the initial onset to the remission of positional vertigo in patients with h-BPPV (Apo) were 3.7 and 2.0, respectively, whereas those in patients with h-BPPV (Geo) were 6.7 and 4.0, respectively. These results are very interesting findings, considering that the mean duration of h-BPPV (Apo) and h-BPPV (Geo) without treatment were previously reported as 16 and 13 days, respectively [13, 16]. A variety of studies have referred to high resolution rates without specific therapeutic maneuver in patients with BPPV and a longitudinal study by Sekine et al. [14] reported that the natural history of h-BPPV was shorter than that of p-BPPV although the exact mean duration of positional vertigo was not presented [13, 16]. However, the previous studies had some limitations in that they had long follow-up intervals usually of more than 2 weeks and that the outcome measures were dependent on the patients’ subjective memory about the time at which their symptoms disappeared. Therefore, to overcome these limitations, the present study was designed to include direct examination
Table 2 The natural courses of positional nystagmus and vertigo in h-BPPV and two subtypes of h-BPPV h-BPPV (n = 106)
Onseta (days)
h-BPPV (Geo) (n = 43)
h-BPPV (Apo) (n = 63)
Mean ± SD
Median
Mean ± SD
Median
Mean ± SD
Median
2.0 ± 3.2
1.0
3.0 ± 3.9
1.0
1.4 ± 2.4
0.0
p value
0.008
Duration of remission (days) Positional nystagmus
4.5 ± 4.5
3.0
4.7 ± 3.9
3.0
4.4 ± 5.0
3.0
0.358
Positional symptom
2.9 ± 3.5
2.0
3.7 ± 4.1
2.0
2.3 ± 2.9
1.0
0.032
Total symptomb
4.9 ± 5.3
3.0
6.7 ± 6.3
4.0
3.7 ± 4.1
2.0
0.008
a
Onset means duration of the symptom until visiting the clinic
b
Total symptom means the duration from the onset until remission of positional symptom
c
Statistical analysis: the comparison between the characteristics of the two subtypes of horizontal canal benign paroxysmal positional vertigo and the p values were computed using the Mann–Whitney U test
123
J Neurol
Fig. 1 Comparison between positional nystagmus and symptoms in the two subtypes of horizontal canal benign paroxysmal positional vertigo (h-BPPV). a No difference was observed between positional nystagmus and vertigo in patients with geotropic type of h-BPPV
(p = 0.228). b A significant difference was observed between positional nystagmus and vertigo in patients with apogeotropic type of h-BPPV (p = 0.001)
Fig. 2 Comparison between the subtypes of horizontal canal benign paroxysmal positional vertigo in the remission from the initial diagnosis to the disappearance of positional nystagmus. a No significant difference was observed between the two subtypes
analyzed by Mann–Whitney U test. b Kaplan–Meier curve with a log-rank test also shows no difference between the two subtypes (p = 0.671)
Fig. 3 Comparison between the subtypes of horizontal canal benign paroxysmal positional vertigo in the remission from the initial diagnosis to the remission of positional vertigo. A significant difference was observed between the two subtypes in the time
courses of vertigo remission a after the initial diagnosis (p = 0.032) and b after the onset of symptoms (p = 0.003) using Kaplan–Meier curve with a log-rank test
123
J Neurol
about the objective nystagmus as well as subjective symptoms with a short follow-up interval. The theoretical hypothesis for the short natural course of h-BPPV could be different for each subtype. In h-BPPV (Geo), the short natural course of h-BPPV (Geo) has been reported to be related to the anatomical position of the horizontal semicircular canal (HC). As the anterior cupular end of the HC is anatomically elevated about 20 degrees from the horizontal plane [17], otoconia within the posterior arm of the HC can theoretically be repositioned back into the utricle possibly by head movements of daily life (e.g. walking) without specific therapeutic maneuvers [13, 14]. The faster symptom remission in h-BPPV (Apo) compared to that in h-BPPV (Geo) suggests that the utricular type of cupulolithiasis may be the predominant pathology underlying h-BPPV (Apo) rather than either the canal type of cupulolithiasis or the presence of free-floating otoconia in the anterior arm of the HC, which is in contrast to the previous reports [5, 6, 18]. If the otoconia is firmly attached to the canal side of the cupula or is freely floating in the anterior arm of the HC in h-BPPV (Apo) as in previous reports, symptom duration should theoretically be longer than h-BPPV (Geo) because the otoconia needs to pass through the posterior arm and the isthmic portion of the HC in order to return to the utricle. However, in the case of the utricular type of cupulolithiasis where the otoconia are attached to the utricular side of the cupula, the pathway to the utricle is very short, which could lead to prompt spontaneous remission of symptoms. Therefore, the short natural course of h-BPPV (Apo) may be explained by the location of the otoconia, which is presumed to be the utricular side of cupula in most cases. Another finding to support the higher incidence of utricular side cupulolithiasis in h-BPPV (Apo) is the low conversion rate (25.4 %) from h-BPPV (Apo) to h-BPPV (Geo) in the course of spontaneous resolution. In a previous study, we have already suggested similar results that the utricular type of cupulolithiais in h-BPPV (Apo) is more common compared to the other two types [19]. In addition to these anatomical factors, spontaneous dissolution of otoconia could be another factor to explain for the short natural course of BPPV as reported previously in several studies [13, 20–22]. Although no significant difference was observed in the remission period of positional nystagmus between the two subtypes, the atypical cases (8/63 patients) of h-BPPV (Apo) demonstrated very long duration of nystagmus of up to 31 days as shown in Fig. 2. Most of these patients showed conversion from h-BPPV (Apo) to h-BPPV (Geo) during the natural course except for two cases. It is postulated that a longer period was needed in these atypical cases for the otoconia to return from the anterior arm of the HC to the utricle, or to return to the utricle after dislodging from the canal side of the cupula. There are numerous
previous studies reporting that cure rate of h-BPPV (Apo) is far lower than that of p-BPPV or h-BPPV (Geo) in contrast to the results of this study [6, 23, 24]. The discrepancy of results among different studies may be associated with the limitation of accurate lateralization methods in the diagnosis of h-BPPV. We checked the sleep position to identify the potential therapeutic effect of forced prolonged position and only seven (6.6 %) out of 106 patients were found to sleep on the contralesional side. The sleep position toward the contralesional side was observed in 7.0 % (3/43 patients) and 6.3 % (4/63 patients) in the h-BPPV (Geo) and h-BPPV (Apo), respectively. Many authors have reported that patients with BPPV have a tendency to sleep with their head to the contralesional side, which may affect the treatment outcome [25, 26]. However, this tendency was observed in only a small proportion of patients in our study, suggesting that the sleep position did not seem to have a significant effect on our results. In this study, only the positional vertigo showed statistically significant difference, while no significant difference was found for the duration of positional nystagmus between the two subtypes of h-BPPV. According to a study about physiomathematical models of BPPV, a greater number of otoconia are required to induce positional vertigo in cupulolithiasis compared to canalolithiasis; 490 otoconia for cupulolithiasis and 62 for canalithiasis [21]. This result indicates that repositioning of fewer otoconia can relieve positional vertigo in cupulolithiasis compared to canalithiasis theoretically, assuming that the same number of otoconia is detached from utricle and also returned to the utricle spontaneously. There are some limitations of this study. First, our results may have potential biases due to the effect of the short interval follow-up on the natural course of h-BPPV. Frequent examination with the positional test can lead to rapid remission of positional nystagmus by the potential therapeutic effect of the diagnostic roll maneuver. Emotional support by frequent consultation with a doctor may have also influenced symptom duration. However, we believe that these effects are probably minimal as no objective evidence to support the therapeutic effects of frequent diagnostic positional test and interview in patients with BPPV has been reported. Another limitation is the difference in onset duration between the two subtypes of h-BPPV. Such a difference was caused by the clinical features of h-BPPV (Apo) exhibiting short latency and long duration of positional nystagmus leading to more severe symptoms than h-BPPV (Geo) caused by minimal movements. To overcome this limitation, the remission time of positional nystagmus as well as symptoms after the initial diagnosis were compared in this study.
123
J Neurol
Based on the results of the present study, watchful waiting might be an important therapeutic option in the treatment of h-BPPV. However, considering that central lesions can also lead to positional vertigo or nystagmus commonly of the apogeotropic type, clinicians should rule out the central causes of positional vertigo and nystagmus before recommending observational therapy to patients [27, 28].
Conclusion The natural course of h-BPPV is much shorter than that reported in previous studies. Although no significant difference in nystagmus remission was observed between the two subtypes of h-BPPV, the natural course of h-BPPV (Apo) was shorter than that of h-BPPV (Geo) regarding the resolution of subjective symptoms. This information may provide clues about the pathophysiology of h-BPPV and also be used clinically by healthcare professionals treating patients who are unwilling to receive the repositioning maneuver for h-BPPV. Acknowledgments The authors thank Dr. Myung-Whan Suh at Seoul National University College of Medicine, for critical review of this manuscript. Conflicts of interest
None.
Ethical standard This study was approved by the Institutional Review Board of Myongji Hospital and informed consent was obtained from all patients. The study has been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki.
References 1. Lee SH, Kim JS (2010) Benign paroxysmal positional vertigo. J Clin Neurol 6:51–63 2. Bhattacharyya N, Baugh RF, Orvidas L, Barrs D, Bronston LJ, Cass S, Chalian AA, Desmond AL, Earll JM, Fife TD, Fuller DC, Judge JO, Mann NR, Rosenfeld RM, Schuring LT, Steiner RW, Whitney SL, Haidari J, American Academy of O-H, Neck Surgery F (2008) Clinical practice guideline: benign paroxysmal positional vertigo. Otolaryngol Head Neck Surg 139:S47–S81 3. Lempert T, Tiel-Wilck K (1996) A positional maneuver for treatment of horizontal-canal benign positional vertigo. Laryngoscope 106:476–478 4. Fife TD (1998) Recognition and management of horizontal canal benign positional vertigo. Am J Otol 19:345–351 5. Nuti D, Agus G, Barbieri MT, Passali D (1998) The management of horizontal-canal paroxysmal positional vertigo. Acta Otolaryngol 118:455–460 6. Casani AP, Vannucci G, Fattori B, Berrettini S (2002) The treatment of horizontal canal positional vertigo: our experience in 66 cases. Laryngoscope 112:172–178 7. Tirelli G, Russolo M (2004) 360-Degree canalith repositioning procedure for the horizontal canal. Otolaryngol Head Neck Surg 131:740–746
123
8. Blakley BW (1994) A randomized, controlled assessment of the canalith repositioning maneuver. Otolaryngol Head Neck Surg 110:391–396 9. Lynn S, Pool A, Rose D, Brey R, Suman V (1995) Randomized trial of the canalith repositioning procedure. Otolaryngol Head Neck Surg 113:712–720 10. Asawavichianginda S, Isipradit P, Snidvongs K, Supiyaphun P (2000) Canalith repositioning for benign paroxysmal positional vertigo: a randomized, controlled trial. Ear Nose Throat J 79(732–734):736–737 11. Froehling DA, Bowen JM, Mohr DN, Brey RH, Beatty CW, Wollan PC, Silverstein MD (2000) The canalith repositioning procedure for the treatment of benign paroxysmal positional vertigo: a randomized controlled trial. Mayo Clin Proc 75:695–700 12. Yimtae K, Srirompotong S, Srirompotong S, Sae-Seaw P (2003) A randomized trial of the canalith repositioning procedure. Laryngoscope 113:828–832 13. Imai T, Ito M, Takeda N, Uno A, Matsunaga T, Sekine K, Kubo T (2005) Natural course of the remission of vertigo in patients with benign paroxysmal positional vertigo. Neurology 64:920–921 14. Sekine K, Imai T, Sato G, Ito M, Takeda N (2006) Natural history of benign paroxysmal positional vertigo and efficacy of Epley and Lempert maneuvers. Otolaryngol Head Neck Surg 135:529–533 15. Woodworth BA, Gillespie MB, Lambert PR (2004) The canalith repositioning procedure for benign positional vertigo: a metaanalysis. Laryngoscope 114:1143–1146 16. Imai T, Takeda N, Ito M, Inohara H (2011) Natural course of positional vertigo in patients with apogeotropic variant of horizontal canal benign paroxysmal positional vertigo. Auris Nasus Larynx 38:2–5 17. Della Santina CC, Potyagaylo V, Migliaccio AA, Minor LB, Carey JP (2005) Orientation of human semicircular canals measured by three-dimensional multiplanar CT reconstruction. J Assoc Res Otolaryngol 6:191–206 18. Baloh RW, Jacobson K, Honrubia V (1993) Horizontal semicircular canal variant of benign positional vertigo. Neurology 43:2542–2549 19. Shim DB, Kim JH, Park KC, Song MH, Park HJ (2012) Correlation between the head-lying side during sleep and the affected side by benign paroxysmal positional vertigo involving the posterior or horizontal semicircular canal. Laryngoscope 122:873–876 20. Zucca G, Valli S, Valli P, Perin P, Mira E (1998) Why do benign paroxysmal positional vertigo episodes recover spontaneously? J Vestib Res 8:325–329 21. House MG, Honrubia V (2003) Theoretical models for the mechanisms of benign paroxysmal positional vertigo. Audiol Neurootol 8:91–99 22. Thalmann R, Ignatova E, Kachar B, Ornitz DM, Thalmann I (2001) Development and maintenance of otoconia: biochemical considerations. Ann N Y Acad Sci 942:162–178 23. White JA, Coale KD, Catalano PJ, Oas JG (2005) Diagnosis and management of lateral semicircular canal benign paroxysmal positional vertigo. Otolaryngol Head Neck Surg 133:278–284 24. Kim JH, Jung EJ, Song CE, Song MH, Park KC, Ko KM, Shim DB (2013) Risk factors for treatment failure in benign paroxysmal positional vertigo. Korean J Otorhinolaryngol-Head Neck Surg 56:74–78 25. Shigeno K, Ogita H, Funabiki K (2012) Benign paroxysmal positional vertigo and head position during sleep. J Vestib Res 22:197–203 26. Li S, Tian L, Han Z, Wang J (2013) Impact of postmaneuver sleep position on recurrence of benign paroxysmal positional
J Neurol vertigo. PLoS ONE 8(12):e83566. doi:10.1371/journal.pone. 0083566 27. Shoman N, Longridge N (2007) Cerebellar vermis lesions and tumours of the fourth ventricle in patients with positional and positioning vertigo and nystagmus. J Laryngol Otol 121:166–169
28. Shim DB, Song CE, Baek SJ, Song MH (2012) A case of isolated cerebellar hemorrhage presenting as vestibular neuritis combined with contralateral benign paroxysmal positional vertigo. Otolaryngol Head Neck Surg 146:865–867
123
